Kaplan’s Principles of

Plant Morphology
Kaplan’s Principles of
Plant Morphology
Donald R. Kaplan

Edited and Compiled by

Chelsea D. Specht
CRC Press
First edition published 2022
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Contents

Preface................................................................................................................................................................................................... vii
Acknowledgments....................................................................................................................................................................................ix
Authors.....................................................................................................................................................................................................xi

1. Introduction to the Science of Plant Morphology: Goals and Concepts...................................................................................1

2. The Cast of Characters: A Review of the Plant Kingdom and Its

Major Representatives.................................................................................................................................................................. 11

3. The Relationship between Morphology and Anatomy in Plants..............................................................................................43

4. Plant Embryogenesis: The Origin of Morphological Organization during Development.....................................................71

5. Early Plant Development: From Seed to Seedling to Established Plant............................................................................... 105

6. Divergent Patterns of Seedling Development and Their Significance for the Interpretation
of Plant Ontogeny and Evolution............................................................................................................................................... 133

7. Phyllotaxis.................................................................................................................................................................................... 159

8. The Concept of Differential Growth......................................................................................................................................... 183

9. The Effect of Internodal Elongation on Shoot Form............................................................................................................... 191

10. The Effect of Stem Thickening Growth on Shoot Form.......................................................................................................... 213

11. Shoot Lateral Symmetry............................................................................................................................................................243

12. Shoot Branching..........................................................................................................................................................................279

13. Developmental Expressions and Specializations of Shoot Branches.....................................................................................309

14. Leaf Morphology and Development.......................................................................................................................................... 335

15. Transectional Symmetry of Leaves...........................................................................................................................................367

16. Longitudinal Symmetry and Zonation of Leaves Part I: Leaf Zones...................................................................................387

17. Longitudinal Symmetry and Zonation of Leaves Part II: Blade Dissection......................................................................... 433

18. Specializations in Leaf Structure and Function......................................................................................................................503

19. Morphology of Reproductive Shoots I: Pteridophytes............................................................................................................585

20. Morphology of Reproductive Shoots II: Gymnosperms.........................................................................................................777

21. Morphology of Reproductive Shoots III: The Angiosperms

A. The Floral Shoot................................................................................................................................................................... 1067

v
vi Contents

22. Morphology of Reproductive Shoots III: The Angiosperms

B. The Floral Organs in Their Pre- and Post-Fertilization States....................................................................................... 1109

23. Morphology of Reproductive Shoots III: The Angiosperms

C. Inflorescence Morphology................................................................................................................................................... 1167

24. Principles of Root Morphology................................................................................................................................................ 1215

References.......................................................................................................................................................................................... 1253
Index................................................................................................................................................................................................... 1281
Preface

Kaplan’s Principles of Plant Morphology defines the field of plant morphology are being brought into studies of crop develop-
plant morphology, providing resources, examples, and theoretical ment, biodiversity, and adaptive responses to climate change, and
constructs that illuminate the foundations of plant morphology increasingly researchers are turning to historic texts to uncover
and clearly outline the importance of integrating a fundamen- research, data, and interpretations concerning plant morphology
tal understanding of plant morphology into modern research and the evolution and diversification of plant form and function;
in plant genetics, development, and physiology. As research on there is great need for a modern reference and textbook that high-
developmental genetics and plant evolution emerges, an under- lights past studies and provides the synthesis of data necessary
standing of plant morphology is essential to interpret develop- to drive our future research in plant morphological and develop-
mental, anatomical, and morphological data. The principles of mental evolution.

vii
Acknowledgments

While I can here recognize the many people who have made book a much more refined product while staying true to Don’s
the final stages of publication of this book possible, this does vision and voice, and I thank all the reviewers who contributed
not fully acknowledge those who supported and influenced Don their time and energy to this project. Among these, I especially
Kaplan during the writing of these chapters. I do know that Don thank Jim Seago for advice, critical feedback, and encourage-
would have thanked his students; all of them. Especially the ment; and Dennis Wm. Stevenson for providing substantial
students who sat in his classroom and experienced his lectures amounts of time, effort, and knowledge of all things plant mor-
delivered with lantern slides and/or slide carousels that were phology. In addition, Dennis was essential in helping me track
occasionally (and famously) dropped and scattered right before down figures, references, and citations, especially the most eso-
class began, for these students were the inspiration for this book. teric ones.
The text and extensive figures of this book served as the pri- The editing, revision, and publication of this book would
mary reading material for C107, Kaplan’s Principles of Plant not have been possible without the herculean efforts of Charles
Morphology at UC Berkeley, typically printed out in five vol- R. Crumly: Chuck’s enthusiasm for this project as well as his
umes from Odin Readers. I believe Don would have thanked the patience, persistence, ingenuity, flexibility, and expertise were all
staff at Odin for printing out copies, year after year, with annual tested time and time again, and each time he rose over barriers to
additions and modifications that were always geared toward build the momentum necessary to drive this project to comple-
making the text more instructive and valuable for his students. tion. This book is in your hands today because of his unwaver-
Don also would have thanked his graduate students and col- ing faith in and commitment to the final product. In addition,
leagues who are cited throughout the text for providing exam- Dorothy Kaplan provided resources, encouragement, and posi-
ples and exemplars of morphological patterns and processes so tive reinforcement every step of the way: And while this publica-
critical to his interpretations of fundamental principles. I also tion has taken much longer than planned, she’s never given up
know he would have thanked his wife, Dorothy, for her unwav- hope that her grandchildren will get to experience their grandfa-
ering support and his two sons, Andrew and Tim, for enriching ther’s work. I thank Chuck and Dorothy for everything they’ve
his life within and beyond academia. Don’s family has contin- done to keep this production on track, for trusting me with their
ued to foster his legacy between the time of his passing and the visions for this book, and for making me feel like part of their
publication of this book, supporting the establishment of the families in the process.
Donald R. Kaplan Memorial Lecture in Plant Morphology and Finally, I thank Ioana Anghel and Maria Pinilla Vargas who
fully endowing the Kaplan Dissertation Award in Comparative both helped extensively with references, figure captions, and edit-
Morphology, a major source of funding for independent gradu- ing; and I thank the entire production team at Taylor & Francis,
ate student research administered through the Botanical Society especially Becky Hainz-Baxter and Elizabeth King, who worked
of America. tirelessly in processing words, figures, legends, and references
For my part, I sincerely thank Raymund Chan and Michael and were always patient yet exacting in assisting me in complet-
L. Christianson who, as students and colleagues of Don Kaplan, ing this project.
provided inspiration and moral support early on to continue this This book is dedicated to the memory of Donald R. Kaplan,
project and honor Don’s legacy. They as well as the other schol- and to his sons and grandchildren who know and understand the
ars who reviewed and commented on various chapters made this weight of his work.

ix
Authors

Donald Robert Kaplan, PhD, w  as born in Chicago on January In addition to botany, Dr. Kaplan had many other interests,
17, 1938. He attended Northwestern University and graduated which he pursued with as much intensity and innovation as he
Phi Beta Kappa with a bachelor’s degree in biology in 1960. He did plant morphology. Among them were photography, railroads,
studied with Adriance Foster at UC Berkeley where he earned his classical music, and movies. He shared these passions with his
PhD in 1965. After completing a National Science Foundation- wife, Dorothy, and sons Andrew and Timothy.
sponsored postdoctoral fellowship at the Royal Botanic Gardens,
Kew, England, Dr. Kaplan became a founding member of the Chelsea Dvorak Specht, PhD,  was born in Wilmington,
newly established University of California, Irvine campus as an Delaware on September 13, 1971. She attended the University
assistant professor of organismic biology in 1965. He returned to of Delaware earning a BA. in biology magna cum laude and
UC Berkeley in 1968 as an associate professor in the Department Phi Beta Kappa in 1993. Initially planning on pursuing medi-
of Botany. Dr. Kaplan was promoted to professor in 1978, and cine, her undergraduate mentor Kenneth A. Campbell provided
moved to the Department of Plant and Microbial Biology during her first taste in academic research, changing her life forever.
reorganization of the biological sciences. He retired in 2004. Dr. Specht earned her MS in 1997 and PhD in 2004 from New
As a plant morphologist, Dr. Kaplan had a unique, European York University, during which time she was a Fulbright Fellow
perspective on plant form. Using key concepts and first princi- and worked for 2 years as a Program Officer and Ecoregional
ples, he approached his research in a strictly analytical way. He Coordinator for the World Wildlife Fund in Bolivia. Dr. Specht
was most interested in fundamental structural and developmental was part of an NSF-funded joint program between NYU and the
commonalities that underpin plant form across different major New York Botanical Garden and studied extensively with plant
taxa. Dr. Kaplan’s publications spanned the algae, bryophytes, morphologist and renowned botanist and cladist Dennis Wm.
ferns, gymnosperms, and angiosperms. Dr. Kaplan’s research Stevenson as her major advisor.
and theories on the relationship of cell and organism in vascular It was during her graduate training that Dr. Specht developed
plants have had a major impact on studies linking plant morphol- an appreciation for the principles of plant morphology combined
ogy with molecular biology/genetics, setting the stage for modern with a developmental genetic and phylogenetic perspective to
investigations on plant form and function. Dr. Kaplan was also investigate the mechanisms underlying the evolution and diver-
interested in the history of plant morphology, especially in those sification of plant form and function. Following a postdoctoral
who established the basic principles and concepts of the field as fellowship at the Smithsonian Institution’s National Museum
he practiced it, e.g. Goethe, Hofmeister, Goebel, and Troll. of Natural History, Dr. Specht became an Assistant Professor
Dr. Kaplan’s research accomplishments were well recognized and Plant Organismal Biologist in the Department of Plant and
by his peers and resulted in many awards. Among these were Microbial Biology at UC Berkeley and curator of Monocots for
the Alexander von Humboldt Distinguished Senior U.S. Scientist the University and Jepson Herbaria in 2005. At UC Berkeley
Award (1988-89), a Guggenheim Fellowship (1987–88), fellow of she taught Kaplan’s Plant Morphology course and used this
the California Academy of Sciences (1982), the Botanical Society book for many years in the form of five massive readers for the
Merit Award (1984), the Botanical Society of America’s Jeanette class. In 2017, she moved to Cornell University as the Barbara
Siron Pelton Award (1989) and Centennial Award (2006), and McClintock Professor in Plant Biology and is currently also
a Miller Research Professorship (1975–76). He was also recog- Associate Dean for Diversity and Inclusion for the College of
nized for his excellence in teaching with a Sigma Xi National Agriculture and Life Sciences. Dr. Specht is married to ento-
Lecturer Award (1995–97), the UC Berkeley Distinguished mologist Patrick O’Grady and shares her love of plants with their
Teaching Award (1976) and the Botanical Society of America’s daughter, Paceyn Julia.
Charles Edwin Bessey Award for excellence in botanical teach-
ing (2005).

xi
1
Introduction to the Science of Plant Morphology:
Goals and Concepts

CONTENTS
Examples of Higher Plant Structural Diversity and Life Forms...............................................................................................................1
Basic Organization of the Higher Plant Body...........................................................................................................................................4
The Shoot System................................................................................................................................................................................4
The Root System..................................................................................................................................................................................5
The Concept of Homology........................................................................................................................................................................5
Homology Criteria...............................................................................................................................................................................6
The Concepts of Analogy versus Homology.....................................................................................................................................10

Have you ever wondered as you stroll through a forest how the the range of their morphological expression. Once you have
many varieties of plants are related to one another? How does a acquired the ability to analyze plant morphology, we will apply
herb differ from a tree or what gives a vine its distinctive climb- these principles to plants that grow in particular kinds of habitats
ing characteristics? Are they radically different kinds of plants to see how form relates to function.
or do they share some common features? Questions such as these Before we delve into the specifics of how plants are con-
are addressed by the science of plant morphology. structed, let’s look at some biologically interesting examples of
The science of plant morphology deals with the external form the kinds of plants we are going to learn to analyze. While at first
of plants. The word morphology comes from the Greek words glance these species may seem simply weird and unrelated to
morphos meaning shape and logos meaning discourse. Since your experience, by the time we come to consider them as indi-
plant morphology is concerned principally with the structure and vidual vegetation types, you will see how even the most extreme
variation of the major plant organs (leaf, stem, and root), another representatives are related structurally to more conventional
term for its study is organography. In terms of the equivalent plant species that you are familiar with.
level of study of animals, plant morphology is comparable to
animal anatomy, whereas plant anatomy, which is concerned
with the cell to tissue levels of organization, is equivalent to ani-
mal histology. In this book our emphasis will be on the mac- Examples of Higher Plant Structural
roscopic aspects of plant structure, or what we can see largely
Diversity and Life Forms
with the unaided eye. We will make occasional excursions into
the microscopic structure of plants, but only to analyze the ori- Among the most distinctive plant types are epiphytes, plants that
gin and development of organs and organ components and where grow on the surfaces of other plants (the term epiphyte comes from
histology can tell us something about the status and function of Greek root words epi meaning upon and phyte meaning plant).
a particular organ type. True epiphytes spend their entire lives up away from the earth’s
All vascular plants (also known as tracheophytes) appear to be surface typically on one of the aerial branches of a forest tree or
built on the same fundamental organizational theme or ground on the surfaces of some other elevated plant. In Figure 1.1, we see
plan. Thus the vast majority of structural variants that we find two epiphytic species which are members of the pineapple fam-
occupying the many different habitats on earth today are simply ily, Bromeliaceae. Interestingly, taxonomically, they are both in
variations on this basic theme. A fundamental goal of the sci- the genus Tillandsia L. Tillandsia fasciculata Sw. has an upright
ence of plant morphology is to deduce this basic organizational shoot system, whereas, T. usneoides L., the well-known Spanish
theme from broad, comparative studies and to determine how moss, has a highly branched shoot system that hangs down, form-
variants come about through differences in plant growth and ing an intertwining reticulum in the air. For both these epiphytes
development. the particular environment in which they grow is a harsh one com-
The principal goals of this text are: 1) to teach the reader how pared to life on the ground below. While they may be in an advan-
to analyze the basic structural features of plants that are altered tageous position with regard to incident light in the forest, such
to produce the major variations in plant form and 2) to determine an aerial growth site is very poor in water and minerals. Plants of
the significance of these morphological variants in the environ- this type must exhibit structural and physiological specializations
ments in which the plants grow. To these ends this book will first that permit them to scavenge the maximum available nutrients
acquaint you with the science of plant morphology and the basic and water. The shoot surfaces of these two Tillandsia species are
organ components of the plant body, how they originate during covered with specialized epidermal scales that take up water and
plant development, and what parameters are varied to produce minerals from the surrounding air (Benzing, 1970).

1
2 Kaplan’s Principles of Plant Morphology

leaves which grow erectly and are heavily ribbed for reinforce-
ment (ML, Figure 1.2). The mantle-type leaves catch water and
debris from the trees above. In essence, the plant forms its own
flowerpot, and its roots grow into the accumulated soil and water
which are sources of nutrients in this otherwise nutrient-poor
environment. We will see numerous other examples of particular
plant groups that exhibit distinctly different but equally effective
morphological solutions to similar environmental problems.
It is an easy step to go from plants that live on the surfaces
of other plants (epiphytes) but do not penetrate the tissues of
their support plant and are nutritionally self-sufficient, to plants
that actually penetrate the tissues of their host and are parasitic.
Figure 1.3 shows an example of a parasitic flowering plant grow-
ing on a branch of a spruce tree, Picea spp. The parasite is the
dwarf mistletoe Arceuthobium microcarpum (Engelm) Hawksw.
& Wiens. While the aerial flowering shoots arising from the host
surface may look conventional, in reality they are only the repro-
ductive phase of this species. The vegetative or feeding phase
consists of simplified strands that permeate the body of the host
and draw water and nutrients from it. At the time of reproduc-
tive dispersal from the old host to a new one, the Arceuthobium
initiates flowering shoots from the internal absorptive system.
These flowering shoots break through the bark of the host to
produce seeds, which are essential for dispersal of the parasite
(Figure 1.3). Given Arceuthobium’s nutritional dependence on

FIGURE 1.1 Two epiphytic species of Tillandsia growing on a tree branch

in a Cypress swamp in southern Florida. Tillandsia fasciculata is the erect
growing rosette shoot and T. usneoides, “Spanish moss,” is the much-
branched, net-like species hanging below it.

Another epiphyte which exhibits quite different morphologi-

cal specializations to cope with the rigors of this environment
is the staghorn fern in the genus Platycerium (Figure 1.2).
Platycerium climbs along its support plant, using its roots for
attachment. It produces at least two different leaf types: large,
elaborate pendant fronds which are the photosynthetic and spore-
bearing organs of the shoot (FL, Figure 1.2) and mantle-type

FIGURE 1.3 The dwarf mistletoe Arceuthobium microcarpum growing as

FIGURE 1.2 The staghorn fern in the genus Platycerium grows as an epi- a parasite on a branch of a species of Spruce (Picea). The mistletoe shoots
phyte along the trunk of a tropical forest tree. This species exhibits two types seen protruding from the surface of the host are actually the flowering por-
of leaves, the large branched and pendant foliage leaves (FL) which photo- tions of the parasite and are formed from the absorptive system inside the
synthesize and bear the spores, and the mantle leaves (ML) that persist and host tissues and secondarily break out onto its surface for pollination and
impound debris as a source of nutrients for the roots of this fern to grow into. seed dispersal. (From Hawksworth and Wiens, 1972.)
Introduction to the Science of Plant Morphology 3

its host, it is not necessary to have an elaborate vegetative struc-

ture differentiated into leaf and stem because this organism is
no longer autotrophic. Such examples show us how closely plant
structure and function can be linked in species with very special-
ized life modes.
Certainly one of the most fascinating plant types are the so-
called insectivorous or carnivorous plants. The thought that
there can be such things as man (and woman)-eating plants has
stirred the imaginations of science fiction writers since time
immemorial. In reality, these plants are adapted to grow in areas
that are deficient in certain mineral elements, especially nitrogen.
Their plant bodies are specialized for the attraction, capture, and
digestion of animals (mostly insects) as sources of nitrogen and
other nutrients. An example is the shoot system of the California
pitcher plant, Darlingtonia californica. This species has a
rosette-type shoot with large, elaborately colored, tubular leaves
that serve as traps and sites of digestion of the insects that nour-
ish the plant. Despite the seemingly bizarre and unique functions
that the leaves of this carnivore perform, their leaf morphology
has been shown to be related to that of other, more conventional
plants. Once we learn how to analyze plant form and understand
the basis for its variation, such modified or functionally special-
ized organs will not seem quite so out of the ordinary.
One of the truly distinctive types of vegetation on the earth
today are the mangroves. Mangroves are trees that grow along
seacoasts and coral reefs in the tropical to subtropical latitudes.
They are salt tolerant and are able to grow on relatively unstable
substrates that can be covered by seawater during high tides.
Because of the distinctive soil environment in which mangroves
grow, it is their roots and root systems that exhibit specialization.
Figure 1.4A shows an individual tree of the black mangrove,
Avicennia germinans L. growing on the southwest coast of the
Florida peninsula. If you observe this species at low tide, you
will notice at the base of the trunk horizontally growing, cable- FIGURE 1.4 A. Black mangrove tree Avicennia germinans growing on the
like roots that spread over the sandy substrate. Growing upward south coast of Florida showing vertically growing root branches or pneu-
from these cable roots are erect, finger-like branches called pneu- matophores exposed at low tide. B. Closeup view of pneumatophores grow-
ing upward from laterally extending strand roots. P, pneumatophore.
matophores (Figure 1.4B). When the rest of the root system is
covered by saltwater at high tide, the pneumatophores protrude
above the water and aerate the submerged roots. If you were to
examine the structure of the pneumatophores microscopically
you would see that they really are roots modified to function in
this distinctive habitat.
While we tend to think of plants as self-supporting struc-
tures whose shoots grow toward the light, vines and twining
plants climb the surfaces of other plants to reach sufficient light.
In contrast to epiphytes, vining plants begin their lives on the
ground and only secondarily ascend their support plants. Many
climbing plants have specialized branches or leaves that exhibit
a particular physiological response called thigmotropism.
Thigmotropism is a growth movement induced by the con-
tact of a plant organ with some surface, usually the surface of
another plant. Plant organs that exhibit a thigmotropic response
are called tendrils. The most typical thigmotropic response of
tendrils is a coiling growth, whereby the tendril organ wraps
around whatever structure it contacts. In most vines, the tendril
FIGURE 1.5 Aerial shoots of the leguminous shrub Bauhinia vahlii exhib-
is a free structure that will strike a potential support surface or
iting watch-spring tendrils (T) developed as lateral branches in the axils of
plant as it swings through the air and respond by grabbing that leaves. In this vine, the support plant grows through the tendril and then the
structure. However, in the leguminous shrub Bauhinia vahlii tendril exhibits a thigmotropic response by coiling tightly around support
(Figure 1.5), the converse occurs: the support plant grows plant axis.
4 Kaplan’s Principles of Plant Morphology

through the already coiled Bauhinia tendril securing support for

the Bauhinia. Tendrils in Bauhinia are modified shoot branches
with tips that coil spontaneously in a single plane, like a watch
spring. If a shoot of some other plant grows through the coil of
one of these tendrils, the tendril will tighten around it. When we
study the morphology and biology of climbing plants in Chapter
24 we will explore the variety of attachment mechanisms that
vines exhibit.

Basic Organization of the Higher Plant Body

Early in this chapter we stated that the vast majority of special-
izations exhibited by higher plants represent structural varia-
tions on a basic theme or organizational ground plan. Now that
we have looked at several examples of these specializations, we
would like to characterize the ground plan that links these seem-
ingly disparate and distinctive species and indicate how we char-
acterize the major plant organs and organ systems.
Figure 1.6 is a general, idealized drawing of the major organs
of the higher plant and their structural relationships. The basic
body of the higher plant can be resolved into two major organ
systems: the shoot and the root. In many plant groups the shoot
and root components are spatially separate, and we can speak
of distinct shoot and root systems. In others there is no spatially
distinct root system and roots arise exclusively from the shoot.
One usually thinks of the shoot as the aerial component of the
plant and the roots the subterranean portion, but as we will see,
one can find plants with subterranean shoots and others with
aerial roots.
Both roots and shoots have regions of continued embryonic
activity at their tips, the apical meristems, where organ forma-
tion, or organogenesis, continues during much of the life of the
plant (Figure 1.6A). Because of the existence of these embry-
onic centers at the extremities of each plant axis, both shoots FIGURE 1.6 A. General ground plan of the body of a dicotyledon-
and roots exhibit gradients of differentiation along their lengths, ous flowering plant, showing differentiation into a proximal root system
with the most embryonic or primordial tissues and organs and a distal shoot system. B. Dicotyledonous embryo after cotyledon ini-
tiation. C. Mature embryo showing shoot pole, root pole, and hypocotyl.
located at the distal end and the most mature at the proximal end
D. Transection of a root showing tissue distribution. E. Transection of a stem
(Figure 1.6A). showing tissue distribution. B, axillary bud; C, cortex; Ca, vascular cam-
bium; Co, cotyledon; E, endodermis; In, internode; L, foliage leaf; LR, LR’,
lateral roots of successive orders; N, node; Pe pericycle; Ph, phloem; Pi, pith;
The Shoot System PR, primary root; RAM, root apical meristem; RC, root cap; SAM, shoot
The shoot system of the plant consists of two major compo- apical meristem; X, xylem. Horizontally shaded areas represent embry-
onic or growing regions. Hatched areas xylem; open phloem and/or mature
nents, leaves and stem. The leaves are the lateral appendages
tissues. (Redrawn from Troll, 1937)
and comprise its major photosynthetic surface (L, Figure 1.6A).
Typically, leaves are dorsiventrally flattened organs of deter-
minate size and shape and can be differentiated regionally into embryonic leaves with protection from desiccation by the sur-
a flattened distal blade region, a petiole or stalk, and the leaf rounding older, more mature leaves. If stem internodes of a bud
base, where they are inserted onto the shoot axis or stem (L, will eventually be extended, elongation usually takes place some
Figure 1.6A). The point of leaf insertion on the stem is called the distance below the shoot tip and results in the separation of the
node and the section of stem between two nodes the internode points of leaf insertion from one another (Figure 1.6A). In so-
(N, IN, Figure 1.6A). called rosette shoots, the internodes do not become extended
The shoot apical meristem is the site of origin of leaves and and the leaves retain the tightly congested pattern characteristic
new stem increments whose continued initiation and expansion of the terminal bud but with the leaves expanded to their full,
are responsible for the extension of the shoot in space (SAM, mature size.
Figure 1.6A). At the shoot apical meristem, the rate of leaf The position of insertion of leaves on the shoot axis is not ran-
inception exceeds that of stem elongation, hence the leaves dom but occurs in a precise geometric pattern that can be charac-
become packed together forming a terminal bud (Figure 1.6A). teristic for a given species. Such patterns of leaf arrangement are
The terminal bud configuration provides the youngest, most called the phyllotaxis (from the Greek words phyllo, meaning
Introduction to the Science of Plant Morphology 5

leaf, and taxis, meaning arrangement) and they influence the cortex before emerging to the exterior. The structure and meri-
overall appearance of the shoot of an individual plant. For exam- stem characteristics of the lateral roots are similar to those of the
ple, because the lateral branches of the shoots of most seed plants parent root.
(gymnosperms and angiosperms) are borne at the positions In the same way that there are distinctive geometric patterns
where leaves are inserted, i.e., the leaf axil (B, Figure 1.6A), the for the positioning of leaves in the shoot (the phyllotaxis), there
spatial distribution of branches will reflect the phyllotactic pat- are distinctive geometric patterns to the arrangement of lateral
tern of the shoot. Thus the phyllotaxis is a fundamental expres- roots on the parent root. One therefore can speak of rhizotaxis
sion of the symmetry and overall morphology of a shoot. (from the Greek words rhizo-, meaning root and taxis, meaning
Because leaves have a limited life span and usually abscise arrangement) and, like phyllotactic patterns, rhizotaxes can be
or fall from the shoot after they die, they leave the stem as a characterized in precise mathematical terms.
relatively naked axis and give the impression that the stem itself One of the most distinctive features of the root is the nature
is the basic component of a plant’s morphology and that the of its meristem. In contrast to that of the shoot, the root apex
leaves are only secondary as though they have been attached produces no lateral appendages from its periphery. In addition,
onto the stem as an afterthought. In fact, from a developmental- the root apex is covered by a cellular product of the meristem, the
morphological perspective, the converse is true. Leaves are the root cap (RC, Figure 1.6A). Cells of the cap are produced con-
primary structures laid down at the shoot apex. In seed plants, tinuously by the root apical meristem so that the youngest, most
at least, they dominate the growth and development of the shoot embryonic cap cells are those adjacent to the body of the root and
and significantly influence the differentiation patterns of tissues, the oldest, most mature cells are at the cap’s periphery. As cap
e.g., the vascular tissues (Esau, l965). If the internodes elongate, cells mature peripherally, they slough off and secrete mucilagi-
they do so after the leaves have been initiated and have influ- nous material. Thus the cap serves not only as a protective buffer
enced the fundamental transectional symmetry (Chapter 10) for the subjacent meristem as the root tip grows through the soil,
of the shoot. In some plants, in fact, the leaf bases extend with but also serves as a lubricant for root growth. Recent research has
the internodes so the stem really looks as though it is made shown that the root cap also is significant in regulating the geo-
up of the extended basal portion of the leaves (decurrent leaf tropic responses of roots or the direction of their growth relative
bases) rather than being an independent structure. The vagaries to the earth’s surface (Feldman, 1985).
of defining the boundaries between stem and leaf components Shoots and roots also differ from each other in the arrange-
of the shoot underscore the fundamental developmental unity of ment of their tissues. Figure 1.6D,E shows transections through
these two elements and the artificiality of attempting to draw a a representative root and stem of a higher plant. Just inside the
rigid boundary between them. peripheral band of cortical tissue of the stem is a cylinder of vas-
As we shall see when we examine in more detail the develop- cular bundles (Figure 1.6E). Of the two vascular tissue types
mental potentials and parameters of the shoot system, the indi- comprising each bundle—the xylem and phloem—the xylem is
vidual axillary buds along the length of a shoot axis can exhibit oriented toward the central pith region and the phloem toward
a range of developmental fates, producing, on the one hand, the outside of the stem or cortex, and both conducting tissues lie
branches that simply replicate the morphology of the parent axis on the same radius (Figure 1.6E). By contrast, in roots the xylem
from which they were derived, and on the other, lateral shoots and phloem are arranged on alternating radii (Figure 1.6D) and
specialized for a range of biological functions. In the shoots of there may or may not be a well-defined pith region. The presence
higher plants, it is the leaf and branch components that play spe- or absence of a pith in roots seems to depend on the diameter of
cial roles. the root’s primary body: Those roots with large diameters usu-
ally have some pith region in their centers whereas those with a
smaller diameter typically do not.
The Root System
Located at the opposite pole of the plant body, or 180 degrees
from the shoot, is the root system (Figure 1.6A). Like the
The Concept of Homology
shoot system, the root system consists of a main axis or pri-
mary root from which branches are produced laterally. Where Now that we have characterized the fundamental organization
a spatially separated root system is developed, this bipolarity of of higher plants, let’s see how it can vary in order to produce the
the plant body is forecast by the bipolarity of the plant embryo great diversity of plant form that we see on earth today.
(Figure 1.6B,C). In order to conclude that the diversity of plant morphology
Roots differ from shoots in that roots lack lateral appendages, represents variations on a basic organizational theme, we must
or the equivalents of leaves. What may look like leaf structures assume that the structural specializations observed represent
emerging from roots (Figure 1.6A) are actually branch roots modifications of the same basic organ systems. This idea is
extending in a lateral orientation from the body of the parent expressed by the concept of homology.
root. In contrast to shoot branches, which originate exogenously We will use the term homology in a strictly comparative con-
from superficial (surface) tissues, root branches arise endog- text to mean morphological correspondence to one of the major
enously from within the body of the parent root and only sec- organ categories, i.e., leaf, stem, or root. You may have heard
ondarily grow out into the substratum (Chapter 24). Typically, the term homology defined as structural correspondence due
their point of origin is from the meristematic pericycle layer at to a commonality of evolutionary descent. However, where we
the periphery of the root’s vascular cylinder (Pe, Figure 1.6A). are concerned with the principles of structural change in plants,
Hence, branch roots must burrow through the surrounding root such phylogenetic definitions of homology are far too restrictive.
6 Kaplan’s Principles of Plant Morphology

In addition, if morphological data is to be used as evidence of have lateral appendages but roots do not, if you found nodes or
phylogenetic relationships, the question of structural equiva- leaf scars along its axis and its branches were not endogenous in
lence must first be determined independent of phylogenetic sta- origin, you would predict you had a modified stem. On the other
tus. Thus, we will determine homologies on the basis of their hand, if the structure had no signs of appendages but had a cap
structural equivalence using strictly morphological criteria. over its meristem with branches that were endogenous in origin,
Evolutionary biologists often develop hypotheses to test whether then most likely it would be a modified root.
such structural correspondences are a result of evolutionary Further discrimination could be provided by analyzing tissue
convergence (either parallel or convergent evolution) and there- arrangements. Since vascular tissues in stems tend to be aligned
fore represent what Lankester (1870) has called a homoplasy or on the same radii (Figure 1.6E), whereas those in roots are on
whether they reflect a commonality of ancestry or in Lankester’s alternate radii (Figure 1.6D), it is possible to determine whether
terminology, a homogeny (Lankester, 1870). Such phylogenetic an unknown axis is a root or a shoot. This is another example of
interpretation requires integration of our morphological data the application of the special quality criterion for determining
with information from all other aspects of the plant’s biology in organ homologies.
order to reach valid conclusions concerning evolutionary rela- The third criterion, the existence of intermediates between
tionships. Thus the determination of structural relationships on two seemingly different structures, is dependent on the first two
the basis of comparative morphology should not be viewed as an criteria but can nevertheless be a useful tool in determining mor-
end in itself, but merely the first step in a long and complicated phological relationships. Since plants are metameric organisms
process of systematic evaluation. whose bodies consist of repeating subunits (e.g., leaves, nodes,
How do we actually determine the homologies of a problem- and internodes in the shoot; Figure 1.6A) and the characteris-
atic plant organ with one of the fundamental units of the plant tics of those metamers can change gradually along the length
body? In other words, what criteria do we apply to determine of the plant, one can see transitions in structure along a shoot
whether a given plant structure is a modified leaf, stem or root? axis. Where intermediates exhibited by positionally homologous
organs occur along the length of a given plant axis, the phenom-
enon is termed serial homology.
Homology Criteria An example of serial homology can be observed in young
plants of the barberry, Berberis wilsonae (Figure 1.7). After
The German morphologist-systematist Remane (l952) has sug- the first leaves or cotyledons, the shoot produces a number of
gested three criteria that can be used to decide homologies of an broadly laminate, green foliage leaves. At the more distal nodes,
organ or organ system. These are: however, the shoot produces non-photosynthetic spine-like
leaves that consist of three to five spine branches. Instead of the
1. Equivalent positions within the general ground plan or main axis bearing the photosynthetic leaf surfaces, short shoots
organization (positional criterion). borne in the axils of the spines (those with little to no internodal
2. Equivalent special quality (quality criterion). elongation) bear the laminate green leaves. The spiniferous
3. Connection of differing structures by intermediates appendages borne on the main axis do not seem at first glance to
(transitions criterion). be homologues of leaves, much less structurally related to more
conventional foliar organs. Yet if we analyze the properties of
The positional criterion is certainly one of the most fundamen- these spines, particularly their structural relationships to other
tal and a feature that influences many of the properties of the leaves of that shoot, their morphological relationships become
organs of the plant body. For example, the leaf component of more apparent.
the shoot always occupies a set position as a lateral outgrowth The spiniferous organs occupy the same position in the shoot
from the stem (Figure 1.6A). In seed plants, this position tends as the earlier-formed leaves and, like these leaves, bear shoot
to be demarcated by the location of a lateral branch or branch branches in their axils (Figure 1.8A). Hence they are position-
primordium in the axil of the leaf. Thus, if you were to observe ally homologous with leaves. Furthermore, by their spiniferous
an axis bearing leaf-like appendages along its length, you could nature it is clear that, like other leaves, they are determinate
determine whether it was (a) homologous with an individual organs. But more significantly, at the nodes between those bear-
leaf whose blade was cut into subunits or leaflets or (b) a lat- ing the basal laminate appendages and those bearing the spines
eral branch bearing its own leaves by determining the location are leaves that are intermediate in morphology between green
of axillary buds. If it were an individual leaf whose blade was and spiniferous leaves and support the homology of spines with
cut into leaflets, there would be a bud in the axil of the entire leaves (Figure 1.8A,B).
structure and no buds in the axils of the leaflets (Figure 1.6A). The intermediate leaves have blades that are cleaved into lobes
If it was a branch bearing its own leaves, it would be subtended but the lobes end in distinct spines (P, Figure 1.8B, II,III).
by a leaf or a leaf scar and each of the leaves would have buds in There is a short step from these intermediates that are spinif-
their axils (Figure 1.6B). erous but still produce a broad, green, photosynthetic surface
The special quality criterion refers to characteristics of an to leaves where each blade segment or leaflet is entirely spine-
organ which are distinctive and whose expression is not neces- like (Tr, Figure 1.8A,B, II–IV). Thus by studying transitional
sarily dependent upon the position of the structure in the plant forms that combine the characteristics of the two extremes we
body. If you were given a plant axis separated from the rest of are able to see a structural relationship, or homology, between
the plant and were asked to decide whether it was a stem or a two structures which, if considered in isolation, would seem to
root, this criterion would be useful. For example, since shoots bear little to no relation to one another.
Introduction to the Science of Plant Morphology 7

Leaflets or pinnate

Stem

Compound leaf
Axillary bud
Petiole
Leaf base

Terminal bud

Axillary buds

FIGURE 1.8 A. Seedling of Berberis wilsonae exhibiting serial (sequen-

tial) changes in leaf morphology along the length of its shoot axis. After the
cotyledons, this plant forms primary leaves that are green and broadly lami-
nate but whose lamina lobes bear spines. In the more distal portion of the
shoot, foliage leaves are strictly spiniferous and bear axillary short shoots
with broad green blades. B. Transitions in leaf morphology between broadly
laminate primary leaves (l) and spiniferous, non-photosynthetic leaves (IV)
Axillary lateral and the intermediates between them (II, III). AS, axillary short shoot; Co,
branch cotyledon; L, lamina; P, primary leaf; Pet, petiole; St, stipule; T, thorn leaf;
Tr, transition leaf. (From Troll, 1939.)

in their axils, one would be hard pressed to think of this spe-

cies as a member of the cactus family (Figure 1.9A). In Opuntia
Subtending or Axillant leaf subulata (Figure 1.9B) the blade has been reduced significantly
B compared to that of the leaves of Pereskia. Instead of having a
broad, dorsiventral blade, the lamina of Opuntia is more linear
FIGURE 1.7 Comparison and contrast between (A) a compound leaf bear- and cylindrical and has considerably less surface area when com-
ing lateral leaflets and (B) a lateral branch bearing leaves. pared with that of Pereskia (compare Figure 1.9A with B). As a
correlative development, the leaf base in O. subulata is expanded
Such transitional forms can be observed not only along the into a prominent, cushion-like outgrowth which students of cacti
length of an individual plant but also between different individ- have termed a podarium (LB, Figure 1.9B). In O. cylindrica,
uals or species of plants. For example, members of the cactus the lamina is even shorter and less conspicuous than that in
family (Cactaceae) are said to be leafless, stem-succulent plants. O. subulata (compare Figure 1.9C with B). Moreover, because
The stem is swollen as an organ of water storage and the leaf the blade of O. cylindrica abscises relatively early in ontogeny,
component so reduced that it seems absent altogether. In reality, it is evident only on the youngest leaves at the distal end of the
the leaf component is present in all members of Cactaceae as we shoot (Figure 1.9C). As the leaves mature and their blades fall
shall see when we take a closer look at members of this family off, the more mature, proximal region of the stem is left clothed
later in this book. The interesting thing about the cactus family is simply by the expanded podaria. In more derived species of cac-
that its evolutionary diversification must have occurred relatively tus, such as those placed in the genus Mammilaria, the leaf blade
quickly because all the intermediates have been preserved. For is so reduced that it is microscopic and seemingly absent in the
example, one can find cacti that bear large, laminate leaves that mature leaf. All that remains of the leaf is the base, which has a
look like those of other dicotyledonous flowering plants all the conspicuously tuberculate form (LB, Figure 1.9D).
way to cacti whose leaves are reduced and even inconspicuous. In this comparison of intermediates in leaf morphology
Four cactus species (Figure 1.9) illustrate transitions in leaf between so-called leafy and leafless cacti it can be seen that all
reduction in this family and provide some insight into how the species bear leaves and that it is only a portion of the leaf,
it has taken place. In a “leaf-bearing” cactus, Pereskia spp., the lamina, which has been reduced. It is the subjacent leaf base
(Figure 1.9A), the leaves are broadly laminate with a very short or the point of attachment of the leaf on the stem that becomes
petiole or leaf stalk. If it were not for the spine-bearing short shoot expanded as the major photosynthetic surface of the shoot. As we
8 Kaplan’s Principles of Plant Morphology

FIGURE 1.9 Members of family Cactaceae illustrating progressive stages of leaf blade reduction in selected genera and species. A. Broadly laminate
foliage leaves in Pereskia aculeata. B. Reduced, cylindrical blades in Opuntia subulata. Note that a cushion-like leaf base has developed in this species. C.
Opuntia cylindrica; only the youngest leaves bear a lamina (L) and the blade abscises later leaving only the cushion like leaf base (LB) or podarium clothing
the stem. D. Shoot of Mammillaria elephantidens showing enlarged tuberculate leaf bases and no sign of a lamina evident. (A–C from Troll, 1939; D from
Goebel, 1932.)

shall see, the comparison of intermediate morphological forms is ways of determining which units can be compared in order to
a useful approach in deducing the structural relationships in what understand the patterns and processes of plant evolution. As we
may seem to be divergent structures. make homology statements, it is important to consider that the
It should be emphasized that these homology criteria should plants themselves do not know that they are being subdivided
not be viewed as rules that are applied rigidly and dogmatically into component parts any more than you think of yourself as
to the evaluation of the diversity of plant morphology. Depending being segmented into arms, legs, and head as you go about your
on the characteristics of the plant organ in question, certain cri- daily activities. We make these subdivisions so that we can com-
teria may be more useful than others. It is always important to pare plants and see how they vary from one another, not because
keep in mind that homology is a hypothesis, and the criteria are we think the subdivisions have any independent reality.
Introduction to the Science of Plant Morphology 9

FIGURE 1.10 Illustrations of spine root morphology and positions on the shoot system of the palm Crysophila guagara. A. Young plant. B. Crown spines
emerging from the tops of leaf sheaths. C. Detail of short trunk spines. D. Detail of prop roots at base of trunk. E. Morphology of individual root types.
1. Trunk roots and apical spine conversion. 2. Large prop roots with unmodified apices. 3. Crown root morphology. (From McArthur and Steeves, 1969.)

Let’s look at one more example of a problematic plant struc- homology to roots, but also provides an example of how devel-
ture, the spine-like outgrowths along the trunk of the Central opmental stages represent the application of the third criterion
American palm Crysophila guagara (Figure 1.10A–D) and (the transitions) to the elucidation of structural relationships.
apply the three criteria to elucidate its homology. McArthur and Figure 1.11 shows the developmental stages of root spine
Steeves (1969) have shown that the spines along the trunk of this formation in C. gaugara. In its early stages the spine has the
palm originate endogenously from stem tissue just like the prop- form of a typical root apex with a well-defined body and cap
type feeding roots at the base of its trunk that penetrate the soil (Figure 1.11A). During subsequent development, it progres-
(Figure 1.10D). Thus there is a serial homology and gradient sively loses the characteristics of a typical root meristem, by
of developmental expression of roots initiated along the length shedding its cap (Figure 1.11B,C) and its apex becomes scleri-
of the shoot with indeterminate, feeding roots initiated close to fied into a thorn (Figure 1.11D,E). The cell lineage patterns
the soil (Figure 1.10D) and determinate, spine-like roots initi- characteristic of root meristems are no longer evident. Thus
ated along the trunk (Figure 1.10B,C). These spine roots have while the root spine may look quite unlike a conventional root
lateral branches that, like lateral roots (Figure 1.10E, 1 and 2), at maturity, it does look like a root in its early development.
arise endogenously from the internal tissues of the parent root. The comparison of developmental stages of the root spine to
Because the tissue arrangement of the spines is characteristic of a conventional root has the same value in determining the
roots rather than shoots (Figure 1.11A–E), the special quality organ’s homology as does comparing morphological interme-
criterion also supports the root homology of these spines. diates using serial homology within an individual or transi-
Finally, the developmental stages of the transformation tions of organs between species.
of a root primordium into a spine reinforces not only their
10 Kaplan’s Principles of Plant Morphology

FIGURE 1.11 Median longitudinal sections of the lateral trunk roots of the palm Crysophila guagara showing the developmental transitions from a con-
ventional root apex to that of a spine root. A. Unmodified root apex. B. Later stage showing acropetal extension of elongation and differentiation resulting in
attenuation of the apex. C. Sloughing off of the root cap. D. Differentiation of elongated sclerenchyma cells in cortical and vascular regions. E. Mature spine
tip. All ×60. (From McArthur and Steeves, 1969.)

The Concepts of Analogy versus Homology shoot-borne roots. In all three we are characterizing structures
that have identical functions (grasping and twining) but are not
If the term homology deals with the structural relationships of homologous: they are analogous.
plant organs regardless of their particular functions, the term As we proceed through this text, we will see numerous exam-
analogy refers to different plant organs that perform the same ples of structural analogies, especially in plants that belong to
function. For example, tendrils are plant structures that exhibit different taxonomic or evolutionary groups but live in the same
a contact-induced growth response or thigmotropism. However, habitat. Behaviorally they all will be similar, but in many cases
tendrils can be modified shoots (branches), leaves, or roots. In will represent differing or analogous solutions to the same envi-
the grapevine relative Cissus spp., tendrils are modified shoots, ronmental stimuli. One of the principal goals of the practicing
equivalent morphologically to sterilized inflorescence branches plant morphologist is to be able to discriminate homologies from
that have acquired thigmotropic behavior associated with flo- analogies. This is accomplished by applying the homology crite-
ral reduction. By contrast, in the sweet pea, Lathyrus spp., ria that we have described in this chapter.
the tendrils are modified subunits of the leaf (leaflets or pin-
nae), whereas in the orchid Vanilla spp., tendrils are modified,
2
The Cast of Characters: A Review of the Plant
Kingdom and Its Major Representatives

CONTENTS
The Concepts of Reproductive Life Histories in Plants.......................................................................................................................... 11
The Major Groups of the Plant Kingdom............................................................................................................................................... 17
The Algae .......................................................................................................................................................................................... 17
The Green Algae (Division Chlorophyta)..................................................................................................................................... 17
The Red Algae (Division Rhodophyta)......................................................................................................................................... 18
The Golden-Brown Algae (Division Chrysophyta)......................................................................................................................20
The Brown Algae (Division Phaeophyta)..................................................................................................................................... 21
Other Algal Divisions...................................................................................................................................................................22
Land Plants........................................................................................................................................................................................22
Division Bryophyta.......................................................................................................................................................................24
Tracheophytes...............................................................................................................................................................................25
Division Lycopodiophyta (Lycophyta, “Lycophytes” or “Lycopods”).........................................................................................25
Class Pteridopsida.........................................................................................................................................................................26
Class Psilotopsida.........................................................................................................................................................................27
Class Sphenopsida........................................................................................................................................................................28
Embryophyta (Seed Plants)...............................................................................................................................................................29
Concept of the Seed......................................................................................................................................................................29
The Gymnosperms........................................................................................................................................................................34
Division Cycadophyta...................................................................................................................................................................35
Division Ginkgophyta...................................................................................................................................................................35
Division Coniferophyta (or Pinophyta)........................................................................................................................................36
Division Gnetophyta.....................................................................................................................................................................36
Division Magnoliophyta (Angiosperms)......................................................................................................................................36
Morphological Convergences between Plant Groups that are Unrelated Evolutionarily.......................................................................39

As we begin our study of the principles underlying morpho- beginning as a single cell and ending with the mature organ-
logical diversity in plants, it is important to be able to associate ism capable of reproduction. In fact, reproduction itself is typi-
the wide variety of plants we will be discussing with the major cally included as an important part of the characterization of the
plant groups to which they belong. Moreover, although we will developmental history of an organism because the production
emphasize vascular plants in our studies because they exhibit the of subsequent generations is viewed as a principal goal of any
greatest range of structural diversity, it is instructive to be able to generation.
relate their morphology with that of other members of the plant Depending upon whether there is a genetic difference between
kingdom. In this chapter we review the broad classification of the the parent and its offspring, we can distinguish between sexual
plant kingdom and some of the principles of life histories that and asexual life histories. In an asexual life history, the offspring
characterize the major plant lineages.* are the result of cell multiplication and possible fragmentation
and the genetic constitution of the derivative cells or tissues is
identical to that of the parent. The simplest asexual life history
The Concepts of Reproductive Life is illustrated by single-celled organisms, such as the green alga
Histories in Plants Chlamydomonas, that undergo mitosis to form derivative cells
identical in morphology and genetic makeup to the parent cell
The term “life history” usually refers to the complete record of (Figure 2.1A–E). By contrast, in sexual reproduction, the off-
the existence of an organism, whether unicellular or multicellular, spring differ genetically from their parents. Genetic variation in
the sexual reproductive cycles of eukaryotic organisms comes
* A section entitled “Contemporary Classifications of the Living World” from two sources: genetic crossing-over in meiosis, and genetic
was removed from Kaplan’s original manuscript. The classifications he recombination in syngamy or fertilization.
provided for unicellular and multicellular lineages continued to change
with genomic sequencing and thorough phylogenetic analyses and are The reproductive life histories of most eukaryotes involve
beyond the scope of this presented work. a regular alternation between a haploid (n) and a diploid (2n)

11
12 Kaplan’s Principles of Plant Morphology

Syngamy

Meiosis
n n

J. K.
+ 2n
H.
F. I.
n
n+Ω
n
−
G.
n

D. + E. − n
n
+

L. +
C. n
n
M.
n N.
n −

n
B. O. −
A. n n

FIGURE 2.1 Zygotic life history of the unicellular green alga Chlamydomonas. A, B. Haploid cells separate from the colony (C) and undergo asexual
reproduction to give rise to the cells that will ultimately function as gametes (D, E). Isogametes F and G fuse in the process of syngamy (fertilization) (H, I)
forming a diploid zygote which overwinters as a thick-walled zygospore (J). Upon germination, the zygospore protoplast undergoes meiosis (K) forming four
haploid unicellular products (L, M, N, and O). (From Scagel et al., 1965.)

chromosomal levels of the nucleus. In humans and most other The diploid state is restored by the fusion of two haploid gam-
animals, for example, cells of the somatic or feeding phase are at etes to form a diploid zygote (Figure 2.4). In the course of typical
the diploid level, which in humans have 46 chromosomes or 23 animal development, the single-celled zygote undergoes mitosis
chromosome pairs. Formation of haploid gametes or germ cells to form an embryo, which enlarges and matures into a function-
involves the reduction of the chromosome number by half (to the ing diploid adult. With its differentiation of the sex organs, this
haploid level) in the process of meiosis (Figure 2.3). sexual reproductive cycle is repeated (Figure 2.4).
Meiosis is a more complicated cell division process than Life histories in which the dominant phase is diploid and the
somatic division or mitosis (Figure 2.2). In the latter, the cell haploid phase is represented only by the gametes, such as that
division process starts with the replication of the chromosomes just described for humans and other animals, are called gametic.
in the interphase period preceding division, followed by a sepa- They also are termed diplontic because of the dominance of the
ration of the replicated chromosomes to the poles of the dividing diploid phase. In the diagram of a diplontic life history relation-
cell prior to the partitioning of the original parent cell into two ship shown in Figure 2.5, meiosis and syngamy (fertilization)
derivative cells. Each daughter cell has the same genetic makeup form the boundaries between haploid and diploid phases. These
and chromosome number as the parent cell (Figure 2.2). By con- diagrams show the relationships of the nuclear cycle in different
trast, meiosis involves a similar replication or doubling of the life history types.
diploid chromosome number, but it is followed instead by two While diplontic life histories with gametic meiosis are pre-
division sequences (called meiosis I and II; Figure 2.3) result- dominantly characteristic of animals, there are a few plants that
ing in four haploid cells, each with a different genetic makeup exhibit this type of life cycle; for example, the brown algal sea-
(Figure 2.3I). The difference in genetic constitution is a result weed Fucus (Figure 2.6). In Fucus, the thalloid, dichotomously
of the pairing of homologous chromosomes during prophase of branched plants one sees in the intertidal region of the seashore
meiosis I followed by the exchange of pieces of adjacent chro- are diploid and bear gametangia on their upper surfaces. Sperm
matids in the process called crossing over (Figure 2.3B). As a and eggs produced in these gametangia are the products of
result of crossing over, each of the four cells is genetically differ- meiosis and are released into the seawater where fertilization is
ent (Figure 2.3E–I). effected (Figure 2.6A–D, H–M). The diploid zygote undergoes
The Cast of Characters 13

Nucleolus
Nuclear envelope
Nucleoplasm
Chromosome

Early Prophase Mid-Prophase

A. B.

Pole
Spindle fiber
Chromatids
Centromere

Late Prophase
Metaphase
C. D.

Nucleolus
Chromosome
Cell plate
Phragmoplast
Daughter chromatids
Nuclear envelope
E. Anaphase F. Telophase

FIGURE 2.2 Stages in mitotic division of a plant cell. A–C. Prophase showing increasing condensation of chromosomes and gradual disappearance of the
nucleolus. D. At metaphase (D) the nuclear membrane has broken down and chromosomes are arrayed on the equatorial plane of the cell. They are attached
to the poles of the cell by spindle fibers. E. At anaphase the subdivided, duplicated chromosomes are pulled to the opposite poles of the cell, and at telophase
(F) the nuclei are reconstituted and the process of cytoplasmic division, or cytokinesis, takes place by the formation of a cell plate between the two nuclei.

A. Early prophase I B. Prophase I C. Prophase I D. Late prophase I

Metaphase I Anaphase I Anaphase II

E. F. G. Metaphase II H.

I. Late telophase II

FIGURE 2.3 Stages in a meiotic division. During prophase in a meiocyte, the individual chromosomes become more apparent due to increased condensa-
tion (A, B). Homologous chromosomes pair and exchange pieces of chromatin in the process of chiasma formation and crossing over (C). In late prophase
(D), homologous pairs separate and align on the equatorial plane at metaphase I (E). Homologous chromosomes are then pulled to the poles in anaphase
(F). At metaphase II (G) chromosomes in each of the resulting cells line up on the equator. In anaphase II, the centromeres of each chromosome split and
daughter chromatids in each dyad cell are pulled to the poles (H). Following reconstitution or nuclei, in telophase II, cytokinesis occurs, resulting in four cell
products (as seen in I), each with a different genetic constitution.
14 Kaplan’s Principles of Plant Morphology

2n 2n n
Male adult Male gonads Sperm
Meiosis 2n 2n 2n
Zygote Multicellular embryo Multicellular adult

2n 2n Meiosis n
Female adult Female gonads Egg

FIGURE 2.4 Life history diagram for a typical animal, illustrating a predominantly diploid or diplontic life history where meiosis is only associated
with gamete formation and where the diploid phase is quickly reconstituted in the union of those gametes to form the zygote or first cell of the new diploid
organism.

mitotic division to form a new multicellular diploid plant of the

M F
next generation (Figure 2.6E–G).
n In addition to this diplontic cycle, plants exhibit two other
major life history variants: haplontic and diplohaplontic. A hap-
lontic cycle is just the converse of the diplontic. Here meiosis is
zygotic; that is, it occurs immediately after syngamy. As a result,
the haploid (n) phase is predominant (Figure 2.5B). Haplontic
life histories are widespread in the algae; for example, the green
alga Chlamydomonas (Figure 2.7).
2n
If the haploid products of meiosis do not function directly as
gametes but instead undergo mitosis to form a haploid multicel-
lular tissue, then meiosis is said to be sporic and the unicellular
A. Gametic meiosis- diplontic life history products of meiosis are called spores. In this type of diplo-hap-
lontic life history, both haploid and diploid phases are free-living
F
multicellular stages. Such a life history is said to exhibit an alter-
M
nation of generations. The diploid phase has been called the
2n
sporophyte generation because its cells give rise to the haploid
spores as a result of meiosis (meiospores), whereas the haploid
phase is called the gametophyte generation because its cells
give rise to the gametes which ultimately fuse in the process
of fertilization, reestablishing the diploid or sporophytic phase
(Figure 2.5C).
n One of the principal variations in plants that have a sporic mei-
osis and hence exhibit an alternation of generations is whether
the two generations are similar or different in their morphology.
B. Zygotic meiosis- haplontic life history
If they are similar, then the plant is said to have an alternation
of isomorphic generations (from the Greek words iso meaning
equal, and morphos meaning shape). If the two generations are
structurally different, the plant is said to exhibit alternation of
heteromorphic generations.
The green alga sea lettuce (Ulva) is an example of a species with
2n
an alternation of isomorphic generations. Both generations con-
m sist of a flattened, thalloid plant body that is two cell layers thick
F
and anchored to the substratum by a holdfast (Figure 2.8A,L).
The two separate generations look so similar that it is impos-
n
sible to distinguish them except by detailed microscopic analy-
sis (Figure 2.8A,L). It should be possible to distinguish the two
generations by counting their chromosomes: Cells of the diploid
C. Sporic meiosis- diplo-haplontic life sporophytic phase should have twice as many chromosomes as
history- alternation of generation. those of the haploid or gametophytic phase. However, there may
be problems with polyploidy that would make the distinction
FIGURE 2.5 Clock-type diagrams, illustrating the relative proportions of equivocal. Furthermore, because the biflagellate spores of both
the haploid (n = clear) versus diploid (2n = shaded) sectors for a diplontic
gametophytes and sporophytes are identical, they are termed
life history with gametic meiosis (A); a haplontic life history with zygotic
meiosis (B); and a diplohaplontic life history with a sporic meiosis (C). isogamous (from the Greek iso meaning equal and gamo mean-
Boundaries between haploid and diploid phases are demarcated by fertiliza- ing marriage) and their form gives no clue as to their ploidy or
tion (F) and meiosis (M). function. The most decisive method of discrimination is to grow
The Cast of Characters 15

Syngamy

2n

D.
n E.
C.
n
F.

Meiosis
A.
2n

2n G.

B.
Meiosis
K.
2n
J. 2n

M. 2n
H.
L.

I.

FIGURE 2.6 Diplontic life history in the brown algal rockweed genus Fucus (division Phaeophyta). Diploid adult plant (G) forms male and female recep-
tacles on the tips of its dichotomizing thallus. Conceptacles embedded in the thallus receptacles bear male and female filaments (H, I) bearing antheridia
and oogonia at their tips (L, M and J, K), which in turn produce sperm and eggs, respectively (A, B). The latter are released into the water where they fuse
in the process or syngamy (C) to form the diploid zygote (D), which then develops into the multicellular diploid adult (E–G). (From Scagel et al., 1965.)

FIGURE 2.7 Haplontic life history with zygotic meiosis illustrated by the green alga Chlamydomonas (Chlorophyta). Each unicell, representing a different
mating strain (+ or –), is capable of asexual reproduction (A, B). With the onset of sexual reproduction, each cell will divide to form a packet of gametes (C).
These isogametes then fuse in the process of fertilization or syngamy (D, E) to form a diploid zygote (F). The zygote then synthesizes a thick wall and is a
dormant stage, the zygospore (F). When conditions for germination are right, then the zygospore cracks open and its protoplast undergoes meiosis to form
four haploid unicell products (G). (From Norstog and Long, 1976.)
16 Kaplan’s Principles of Plant Morphology

I.

E. n Syngamy
n H. J.
G. 2n 2n
C.
K.
F.
n 2n

D.
n

A. n n L.

P. n Meiosis
R. N.
T.

n
U. n
n
B.
n n

S. M.
Q. O.

FIGURE 2.8 Diplohaplontic life history of the sea lettuce Ulva (Chlorophyta) illustrating a sporic meiosis resulting in the development of an isomorphic
alternation of generations. Beginning with a pair of haploid gametophytic plants, biflagellate anisogametes are released into the seawater (A–F) where
they fuse (G, H) in the process of syngamy to form a quadriflagellate zygote (H). The zygote then settles down and divides up to form a diploid multicel-
lular sporophyte plant that is morphologically identical to the haploid gametophyte (compare L with A and B). Meiosis in cells of the sporophyte produces
quadriflagellate haploid spores (N, O) that settle down on the substratum and undergo mitotic division to form the haploid gametophyte stage (P–S). (From
Scagel et al., 1965.)

this species in the laboratory and follow its life history in detail. Let us trace the life history of this unusual alga in more detail.
If the biflagellate cells released from the thallus fuse to form a The Derbesia or sporophyte phase has a coenocytic body con-
single, quadriflagellate cell (Figure 2.8E–H) which divides to struction, i.e., it is a multinucleate organism in which there is
form a multicellular thallus (Figure 2.8J–L), then it is logical nuclear division (karyokinesis) without concomitant cell division
to conclude that the thallus was derived from the gametophyte (cytokinesis). Hence the plant body is an elaborate, branched sin-
phase because the cells functioned as gametes (Figure 2.8E,F). gle cell containing a large number of nuclei (Figure 2.9J). Cell
If, on the other hand, the cells released do not fuse but settle down partitioning takes place only at the time of reproduction, when
and divide to form a thallus (Figure 2.8N–U), one would deduce globose meiosporangia are formed on the tips of reduced lateral
that they were products of meiosis (zoospores) that were develop- branches (Figure 2.9J,K). Here the diploid nuclei undergo mei-
ing into the haploid gametophytes (Figure 2.8A,B) by mitotic osis to form numerous flagellated meiospores that are released
division of parent cells. In order to validate these deductions, it through a pore in the meiosporangium (Figure 2.9L,M). After
would be necessary to make chromosome counts at all phases of swimming for a short period, each of the haploid spores settles
the life history. In the case of Ulva chromosome, counts provide down on the substrate and develops into a macroscopic, multi-
the evidence for its alternation of isomorphic generations. nucleate vesicle, representing the Halicystis, or gametophytic,
The green alga Derbesia provides a good example of a life his- phase in the life cycle (Figure 2.9A,B).
tory consisting of an alternation of heteromorphic generations. The gametophytes are dioecious (from the Greek dis meaning
Here the gametophytic and sporophytic phases are markedly dif- two and oikos meaning house), bearing male and female gametes
ferent in morphology. In fact, before the details of this life history on separate individuals (Figure 2.9A,B). (Some algae have mon-
were worked out in culture, the two phases were considered to oecious gametophytes that bear male and female gametangia on
be members of two different genera! The branched, tubular spo- the same individual.) The protoplasts of each gametophyte dif-
rophyte was placed in the genus Derbesia, whereas the simple, ferentiate into many gametes, which are forcibly ejected through
spherical gametophyte was called Halicystis. It was only after a pore. Since the biflagellate gametes are unequal in size, they are
the work of Kornmann (1938) that the two were demonstrated to termed anisogamous (from the Greek aniso meaning unequal
be alternate stages in the life history of a single organism. and gamo meaning marriage) (Figure 2.9C,D). Syngamy results
The Cast of Characters 17

2n
2n
I.
n

Syngamy
F.
n
n
E.
D.
G. H.

n
n
C. n

n Meiosis

B.
M.
n 2n

A.
J.
K.
L.

FIGURE 2.9 Diplohaplontic life history with a sporic meiosis and a heteromorphic alternation of generations in the green alga Derbesia (Chlorophyta).
Mature saccate male and female gametophytes of the Halicystis stage (A and B) produce motile anisogametes (C and D) that fuse in the process of syngamy
(E). The resulting unicellular zygote (F) then grows (G,H) and develops into the filamentous, coenocyte, or Derbesia stage (I and J). Globose meiosporangia
along the length of some principal filaments (J) produce multiciliate free-swimming, haploid zoospores as products of meiosis (L and M), that then settle
down on the substratum and undergo free-nuclear development as the saccate gametophyte stage. (From Scagel et al., 1965.)

in the formation of a non-motile zygote cell (Figure 2.9E,F), photosynthetic storage products; 3) cell wall characteristics; 4)
which quickly settles and develops into the branched coenocytic cytological characteristics; and 5) presence and nature of flag-
Derbesia sporophyte (Figure 2.9G–J), and we’re back to where ellation. It is generally assumed that these characteristics have
we started in the life cycle. been evolutionarily conserved. While each major algal division
When we characterize the major groups of land plants, we will may exhibit similar morphologies, the features considered to be
see that they exhibit an alternation of heteromorphic generations the most accurate indicators of their affinity are these basic bio-
similar to the algal example we have just described. In addition, chemical and cytological features. Similarities in morphology in
land plants differ not only in which of the two phases is dominant representatives of the different algal groups are thus considered
but also in whether sporophyte and gametophytes develop as spa- to represent convergent evolution in these separate but parallel
tially separated or organically connected entities. phyletic lines.

The Major Groups of the Plant Kingdom The Green Algae (Division Chlorophyta)
Members of Chlorophyta are characterized by the possession
The Algae
of chlorophylls a and b as their principal photosynthetic pig-
The term “algae” refers to a heterogeneous assemblage of pho- ments with carotenoids and xanthophylls as accessory or light
tosynthetic, eukaryotic organisms. Although some algae are ter- harvesting pigments. Typically, the green algae deposit starch
restrial and even subterranean in distribution, the majority live as the photosynthetic storage product. Green algal morphology
in an aquatic environment. Despite a range of morphology from ranges from unicellular to colonial and includes filamentous,
unicellular to complex multicellular types, the characteristic that sheetlike, parenchymatous, and coenocytic forms. Many of the
most consistently distinguishes the algae from land plants is that unicellular and colonial species are motile by flagellar movement
all of the cells of algal gametangia are fertile and function as (Figure 2.10). Examples of every type of life history outlined
gametes (Bold and Wynne, 1985); unlike the sex organs of land above, including gametic, zygotic, and sporic meiosis patterns
plants, the gametogenous cells are not surrounded by sterile cells. can be found in the green algae. Since the green algae have the
Traditionally, the major algal groups are distinguished on the same photosynthetic pigment systems as the green land plants
basis of 1) photosynthetic pigments; 2) chemical nature of their (Divisions Bryophyta and Tracheophyta), they are considered to
18 Kaplan’s Principles of Plant Morphology

FIGURE 2.10 Morphological diversity in the green algae (Division Chlorophyta). A. Unicellular flagellated cell of Chlamydomonas. B. Plate-like coeno-
bium of Gonium. C. Spherical coenobium Volvox. D. Filamentous form, Spirogyra. E. Net-form in genus Hydrodictyon. F. Organographic differentiation in
coenocytes Caulerpa.

be the ancestors of the land plants that form the major vegetation filamentous to sheetlike to parenchymatous in their construction
on the earth’s surface today. (Figure 2.11). Cell division in this subclass is diffuse or interca-
lary. Thus thalli in Bangiophycidae have no distinct apical meri-
stems. They also lack pit connections between their cells. Sexual
The Red Algae (Division Rhodophyta)
reproduction in Bangiophycidae is relatively rare.
These are eukaryotic plants that are predominantly marine in By contrast, subclass Florideophycidae are strictly multicellu-
distribution but have some freshwater representatives. The group lar and have distinct pit connections between genetically related
is characterized by the possession of chlorophylls a and d with cell lineages of their thalli. They range in morphology from
phycobiliproteins phycoerythrin and phycocyanin as accessory simple filamentous forms to pseudoparenchymatous bodies with
pigments. Photosynthate is stored in a branched, amylopectin- complex regional differentiation (Figure 2.12). In contrast to the
like polymer called Floridean starch. One of the diagnostic Bangiophycidae, in Florideophycidae cell division is predomi-
characteristics of the red algae is the absence of flagellated cells nantly apical with distinct apical meristems. Sexual reproduction
in all stages of their life histories. Cell walls are fundamentally is widespread in Florideophycidae, and many species exhibit a
cellulosic covered by mucilaginous, amorphous matrix material complex triphasic life history, involving free-living haploid
usually comprised of a sulfated galactan polymer. gametophytic and sporophytic phases and a third, reduced phase,
Traditionally, Rhodophyta are considered as comprising a also diploid borne on the female gametophyte.
single class, Rhodophyceae, consisting of two subclasses, the Because they share similar pigment systems with the
Bangiophycidae and Florideophycidae. Bangiophycidae are bluegreens (chlorophyll a plus phycobiliprotein accessory pig-
unicellular to multicellular, and the latter species range from ments) and both groups lack flagellated stages, the Cyanophyta
The Cast of Characters 19

FIGURE 2.11 Morphological diversity in subclass Bangiophycidae of the red algae (Division Rhodophyta). A. Unicellular Porphyridium. B. Uniseriate,
unbranched filaments in Erythrotrichia. C, D. Parenchymatous axes in Bangia. E. Branched filaments in Gonotrichium. F, G. Unistratose flattened plate in
Erythrocladia. H–L. Uniseriate and biseriate blades in Porphyra. (From Scagel et al., 1965.)

FIGURE 2.12 Morphological diversity in subclass Floridiophycidae of the red algae (Division Rhodophyta). A–C. Agardhiella. A. Overall architecture.
B, C. Longisection and transaction, respectively, of thallus showing pseudoparenchymatous nature of construction based on a fundamentally filamentous
cell geometry webbed together by a common wall matrix. D, E. Rhodoglossum showing blade habit (D) and anatomy (E). F, G. Habit and anatomy of
Callophyllis. H, I. Morphology and anatomy of Polyneura. (From Scagel et al., 1965.)
20 Kaplan’s Principles of Plant Morphology

have been considered to be the most logical progenitors of the red Members of Class Xanthophyceae differ from those of
algae. The reds cannot be traced as sources of any of the higher Chrysophyceae and Bacillariophyceae in the lack the carot-
land plants. enoid accessory pigment fucoxanthin. Because of their relatively
greenish appearance, at one time members of this group were
classified with the green algae. However, with the integration
The Golden-Brown Algae (Division Chrysophyta)
modern biochemical and cytological data, the present consensus
The golden brown coloring of members of this division is due is that their affinities are with the golden browns.
to their chlorophylls a and c and carotenoid pigments includ- Members of Class Xanthophyceae range in form from flag-
ing the distinctive xanthophyll fucoxanthin in certain groups. ellated unicells to colonial and even filamentous and coeno-
Food reserves consist of the β-glucan chrysolaminarin, a cytic body plans (Figure 2.13). Hence they overlap in habit and
feature which they share with the brown algae of Division organismal form with species of Chlorophyta and represent a
Phaeophyta. Traditionally, Chrysophyta has been subdivided prime example of convergent evolution between different algal
into three major classes: 1) the Xanthophyceae or yellow-green lines. Most of the members exhibit a haplontic life history with
algae; 2) the Chrysophyceae or golden-brown algae; and 3) the zygotic meiosis.
Bacillariophyceae or Diatoms. Recent treatments recognize as Class Chrysophyceae includes a great diversity of both fresh-
many as six classes for this division (Bold and Wynne, 1985) water and marine organisms. The majority are unicells, but some
but for our purposes of general characterization, we recognize taxa are multicellular-colonial and even filamentous in organi-
just three. zation (Figure 2.14). Some species have their cells bounded by

ch

ch

ey

A. B. C. J. L.

ch

mx

ey ch
F.
G.

E.
ch
ch

ch mx

D. H. I.
M.

N.
ch

K.

FIGURE 2.13 Morphological diversity of class Xanthophyceae of the golden-brown algae (Division Chrysophyta). A, F, and G. Motile forms in the genera
Pseudomicrosportella (A), Xanthophycomas (F), and Heterochloris (G). B–E, I. Coccoid forms in the genera Ophiocytium (B, C), Charraciopsis (D and E),
Chloridella (I); and the amoeboid Rhizochloris (H). Coenocytic forms in J, Botrydium and K, Vaucheria. L. Filamentous form in Tribonema; and palmelloid
forms with a mucilaginous matrix Mischococcus (M) and Chlorosaccus (N). (From Scagel et al., 1965.)
The Cast of Characters 21

FIGURE 2.14 Morphological diversity of class Chrysophyceae of the golden-brown algae (Division Chrysophyta). A and C, motile colonial forms.
A. Synura. C. Uroglena. B. Coccoid form, Epichrysis epiphytic on an algal filament. D, E, and I, palmelloid forms. D, E. Hydrurus. H, I. Chrysocapsa.
F. Amoeboid form with a flagellum (Chrysamoeba). G. branched filamentous form (Pheothamnion). (From Scagel et al., 1965.)

cell walls of various degrees of elaboration, whereas others have which we have mentioned as a sensory pigment in Chrysophyta.
completely naked cells and may even exhibit amoeboid motion Photosynthate is stored as the complex polymer laminarin, man-
(Figure 2.14F) (Bold and Wynne, 1985). nitol, or oil droplets. Cell walls are cellulosic surrounded by a
Bacillariophyceae, the diatoms, is the most distinctive class mucilaginous polymer, alginic acid. Although they exhibit a
in Chrysophyta. Diatoms are unicellular to colonial to filamen- great range in morphology, there are no strictly unicellular,
tous species whose protoplasts are encased in a distinct, two- ranging from filamentous to complex parenchymatous, bodies
parted siliceous cell wall or frustule (Figure 2.15). It is because (Figure 2.16).
this silica cell wall material persists long after its protoplast has Among the algae, the browns exhibit the greatest degree of
died that these organisms are fossilized as “diatomaceous earth.” structural complexity. They exhibit organographic and tis-
Diatomaceous earth is used in various abrasives and as a filter- sue differentiation comparable to that of the higher land plants
ing material. Diatoms are unique in Chrysophyta because of (Figures 2.16, 2.17). The kelps Nereocystis, Macrocystis, and
their lack of flagellated phases in all stages of their life histories. Laminaria, for example, are differentiated regionally into stem
Vegetative diatom cells are haploid; at the time of reproduction, and leaf components, even though their growth and develop-
two protoplasts fuse, followed by zygotic meiosis to restore the ment are markedly different from those in vascular plants
haploid phase in their fundamentally haplontic life histories. (Figure 2.17). They even have phloem tissue in their axes for
Because of their distinctive pigmentation and cell wall chem- rapid conduction of photosynthate produced in the distal blades
istry it is believed that Bacillariophyceae were not the source of (Nicholson and Briggs, 1972). In fact, in the early part of the
land plants. century, the brown algae were considered progenitors of land
plants, and their subtidal to intertidal distribution was cited as
the type of migration from sea to land that was the source of the
The Brown Algae (Division Phaeophyta)
land flora (Church, 1919). Present concepts of plant evolution,
The brown algae are almost exclusively marine, with a few fresh- however, do not support this interpretation. Instead they trace the
water forms. Their photosynthetic pigments consist of chloro- ancestry of green land plants to the Chlorophyta (Graham, 1985).
phylls a and c, β-carotene xanthophylls, including fucoxanthin, The more elaborated members of Phaeophyta are now viewed as
22 Kaplan’s Principles of Plant Morphology

FIGURE 2.15 Morphological diversity in class Bacillariophyceae of the golden-brown algae (Division Chrysophyta). A, B, D, E, centric forms; F–J, pen-
nate forms. A–C, G, unicellular representatives. I, J. Navicula, colonial species. (From Scagel et al., 1965.)

interesting convergences in organization in a parallel but unre- Land Plants

lated plant group. Life histories in members of Phaeophyta range
from alternation of isomorphic or heteromorphic generations to The prevailing view of plant evolution is that the earliest evolu-
the gametic meiosis we have already described for Fucus. tion and diversification of photosynthetic organisms took place
in an aquatic environment and that plants secondarily occupied
the land (Banks, 1970). Thus the predominantly aquatic algal
Other Algal Divisions groups we have just reviewed are considered to be the source
of the land flora. Since green land plants have the same pigment
In our brief review of the algae we have dwelt only on the larg-
systems as the green algae, it is hypothesized that they evolved
est and most conspicuous groups, particularly those that we
from the Chlorophyta, although the specific progenitor is still a
will refer to in subsequent chapters to help interpret the orga-
matter of debate (Graham, 1985; Bhattacharya and Medlin 1998;
nization and development of higher plants. While the Divisions
Leliaert et al. 2012).
Euglenophyta, Pyrrophyta, and Cryptophyta represent biologi-
The diagnostic features of land plants are: 1) cutinized spores;
cally fascinating groups, they repeat some of the same themes we
2) stomata; 3) cuticle on their plant surfaces; and 4) a vascular
have already discussed and will not be treated in this book. The
system (Banks, 1970). Compared to life in an aquatic environ-
interested reader is directed to a general phycology text, such as
ment, that on land is a relatively desiccating one. The devel-
that by Bold and Wynne (1985).**
opment of a lipid cuticle on plant surfaces and spores reduces
water loss in the land environment. Likewise, the presence of
stomata as portals of gas exchange between the surrounding
** The reader is also referred to more recent work that characterizes pat-
terns of algal taxonomy, systematics, and evolution, such as Cock et al. air and plant tissues is a significant feature for habitation of
Nature 465,617–621 (Brown algae); Bhattacharya & Medlin 1998 Plant the land. Obviously, these criteria are useful for the evaluation
Physiology 116(1),9–15 (Algal phylogeny and the origin of land plants). of fossil plants because they are the characteristics that would
The Cast of Characters 23

ac ac

Ectocarpales N.

L.
M.
A. B. Syringoderma
O.

C. J. Dictyota P.

Sphacelaria
Ectocarpus

D. E. Q. R.
I.
K.
me

F.

Laminaria
im
im Macrocystis
S. T.
U.

H.
Desmarestia
Leathesia G.

FIGURE 2.16 Diversity in growth forms in brown algae (Division Phaeophyta). A–F. Unbranched and branched filaments exhibiting apical growth (A, B,
D, and E) and intercalary growth (F and G) as well as pseudoparenchyma formation in Leathesia (H). I–U. Parenchymatous forms, including the transition
from filamentous to parenchymatous anatomy in Sphaceleria (I–K), plate development in Syringoderma (L, M) and Dictyota (N–R) as well as multiseriate
blade development in the kelps Laminaria and Macrocystis (S–U). ac, apical cell; im, intercalary meristem; me, meristoderm. (From Scagel et al., 1965.)

F.
E. H.
G.

T
D.
A. B. C.

FIGURE 2.17 Morphological diversity and structural range in larger parenchymatous kelps in the brown algae (Division Phaeophyta). A. Bull kelp
Nereocystis. B. Laminaria cloustoni with red algal epiphytes growing attached to its stipe. C. Alaria with fertile leaflets on its stipe. D. Laminaria sac-
charina with a new blade below its old one. E. Saccorhiza showing bulb formation above the first holdfast. F. Macrocystis mature plant. G. Young plant of
Macrocystis showing stipe bifurcation. H. Growing ends of the frond, illustrating the splitting process that delimits derivative fronds. (From Corner, 1964.)
24 Kaplan’s Principles of Plant Morphology

photosynthetic phase and the sporophyte is reduced and simple

by comparison and undergoes its entire development attached to
the parent gametophyte (Figure 2.18A). Typically, three classes
or subdivisions are recognized: 1) the Anthocerotopsida or horn-
worts; 2) the Hepaticopsida or liverworts; and 3) the Bryopsida or
mosses. In all three groups the gametophyte generation bears the
archegonia, the female gametangia which produce the eggs and
the antheridia, the male gametangia, which produce the sperm.
The three classes of Bryophyta can be distinguished princi-
pally on the distribution of growth in the sporophyte (Doyle,
1964). In all three groups, the mature sporophyte is differenti-
ated into: 1) a basal foot or region of nutrient absorption from the
parent gametophyte; 2) a terminal capsule or sporangium where
the meiospores are produced; and 3) a seta or stalk between the
capsule and foot. Sporophytes of the hornworts grow by means
of an intercalary meristem between the foot and the capsule. As
a result of the prolonged basal meristematic activity, new sporog-
enous and sporangial tissues are produced continuously for the
FIGURE 2.18 Comparison between a bryophytic life history (A), where life of the sporophyte. Thus the tip of the capsule in Anthoceros
the gametophyte is dominant and the sporophyte remains attached, and a is the most mature and the base the least mature. As the spores
pteridophytic life history pattern in B, where it is the sporophyte which is and capsule tissues mature at the tip of the capsule, the cap-
free-living and dominant and the gametophyte is independent and reduced. sule dehisces and disperses spores into the air (Figure 2.19A).
(From Stewart, 1983.)
The basal growth of the sporophytes in Anthocerotopsida is

be preserved. These criteria give some indication when, in the

earth’s history, plants first migrated onto the land.
Two major groups of land plants are generally recognized:
1) Division Bryophyta and 2) Division Tracheophyta. The
Bryophyta include the hornworts, liverworts, and mosses and
are generally considered to be nonvascular plants. Tracheophyta
includes all vascular plants that possess distinct conducting sys-
tems, xylem for the transport of water and mineral elements,
and phloem for the transport of organic molecules, principally
sugars. Since some of the larger Bryophyta have internal vascu-
lar systems and conduction (Hébant-Mauri, 1977) which, at the
very least, converge with those of Tracheophyta, the distinction
between these groups based on the differentiation of vascular tis-
sues alone is not entirely clear.
A more fundamental distinction between the major groups of
land plants has been the nature of their reproductive life histo-
ries. Members of both divisions exhibit an alternation of hetero-
morphic generations in which the sporophyte and gametophyte
are structurally different from one another. However, the two
groups differ in the degree of dominance and structural connec-
tion between the two generations. In the bryophytes, the haploid
phase or gametophyte generation is the dominant phase of the
life cycle and the diploid sporophyte generation is reduced and
undergoes its entire development attached to the parent game-
tophyte (Figure 2.18A). In the tracheophytes, by contrast, the
sporophyte is the dominant phase and the gametophyte genera- A. B.
tion is reduced (Figure 2.18B). Furthermore, in contrast to the
attached and dependent nature of the bryophyte sporophyte, the
tracheophyte sporophyte is ultimately independent of the game-
tophyte (Figure 2.18B).
C.

Division Bryophyta FIGURE 2.19 Morphology and structural relationship of sporophyte

to gametophyte in three classes of Bryophyta. A. Anthoceros laevis in
This group of land plants is characterized by an alternation of het- Anthocerotopsida. B. Marsupella sprucei in Hepaticopsida. C. Dawsonia
eromorphic generations where the gametophyte is the dominant superba in Bryopsida. (From Scagel et al., 1965.)
The Cast of Characters 25

responsible for the extended, linear nature of their capsules com- Lycophyta today is a relictual group which was much larger and
pared to those in the other two classes (Figure 2.19). more diversified in the Carboniferous period some 350 million
By contrast, sporophytes in class Bryopsida, the mosses, have years ago. While there were numerous genera at the time of
an apical meristem at both poles of the embryonic sporophyte; the group’s zenith, only six genera in three orders persist
hence sporophytic growth in Bryopsida is bipolar. Sporophytic today: Lycopodium, Lydopodiella, Phylloglossum, Huperzia
growth in the liverworts of Class Hepaticopsida is not localized (Lycopodiales), Selaginella (Selaginellales), and Isoetes (incl.
in discrete meristems but instead is diffuse within the sporophyte Stylites, Isoetales). All lycopods have their sporophytes differen-
body. The simultaneous maturation of spores in the capsule of a tiated into root, stem, and leaf. Lycophytes bear their sporangia
liverwort as compared with successive maturation in the capsule on the adaxial surfaces of specialized sporophylls, which may or
of a hornwort emphasizes this difference in growth distribution may not be aggregated into distinct cones or strobili at the distal
in these two groups. ends of their shoot branches (Figure 2.26A).
In contrast to the simplified, relatively stereotyped morphol- Although all five lycophyte genera share the basic type of life
ogy of the sporophytes, gametophyte morphology in Bryophyta history we have characterized previously for the ferns, Selaginella
is much more varied and exhibits a greater degree of organo- and Isoetes (incl. Stylites) exhibit the phenomenon of heterospory.
graphic differentiation. For example, whereas gametophytes All members of Bryophyta and Tracheophyta that we have
in Anthocerotopsida are flattened, dorsiventral, dichotomously described thus far are homosporous (from the Greek homo
branched, and regionally undifferentiated (Figure 2.19A), meaning similar and sporous referring to seeds or spores). They
those in Hepaticopsida range from thalloid to shoot-like clearly produce only one kind of spore. Germination of that single spore
differentiated into leaf and stem, resembling those of higher type results in the development of exosporic gametophytes that
plants (Figure 2.19B). Moss gametophytes are likewise shoot- undergo their development principally outside of the original
like with leaves initiated from the shoot apex in a distinctive, spore wall (Figure 2.26D–F). Sexual differentiation in exo-
three-ranked pattern (Figure 2.19C). Interestingly, in both sporic gametophytes is not expressed until after they form arche-
gametophytes and sporophytes of some of the larger polytri- gonia and/or antheridia (Figure 2.26G–I).
choid mosses, such Polytrichum and Dawsonia, not only do the Species with a heterosporous life history produce two different
gametophores converge with shoots of higher plants, but the spore types, hence the term heterospory (from the Greek hetero
plants also have the equivalent of vascular tissues. Evidence of different, and sporous, to seeds or spores). The two spore types
this kind has led some systematists to see an evolutionary rela- differ not only in size but also in the sexual determination of
tionship between mosses and other Tracheophyta (Mishler and their gametophytic products. The larger megaspores form the
Churchill, 1984). female or megagametophytes, and the smaller microspores
form the male or microgametophytes (Figure 2.27E,G,I,K
and H,J,L). Microspores are formed in a microsporangium
Tracheophytes
(Figure 2.27D,E) whereas megaspores are differentiated in a
The tracheophytes are also known as the vascular plants, those megasporangium (Figure 2.27D,F). The developmental basis
land plant groups whose bodies have evolved vascular tissues of heterospory is that in the megasporangium all the spore
specialized for long distance transport. The diploid sporo- mother cells except one degenerate. The remaining megasporo-
phytic phase of the tracheophyte life history is elaborated and cyte undergoes meiosis to form a tetrad of four large haploid
ultimately develops independent of the reduced gametophyte megaspores (Figure 2.27D). Presumably, nutrients released by
phase (Fig. 2.18B). The vascular land plants of today exhibit the nonfunctional spore mother cells are absorbed by the devel-
differentiation of the three major plant organs - stem, leaf, and oping megaspores, which allows them to become larger than the
root - that we characterized briefly in Chapter 1. Within the tra- microspores (Figure 2.27D). All the spore mother cells in the
cheophytes, taxonomic divisions are used to define evolution- microsporangium undergo meiosis and result in the formation of
ary lineages that will be discussed independently. These are numerous, small microspores (Figure 2.27D).
the Lycophytes (Division Lycopodiophyta), the Pteridophytes In addition to the difference in size and sex of the spores,
(Division Pteridophyta, including classes Pteridopsida [lepto- heterospory is also characterized by the endosporic devel-
sporangiate ferns], Marattiopsida [eusporangiate tree ferns], opment of gametophytes. In endosporic development (from
Sphenopsida [horsetails], and Psilotopsida [wisk-ferns]), and the Greek endo- meaning inside, and sporic meaning spores) the
Spermatophytes (Gynmosperms and Angiosperms). haploid spore proliferates of into a multicellular gametophyte
within the original spore wall (Figure 2.27E,G,I,K) A conse-
quence of endosporic gametophyte development is that it lim-
Division Lycopodiophyta (Lycophyta,
its the size and degree of elaboration of the gametophyte. For
“Lycophytes” or “Lycopods”)
these reasons the gametophytes in the heterosporous clubmoss
The Lycophyta comprise a lineage of vascular plants that is sister Selaginella, for example, are relatively few-celled and markedly
to all remaining vascular plants. They are known as the “club- simplified in structure in comparison with their exosporic coun-
mosses” because their small-leaved, bushy habit is reminiscent terparts in ferns (including Psilotum and Equisetum) (compare
of the mosses in Bryophyta. In fact, many clubmosses can be Figure 2.27I and J with 2.26G, 2.24H, 2.23H and 2.22G). The
found in the same moist, shaded habitat as true mosses. The sig- male or microgametophyte that develops from the microspore of
nificant difference is that the lycopods are true vascular plants Selaginella is the equivalent of an antheridium within the origi-
and have a pteridophytic life history with a dominant, indepen- nal spore wall (Figure 2.27I). The female or megagametophyte
dent sporophyte and a reduced independent gametophyte. which develops from the megaspore is larger and has many more
26 Kaplan’s Principles of Plant Morphology

cells than the microgametophyte because it arose from the sig- Class Pteridopsida
nificantly larger megaspore, but it is much smaller and less elabo-
rate than exosporic gametophytes (compare Figure 2.27J with The Pteridopsida, or leptosporangiate ferns, are the largest and
2.26G). Moreover, the Selaginella megagametophyte is very most diversified class within the pteridophytes. They are also cur-
simple in structure, consisting of a parenchymatous tissue with rently referred to as a subclass of ferns, the Polypodiidae. Members
archegonia along its periphery (Figure 2.26J,L). Proliferation of this group occupy the widest variety of habitats and exhibit
of megagametophyte tissue at the time of fertilization forces the greatest diversity of life forms, including trees and vines,
the spore wall apart, exposing the archegonia for fertilization submerged and floating aquatic species, and epiphytes of great
(Figure 2.27J,M). Undoubtedly the significance of the marked diversity. Only the leptosporangiate ferns come close to exhib-
difference in spore size between megaspores and microspores iting the diversity of adaptations that the dominant plant group
in heterosporous plants such as Selaginella is that the megaga- today, the flowering plants, exhibit. Interestingly, in the ferns the
metophyte must be more massive in order to nourish the young leaf component of the shoot carries out most of the functional
sporophyte until it is large enough to be photosynthetic and nutri- roles expressed by the entire shoot of seed plants. Not only is the
tionally independent (Figure 2.27O,P). Since Selaginella is free- frond the principal organ of photosynthesis, but in many species
sporing—that is, it disseminates its spores away from the parent it also bears the reproductive structures (i.e., the sporangia). In
sporophyte—the size and nutrient content of the megaspore and all the other vascular plants sporangia are borne on specialized
the megagametophyte must be sufficient to support the gameto- reproductive appendages, called sporophylls (sporo referring to
phyte some distance from its parent sporophyte (Figure 2.27Q). spore or seed and phyll meaning leaf), which are spatially seg-
The homosporous genera of Lycophyta, Lycopodium, and regated from the purely photosynthetic leaves or trophophylls
Phylloglossum, have exosporic gametophytes but differ in mor- (from the Greek tropho, feeding and phyllo leaf) of the vegeta-
phology and habit. Some species of Lycopodium, for example, tive portion of the shoot. The sporangia are borne on the abaxial
have annual gametophytes that are green and photosynthetic or morphological undersurface of the frond (Figure 2.20A,B).
whereas others, including the genus Phylloglossum, have long- Although the majority of ferns are homosporous and exosporic
lived subterranean gametophytes that are non-green and depen- (Figure 2.20C-F), heterospory can also be found in this group.
dent upon an endophytic fungus for nutrition. Mycorrhizal fungi The aquatic ferns of the families Marsileaceae and Salviniaceae,
also invade the tissues of the green gametophytes in Lycopodium, both in the order Polypodiales, are heterosporous with endo-
but the latter are principally autotrophic. sporic gametophyte development. Interestingly, if one looks at

Meiosis

Annulus
C. D.
Mature, Spore Germinating
Sporogenous dehiscing (n) spores
Sorus
tissue (2n) sporangium
with spores (n) E.
B.
Immature sporangium
Young gametophyte (n) Rhizoid
F.
Leaf
(megaphyll)

Sori

G.
Adult sporophyte (2n)

Mature gametophyte
Young leaf (prothallus) (n) Rhizoids
Rhizome

A. Egg
Adventitious roots (n) Spermatogenous
tissue (n)

H. I.
Immature Immature
archegonium antheridium
Leaf of young Egg
sporophyte (n)
Gametophyte Zygote
(2n)
P. Foot Mature
L. archegonium
Shoot apex Syngamy Mature
Rhizoids Sperm J. antheridium
M.
Root Young (n)
First leaf N. embryo K.
First root
O. Embryo

FIGURE 2.20 Life history pattern in a representative fern, showing an independent, free-living sporophyte generation differentiated into leaf stem and
root (A). The sporophyte bears sporangia (B) which is the site of spore formation (B,C). Spores are released and germinate (C) to produce a free-living
gametophyte generation (E-G) bearing the gametangia (H,I) where the gametes (L,J-K) are produced. Fusion of gametes results in the development of the
next sporophyte generation (M-P).
The Cast of Characters 27

the fossil representatives of both Sphenopsida and Lycophyta, sperm to be released, and they swim in films of water to the
one finds heterospory developed in various extinct members of egg (Figure 2.20I–L), which is retained within the base of a
these groups as well. Thus this mode of sexual expression may flask-shaped archegonium. A sperm swims down the neck of the
have evolved relatively early in the history of vascular plants. archegonium and fertilizes the egg (Figure 2.20L). Fusion of
Figure 2.20 illustrates the life history of a fern of the family sperm and egg in the process of syngamy results in of a diploid
Polypodiaceae. The sporophyte generation is differentiated into (2n) cell, the zygote (Figure 2.20M). The zygote then under-
shoots bearing roots (Figure 2.20A). The most conspicuous ele- goes mitosis division to form a multicellular plant embryo, dur-
ments of the shoot are the leaves, which tend to be large with ing whose development the major organographic regions of the
greatly dissected blade surfaces. They are called fronds. Fern sporophyte become defined (Figure 2.20N,O).
fronds function not only as the plant’s principal photosynthetic During its early development the young fern sporophyte is
surface but also bear the reproductive structures, the sporangia, attached to and nourished heterotrophically by the parent game-
in aggregations called sori, on their underside or abaxial surface tophyte (Figure 2.20P). As the young sporophytic plant enlarges
(Figure 2.20A,B). Haploid spores are produced in each sporan- and unfolds its own leaves, it becomes self-supporting by its own
gial primordium by meiosis of diploid spore mother cells. photosynthesis. As it continues to grow, it enlarges beyond the
Once the spores have been released from the sporangium limits of the gametophyte and becomes established as the inde-
(Figure 2.20C,D), they are carried by wind some distance from pendent, free-living diploid generation with which we began our
the parent sporophyte. If the environmental conditions are right, life cycle description (Figure 2.20A).
the spores germinate and give rise to an initially green, haploid, This broad outline of the fern’s life history is characteristic of
filamentous structure, the beginning of the gametophyte gen- all the Pteridopsida, with some modifications in the other classes
eration (Figure 2.20E). Cells of the filamentous gametophyte represented below.
divide in two dimensions to form a heart-shaped prothallus.
During successive periods of its development, the fern gameto-
Class Psilotopsida
phyte will form male (antheridia) and then female (archegonia)
sex organs or gametangia mostly on its lower (or ventral) surface This is a small lineage of pteridophytes, whose common name
(Figure 2.20G-I). Most fern prothalli are green and photosyn- is the “whisk ferns,” consists of only two genera, Psilotum and
thetic and undergo an independent existence spatially separated Tmesipteris. Both have representatives that grow either as ter-
from their parent sporophytes (Figure 2.20G). restrial or epiphytic species (Figure 2.21F,G). Their shoots
The antheridia and archegonia give rise to the fern’s gametes, consist of a subterranean, horizontally growing rhizomatous
the sperm and eggs. Fern sperm are motile and multiflagellate. portion, the branches of which turn upward and grow erectly.
Uptake of water by the antheridia causes the free-swimming The aerial shoots of Psilotum bear small, scale-like leafy

G.

A.

B.

D.

E. F. C. H. I.

FIGURE 2.21 General organography of members of class Psilopsida. A–F. Psilotum nudum. A. Overall form of shoot. B. Reduced undivided scale leaf
borne on vegetative portion of shoot. C. Synangial-bearing reproductive part of a shoot axis. D, E. Detail of tripartite synangia borne on adaxial surface
or bifid sporophyll. F. Clumps of Psilotum growing in axils of persistent leaf bases of a palm. G–I. Tmesipteris tannensis. G. Epiphytic habit growing off
the surfaces of a tree fern. H. Detail of shoot showing vertically planated leaves and bifid sporophylls, bearing bisporangiate synangia (I) on their adaxial
surfaces. (From Norstog and Long, 1976.)
28 Kaplan’s Principles of Plant Morphology

appendages (Figure 2.21B), have elongated internodes, and such as Psilotopsida. The vascular plant taps the fungus for
exhibit extensive dichotomous branching (Figure 2.21A). The its nutrients.
aerial shoots of Tmesipteris have shorter internodes, are rela- Because of the close morphological resemblance of the game-
tively unbranched, and bear larger, vertically planated foliar tophyte and sporophyte, their rootless nature, and their retention
appendages (Figure 2.21G,H). In both genera two or more of a primitive dichotomous branching system, the Psilotopsida
sporangia are united to form a compound structure called a have been considered a primitive plant group reminiscent of the
synangium (from the Greek syn- meaning with or united and most ancient vascular plants. However, recent studies have also
angium meaning vessel). The synangia are inserted on the suggested that their structural simplicity may reflect evolution-
adaxial or upper surface of the sporophylls or sporangial bear- ary reduction in relation to their epiphytic habit (Kaplan, 1977).
ing leaves (Figure 2.21C-E, H and I). Sporophylls in Psilotum Because the group has no fossil record, its true systematic affini-
and Tmesipteris differ from the purely vegetative leaves borne ties and evolutionary status remain problematic.
lower on their shoots in having a pair of blade lobes instead
of the single blade (Figure 2.21E,I). The sporophytes of
Psilotopsida differ most significantly from those of most other
Class Sphenopsida
Tracheophyta in their complete lack of roots at all stages of
their development. The Sphenopsida, also known as Equisetopsida, are another
The spores of Psilotopsida germinate to form cylindrical lineage of pteridophytes comprising only a single living genus,
gametophytes, which except for their possession of archegonia Equisetum, commonly called the “scouring rush” because of the
and antheridia are morphologically indistinguishable from the deposition of silica on and in the walls of the epidermal cells
underground portion of the sporophyte (Figure 2.22, compare of its stems, or the “horsetail” because the extensive branching
A with H). In contrast to the gametophytes of most ferns, those pattern of the shoots of some species gives the appearance of the
of Psilotum and Tmesipteris are non-green, subterranean, and tail of a horse (Figure 2.23A). The sporophytes of Equisetum are
dependent upon a symbiotic (mycorrhizal) association with a differentiated into leaf, stem, and roots, and the shoot system has
fungus for their source of nutrition (Figure 2.22I). In a mycor- a distinctive morphology which is diagnostic for members of this
rhizal association, the fungal partner lives off of dead, decay- class (Figure 29A,B). The stem is markedly differentiated into
ing organic matter and invades the tissues of a higher plant’s nodes and internodes with reduced, scale-type leaves fused into
subterranean organs, usually roots of a higher plant or the distinct whorls at each node (Figure 2.23C). In Equisetum the
subterranean stems and gametophytes of lower vascular plants stem internodes are green and photosynthetic, and the leaves play

Immature
sporangium Spores
Meiosis

Spore
mother cells Spore F.
(2n) (n) Germinating spore
C. E.
Mature
sporangium Young gametophyte
Sporogenous Scalelike
Scalelike
B. tissue outgrowth
Immature outgrowth
(2n) D. G.
sporangium Antheridium

Sporangia Archegonium

Rhizoids
Scalelike
outgrowth

Mature
sporophyte (2n)

Aerial stem
A.
Spermatogenous
Rhizome Immature
tissue (n)
archegonium H.
Mature archegonium Gametophyte
Mature antheridium (n)
Shoot apex Egg
(n)
Calyptra
Symbiotic
Young fungus Sperm (n)
N. sporophyte

Foot
M. Immature archegonium I.
Embryo
L. Young embryo K. J. Immature
Syngamy antheridium
Sperm (n)
Gametophyte
Egg (n)
Gametophyte Zygote (2n) Archegonium
Gametophyte

FIGURE 2.22 Life history of the whisk fern, Psilotum nudum, exhibiting a heteromorphic alternation of generations, with an independent sporophyte
differentiated into leaf and stem but without roots (A–D) and a free-living subterranean, mycorrhizal gametophyte (F–L).
The Cast of Characters 29

Haploid spores released from the parent sporophyte are car-

Strobilus ried by wind to a new site some distance from the parent plant
(Figure 2.24D). If the conditions for germination are right,
Sporangiophore the spores will develop into lobed, haploid gametophytes
(Figure 2.24E-H). Depending upon environmental conditions
Equisetum gametophytes can be either male or female; if female,
F. they can produce antheridia after the archegonia have been
formed. The sperm are multiflagellate and swim in films of water
E. to the archegonia where they fertilize the egg to give rise to the
new sporophyte generation (Figure 2.24I-P).
While present-day Sphenopsida consists of only the genus
Equisetum, the group has a much richer fossil history and was
Leaves large and diversified in the past history of the earth. During the
Carboniferous period of the Paleozoic Era, Sphenopsida was
one of the dominant groups in the swamp forests. At that time
the giant horsetails of the genus Calamites were major elements
of the vegetation. Such plants had much the same overall mor-
phology as contemporary Equisetum, and therefore there is little
doubt of the evolutionary relationship between the present and
past representatives of this class (Figure 2.25).
C.

Fertile Embryophyta (Seed Plants)

shoot
Today’s seed plants form the dominant element of the floras of
Rhizome the world. They consist of two major groups: the Gymnosperms
D. and the Angiosperms or flowering plants. In both of these groups
Sterile the sporophyte generation initially develops within the confines
shoot of the seed, which is made up of both sporophytic and gameto-
PF phytic tissues and which has become the unit of dispersal and
A. B.
Root establishment in these plant groups. In contrast, in pteridophytes
it is the spore which is the unit of dispersal and gives rise to
FIGURE 2.23 Organography of the horsetail Eguisetum sylvaticum (Class the gametophyte.
Sphenopsida). A. Morphology or sterile aerial shoot exhibiting differentia-
tion into nodes and internodes with whorls of reduced scale leaves at each
node (C). Whorls of lateral branches have grown out at the upper nodes (A). Concept of the Seed
Each aerial shoot is an outgrowth from a plagiotropic subterranean rhizome
(B). In this species, spores are borne on a separate non-green unbranched Now that we have defined the features of heterospory in plants
aerial shoot which terminates in a cone consisting of whorls of peltate spo- we can proceed to the next step in the refinement of plant life
rophylls (D–F). (From Norstog and Long, 1976.)
history relationships, namely the development of the seed habit.
In order to understand what a seed is, we need to review the high-
only a limited role in overarching and preventing desiccation of lights of heterospory in Selaginella in a theoretical context.
the terminal bud (Figure 2.23B,C). Shoot branching is lateral, Instead of releasing its megaspores from its megasporangia,
and branches are initiated from the nodes inside of the leaf sheath suppose our Selaginella plant retained them within a megasporan-
and break through the sheath as they emerge (Figure 2.23A,C). gium borne on the shoots of the parent sporophyte (Figure 2.27).
The aerial shoots of Equisetum are outgrowths of a subterra- Under such conditions the megagametophyte would be nourished
nean rhizome system. The horizontally growing rhizome bears by the photosynthetic sporophyte, and the megaspore wouldn’t
scale leaves and roots at the nodes (Figure 2.23B). The rapid have to be as large because it wouldn’t have to store nutrients.
horizontal spread of the underground rhizome system permits Megagametophyte proliferation would be at the expense of nutri-
the plants to colonize a large area. ents contained in the megasporangium, which would draw its
The sporangial bearing portion is segregated from the vegeta- sugars from the shoot upon which it was borne.
tive part of the shoot and located at the tip of the main axis or If fertilization of Selaginella’s megagametophyte were to
branches or both (Eames, 1936) (Figure 2.23D,E). The sporo- occur while it was retained by the sporophyte, we would have the
phylls are aggregated in whorls in a terminal cone or strobilus next sporophyte generation developing on the preceding sporo-
(Figure 2.23E). Each sporophyll is polygonal in outline and pel- phyte generation and contained within the tissues of the gameto-
tate (umbrella-shaped) in shape, bearing from five to ten spo- phyte generation (Figures 2.27, 2.28). This is the seed habit. A
rangia on its undersurface (Figure 2.23F). When the cone is report by Lyon (1901) that sporophytes in Selaginella rupestris
mature, the short internodes elongate, separating the sporophylls can develop in megaspores retained on the parent sporophyte
from one another and allowing the sporangia to dry, and release suggests that some features of the seed habit can be developed
their spores (Figure 2.24A-C). here too.
30 Kaplan’s Principles of Plant Morphology

Sporogenous
Strobilus tissue (2n) Germinating Rhizoid
spores
F.
Meiosis Spores
Elaters E. Young Gametophytes G.
Mature (n)
sporangium D. Rhizoids
Sporangiophore
Immature
sporangiu
C.
Archegonium
Antheridium
B. Strobilus

Leaves
H. Rhizoid Gametophyte
(n)
Mature sporophyte (2n)

Node
Internode Spermatogenous
Branches
tissue
(n)
Egg
Rhizome (n)
I. Immature
Archegonium
A.
Adventitious Immature
roots Shoot apex Antheridium J.
Leaf
First leaf
Sperm Sperm
(n) (n)

Archegonium

Root Egg
Mature
Foot Young Syngamy Mature (n) K. Antheridium
Zygote
Gametophyte
O. embryo N. archegonium L.
P. (2n)
M.

FIGURE 2.24 Life history pattern in Equisetum, showing its heteromorphic alternation or generations with a free-living sporophyte differentiated into leaf
stem and root (A–C) and a free-living photosynthetic gametophyte generation (F–M).

Interestingly, heterospory in seed plants is not expressed by

the marked difference in spore size that we see in Selaginella.
In seed plants not only may microspores and megaspores be
nearly the same size but in some instances the megaspore may
be smaller (Thompson, 1927). The lack of disparity in spore size
in seed plants which retain their megaspores in the ovule can be
interpreted in relation to the free-sporing habit we have already
mentioned for Selaginella. Retention of the megaspore by the
ovule means that it does not need a great deal of reserve storage
because the megagametophyte will be nourished during its devel-
opment by the parent sporophyte. For this reason, seed plants
do not need to have an enlarged megaspore. It suggests that the
size difference between male and female spores in heterosporous
lycopods such as Selaginella is related simply to these nutritional
requirements of free-sporing heterosporous species rather than
a basic difference related to sex differentiation. In seed plants
heterospory is expressed mainly by the sexual differences rather
than by spore size.
A seed is the developmental product of an ovule. An ovule
is defined as an integumented megasporangium in which the
megaspore is retained and develops its gametophyte while it is
attached to the parent sporophyte. The integument is a collar-
like growth that surrounds the megasporangium or nucellus
(Figure 2.28C). In the mature, fertilized seed, the integument
develops into the seed coat or protective layer(s) of the seed
FIGURE 2.25 Reconstruction of the fossil horsetail Calamites carina-
tus from the Carboniferous period of the Paleozoic. Despite its antiquity, (Figure 2.29).
note its fundamental resemblance to modern species of Equisetum. (From In seed plants the haploid microspores formed in the micro-
Stewart, 1983.) sporangia will undergo mitotic division to form an endosporic
The Cast of Characters 31

Sporogenous
Meiosis
tissue
(2n)

Spores
(n) E.
Germinating spore
C. Sporophyll
(n)
F.
Sporangium Young
D. Rhizoids
gametophyte
Sporophyll Sporangium
B. Immature
Strobili Strobilus
sporangium
Archegonia Antheridia

Leaves
(microphylls)
G.

Aerial
stem Symbiotic
Rhizome
fungus
Mature sporophyte (2n) Gametophyte
(n)
H. Spermatogenous
Immature tissue (n)
archegonium Egg
(n)
Rhizoids Sperm
Adventitious root
I.
Gametophyte (n)
Immature
antheridium
Suspensor Mature
Shoot apex
archegonium
A.
Root First leaf Sperm
(n)
J.
Gametophyte Egg
Syngamy
(n) Mature K.
Foot Root M. L. antheridium
Young Young embryo Zygote
N.
sporophyte (n)

FIGURE 2.26 Life history pattern of the clubmoss genus Lycopodium (Class Lycopsida). Note this clubmoss exhibits a homosporous life history whereby
a single spore-type is produced (D) which develops into the tree-living subterranean, mycorrhizal gametophyte (F, G).

Microspore (n)
Microsporanger

Ligule
Meiosis E. Microspore (n)
Sporogenous
tissue
Immature microgametophyte Spermatogenous
(2n) Microspore
inside microspore wall tissue (n)
Ligule G. I.

Meiosis
Megaspore (n)
Megaspore (n) Sperm (n)
C. Immature micro Megasporangium Archegonia
or megasporangium Megasporophll F. H.
D. Ligule Megagametophyte protruding K.
B. Strobilus
Strobilus from microspore wall Rhizoids
Mature
microgametophyte
(n)
Mature megagametophyte
inside megaspore wall (n)
J.
Strobilus

Adventitious root
Egg (n)

L. Archegonium Sperm (n)

Leaf (microphyll) 2 Celled

embryo
First leaves Suspensor Rhizoids
Sperm
A. Stem Root (n)
Shoot apex
Mature
sporophyte Stem Egg
(2n) Leaf
Foot (n)

Megaspore wall Syngamy

Young sporophyte M.
attached to gametophyte Root Megaspore wall N.
Q. O. Zygote
Young embryo
P. Megametophyte inside archegonium (n)

FIGURE 2.27 Life history of the heterosporous clubmoss genus Selaginella (Class Lycopsida). In contrast to the homospory in Lycopodium, two different-
sized spores are produced by the sporophyte (E and F) which in turn produce male and female gametophytes, respectively (H and I).
32 Kaplan’s Principles of Plant Morphology

A. B. C.

FIGURE 2.28 Diagrammatic relationship between homospory (A), hetero-

spory (B), and the development of the seed habit (C) whereby the megaspore
is retained in the megasporangium and megagametophyte development
occurs within the integumented megasporangium or ovule. I, integument;
M, megasporangium or nucellus; S, megaspore; G, female or megagameto-
phyte. (From Banks, 1970.)

microgametophyte or pollen grain. When mature, the pollen

grains are shed from the microsporangia and carried by wind or
an animal to the ovule. There the pollen grain germinates and FIGURE 2.29 Structure of a mature, fully developed seed in a gymno-
sperm which developed from fertilization of an ovule like that shown in
puts out a pollen tube that grows through the tissue of the mega- Figure 2.28C. (From Foster and Gifford, 1974.)
sporangium carrying the sperm cells to the egg for fertilization
(Figure 2.30).
In the ferns and all the lower vascular plants we have described, years ago. For example, heterospory has been reported in certain
because the sperm are motile and swim to the archegonia, it is fossil Sphenopsida and Lycophyta. Within Lycophyta the seed
not necessary for their spores to be deposited precisely on the organ genus Lepidocarpon exhibited remarkable ovule structure.
surface of the archegonial-bearing portion of the gametophyte. The subtending megasporophyll folded upward around the mega-
But in seed plants not only are microgametophytes transported sporangium and functioned like an integument (Figure 2.31).
to the nucellus of the ovule by wind or an animal, but the male Whether such an “integument” ultimately matured and served as
gametes or sperm are brought to the egg by a pollen tube which a true seed coat is unclear. The point is that there were parallel
grows through nucellar tissue. Only the cycads and Ginkgo attempts at the evolution of the seed habit within various vascu-
biloba among seed plants have flagellated sperm that swim to lar plant lines before it was established in today’s gymnosperm
the archegonia and fertilize the egg. In these species the pollen precursors (Stewart, 1983.)
tube seemingly plays a role in nutrient absorption rather than just The two major groups of contemporary seed plants, gymno-
gamete transfer (Friedman, 1987). sperms and angiosperms, differ principally in how their ovules
Once the egg in the archegonium is fertilized by a sperm cell, are borne on their shoot systems as well as in their modes of
a diploid zygote is formed which proliferates to form the embry- pollination and sources of seed nutritive tissues. The term gym-
onic sporophyte. The young sporophyte grows at the expense nosperm (from the Greek gymno, naked and sperm, seed) refers
of nutrients deposited in the surrounding gametophyte tissues. to so-called naked-seeded plants or those whose ovules are not
With the onset of dormancy, the embryonic sporophyte ceases its enclosed in an investing structure. As a result of their lack of enclo-
growth and organogenesis and the seed is ready to be dispersed sure, seeds of gymnosperms exhibit what has been called direct
to its new environment where the new sporophyte generation pollination; that is, the pollen is usually transferred directly to
will become established (Figure 2.30). Thus the mature ovule the nucellus and germinates on its surface (Figure 2.32E,G). In
or seed consists of: 1) parent sporophytic tissue (integument and addition, the megagametophyte tissue inside the ovule serves as
remains of the nucellus of the ovule); 2) some remains of the the nutritive tissue for the developing sporophytic embryo.
megagametophyte tissue that was a source of nutrition for the Angiosperms (from the Greek angio, vessel and sperm, seed)
young sporophyte; and 3) the young sporophyte (Figure 2.29). have their ovules enclosed within a leaf homologue termed a car-
The mature seed is then the unit of dispersal for gymnosperms pel (Figure 2.33A). As a result of this enclosure, pollination in
and angiosperms. In its new environment, the seed imbibes water flowering plants is indirect with microgametophytes or pollen
and germinates. The young sporophytic plant grows out from the grains being deposited on the stigmatic surface of the carpellary
confines of the seed coat and becomes established as an indepen- leaf and germinating there (Figure 2.33A). Following germina-
dent plant. tion, the pollen tube grows through the stigma and style to the
It should be emphasized that while only gymnosperms and ovules in the ovarian cavity (Figure 2.33O). Once the pollen
angiosperms among contemporary plants exhibit the seed habit, tube has penetrated the ovule’s integument via the micropyle, it
analysis of the fossil record has shown that seed production was deposits the two male gametes or sperm cells inside the megaga-
approached in selected, extinct pteridophytic groups millions of metophyte (Figure 2.33P).
The Cast of Characters 33

FIGURE 2.30 Schematic diagram of the reproductive cycle in a gymnospermous seed plant. (From Foster and Gifford, 1974.)

Angiosperms differ from gymnosperms in that both sperm

are active in the fertilization of the seven-celled, female gameto-
phyte. One gamete fuses with the egg cell to form the zygote, and
the other unites with the two haploid polar nuclei in the central
cell of the megagametophyte to give rise to a triploid (3n) pri-
mary endosperm cell (Figure 2.33P,Q). Endosperm is the tissue
that surrounds the embryonic sporophyte and nourishes it during
its development (Figure 2.33Q,R). It differs from the haploid
megagametophyte nutritive tissue in the ovules of gymnosperms
because it arises as a result of fertilization. In flowering plants
both the embryo and the tissues that nourish it originate simul-
taneously as a result of “double fertilization” (Figure 2.33O,P)
whereas in gymnosperms ovular nutritive tissues build up before
fertilization (Figure 2.32E,F). The endosperm of flowering
plants develops much more rapidly than the embryo it will nour-
ish (Figure 2.33Q). It has been speculated that the rapid rate of
endosperm development is a result of its hybrid origin through
fertilization (Brink and Cooper, 1947). FIGURE 2.31 Diagrams of transections of subtending megasporophylls
The rapid evolution of flowering plants at the end of the in various Carboniferous clubmosses showing the stages of their enclosure
Mesozoic Era may have resulted in part from the competitive around the ovule and function as an integument for the fertilized megaspo-
advantage of the more rapid reproductive life histories afforded rangium. A. Megasporangium on the adaxial surface of the megasporophyll
of Lepidocarpopsis lanceaolatus. B. L. semialata with megasporophyll par-
by the evolution of endosperm. Instead of having to build up
tially investing the sporangium. C. Lepidocarpon lomaxi with megasporo-
gametophytic tissues prior to fertilization, the ability to form phyll completely investing sporangium as an “integument.” D. Longisection
nutritive tissue quickly after fertilization would result in the of a gymnosperm ovule for comparison. i, integument, m, micropyle; mg,
more rapid rates of ovule and seed development that characterize megagametophyte. (From Stewart, 1983.)
34 Kaplan’s Principles of Plant Morphology

FIGURE 2.32 Life history of the cycad Zamia (Class Cycadopsida) a. Pollen plant. b. Microsporophyll. c. Young microsporangium with microspore
mother cells. d. Microsporangium containing microspore tetrads. d1. Microspores. d2. Three-celled pollen (immature megagametophytes). A. Seed cone.
B. Megasporophyll. C. Ovule with megaspore mother cell. D. Tetrad of megaspores, one of which is functional. E. Pollination, showing pollen in pollen
chamber and young megagametophyte. F. Developing pollen tube (microgametophyte). G. Mature megagametophyte. H. Mature microgametophyte. I.
Fertilization. J. Mature seed with embryo. (From Norstog and Long, 1976.)

angiosperms as contrasted with gymnosperms. Thus the ability several evolutionary lineages that all bear exposed ovules on
to complete their life cycles more rapidly would have permitted their shoots. Like the pteridophytes, present-day gymnosperms
angiosperms to more effectively colonize and dominate a given are represented by only a few relictual members of groups that
habitat than their gymnosperm contemporaries. were much more extensively represented in the past history of
the earth. The term “gymnosperm” comes from a Greek com-
posite work gymnos or naked and sperma or seed, meaning
naked seeds, referring to the state in which the ovules (unfertil-
The Gymnosperms
ized seeds) are not surrounded by maternal tissue. This is in con-
While at one time they were considered to be a natural, evolu- trast to the angiosperms in which the ovules are enclosed within
tionarily related systematic group, contemporary knowledge sup- an ovary. Gymnosperm leaves are often found on the surface of
ports the concept that the extant (living) gymnosperms include scales or leaves termed megasporophylls, and these are often
The Cast of Characters 35

FIGURE 2.33 Life history of a flowering plant (Class Angiospermopsida). A. Flowering plant model. B–G. Development of the ovule and embryo sac.
H–N. Development of the microgametophyte or pollen grain. O. Fertilization. P–R. development or the seed, including endosperm and embryo. S. Seedling.
G, gametophyte; Sp, sporophyte. (After Strasburger and Sharp.)

modified to form strobili (= cones). Contemporary gymnosperms are borne on specialized sporophylls (reproductive leaf homo-
are recognized as four divisions of the Embryophyta. logues) typically aggregated in large, conspicuous cones or stro-
bili (Figure 2.34). Cycads are dioecious with megasporangiate
and microsporangiate strobili borne on separate plants. They
are distinctive among gymnosperms in having multiflagellated,
Division Cycadophyta
swimming sperm, and the pollen tube is not involved directly in
The three extant families of cycads belong to the order Cycadales, the transport of the male gametes to the egg.
a relictual group consisting of 10 genera widely separated geo-
graphically. The plants have a distinctive shoot morphology rem-
Division Ginkgophyta
iniscent of palm trees in the angiosperms. Like palms, they have
stout, typically unbranched rosette shoots which exhibit little This gymnospermous group is represented today by only a sin-
internodal extension and bear large, pinnately dissected leaves gle species, the maidenhair tree Ginkgo biloba native to China.
morphologically similar to the fronds of palms (Figure 2.34). Ginkgo is a large plant and for centuries has been cultivated
In contrast to palms, however, their ovules and microsporangia as a park tree in the temperate regions of the world. Ginkgo is
36 Kaplan’s Principles of Plant Morphology

Division Gnetophyta
The living gnetophytes are an isolated and small but singular class
of gymnosperms. It consists of three genera that are as distinctly dif-
ferent from one another as they are from the remainder of the gym-
nosperms. They include the genus Ephedra, native to arid regions
of the western United States, central South America, Europe, and
Asia; the genus Gnetum from the lowland tropics of South America,
Africa, and southeast Asia; and the genus Welwitschia, known only
from a restricted desert region in southwest Africa.
The three extant genera of gnetophytes are very different in
habit. The 35 species of Ephedra are profusely branched shrubs
with elongated, photosynthetic shoots with reduced scale leaves
reminiscent of those of Equisetum (Figure 2.39). Most of the
30 described species of Gnetum are vines (Gnetum gnemon can
become a small tree) that climb high into the canopy of the rain
forest. Gnetum differs from Ephedra in having enlarged, lami-
nate foliage leaves (Figure 2.40). Welwitschia is the most bizarre
FIGURE 2.34 Cycad Macrozamia moorei. species in the entire plant kingdom and initially defies conven-
tional characterization. At maturity it consists of a short, squat
deciduous; that is, it loses its leaves at the end of each season stem, flush with the ground, bearing a single pair of twisted and
of growth. Like the cycads, it is dioecious with separate male tattered, strap-shaped leaves that function as the photosynthetic
or microsporangiate and female or megasporangiate trees. organs for the entire life of the plant (Figure 2.41). Some larger
Characteristically, a pair of ovules is borne at the tip of each specimens of Welwitschia have been estimated to be over 1000
ovuliferous shoot initiated from its distinctive short shoots years old (Martens, 1971).
(Figure 2.37B). The microsporangia of male Ginkgo trees are All three genera are dioecious, and their megasporangiate
borne on microsporophylls aggregated into loose strobili on the and microsporangiate strobili are compound and reminiscent of
short shoots (Figure 2.37A). floral shoots of angiosperms (Figures 2.39–2.41). Their ovules
Like the cycads, Ginkgo is essentially a living fossil, the also seem angiospermic in the possession of a fleshy second
last representative of a group that was much more extensively integument. Some investigators see the homology of this second
developed during the late Paleozoic and Mesozoic. Besides integument with the carpels of angiosperm flowers (Martens,
the cycads, it is the only other contemporary gymnosperm to 1971). In fact, the Gnetophyta have been of considerable interest
have flagellated, swimming sperm, a feature considered to be phylogenetically because they have characteristics intermediate
retained from the ancestral use of water as a medium for gamete between gymnosperms and angiosperms, and some evolution-
movement. ary schemes have postulated them to share a common ancestor
with the Angiosperms to the exclusion of the remaining gym-
nosperms. Such views are not in vogue today, however, and
the characteristics that unite Angiosperms and gnetophytes are
Division Coniferophyta (or Pinophyta) thought to be examples of convergent evolution.
With 51 genera and 548 species, this is the largest and most wide- Regardless of their phylogenetic status, it is clear that gento-
spread group of gymnosperms and the one that is most famil- phytes are another remnant group that was widespread in earlier
iar to us. Coniferous trees form a significant component of the geological times and whose pattern of extinction has left only
world’s temperate forests and species of pine, redwood, spruce, isolated, distantly related representatives. While macrofossils of
fir, juniper, cypress, larch, and cedar are familiar members of Gnetophyta are only available in the Tertiary, there is an abun-
this group. Conifers are also important economically as a major dance of gnetalean pollen from in the late Triassic and Cretaceous
source of timber. periods of the Mesozoic (Scott, 1960; Srivastava, 1967), suggest-
Conifers are elaborately branched, usually evergreen trees that ing a wider representation of this group than we have today.
bear reduced, scale- or needle-like foliage leaves. Most species
are monoecious, i.e., they bear megasporangiate and microspo-
Division Magnoliophyta (Angiosperms)
rangiate cones on the same plant, but the male and female cones
are initiated and function at different times during the develop- The largest and dominant division of vascular plants are the
ment of a shoot. The microsporangiate or pollen-bearing cones angiosperms, or flowering plants. Present estimates place it
tend to be smaller and less conspicuous than the megasporangi- between 200,000 and 250,000 species and there may be many
ate cones (Figure 2.38B,C) and typically abscise from the tree species that are still unknown to science. Angiosperms dif-
after their pollen has been shed. Ovulate cones are larger and fer from gymnosperms in the enclosure of their ovules within
more complicated, and usually develop on the tree for a longer the “carpel,” proposed to be a leaf homolog, and the develop-
time (Figure 2.38E). The number of ovules borne per ovulifer- ment of triploid endosperm as the primary nutritive tissue in
ous scale varies according to family. the seed (Figure 2.33O–Q). Characteristically mega- and
The Cast of Characters 37

B.

A. C.

FIGURE 2.35 Morphological features of fossil seed ferns (Class Cycadopsida; Order Pteridospermales). A. Reconstruction of the habit of seed fern
Medullosa noel. B. Seed fern foliage—pinna with terminal seed of Neuropteris heterophylla. C. Seeds attached to the pinnules of leaf of Emplecopteris
triangularis. (From Foster and Gifford, 1974.)

A. B.

or

ms

C.

FIGURE 2.36 Representative fossil Cycadeoidales (Class Cycadopsida). A. Cycadeoidia sp. from Cretaceous. B. Reconstruction of Williamsonia sewardi-
ana. C. Diagrammatic view of reproductive shoot of a cycadeoid—Williamsoniella coronata showing: or, ovulate receptacle; ms, microsporophyll; b, bract.
(A and C from Stewart, 1983; B from Andrews, 1961.)
38 Kaplan’s Principles of Plant Morphology

FIGURE 2.37 Reproductive shoots of the maidenhair tree. Ginkgo biloba (Class Ginkgopsida). A. Male tree. Microsporangiate strobili, bearing microspo-
rophylls, are borne in the axils of bud scales on short shoot lateral branches. B. Female tree. Biovulate lateral branches are borne in the axils of bud scales
on short shoot lateral branches.

A. B.

D. F.

G.

FIGURE 2.38 Life history of the pine (Pinus) (Class Coniferopsida). A. C. E.

Mature sporophyte. B. Pollen cones. C. Microsporophyll and microspo-
rangium. D. Pollen at time of shedding. E. Seed cone with cone scales. F. FIGURE 2.39 Morphology of Ephedra antisyphilitica (Class Gnetopsida).
Longitudinal section of cone scale with developing ovule at the time of fer- A. Male shoot branches bearing male flowers. B. Female shoot branches. C.
tilization. G. Mature female gametophyte (megagametophyte). H. Mature Sterile branch showing scale leaves in pairs at each node. D. Male strobilus
male gametophyte (microgametophyte). I. Section of seed with developing with microsporophylls exerted. E. Female strobilus with a pair of ovules in
embryo. J. Section of mature seed. K. Germinating seedling. (From Norstog the axils of the uppermost bract pair. F. Section through an ovule. G. Bracts
and Long, 1976.) from the megasporangiate strobilus. (From Lotsy, 1911.)
The Cast of Characters 39

principle defining features of the two groups, other less subtle

characteristics help to distinguish members of these two groups
of angiosperms. These include:1) numerical plan in their floral
whorls—three in monocots, four or five in dicots; 2) leaf vena-
tion—longitudinally striate in the monocots and reticulate in the
dicots; 3) stem vasculature—appearing scattered and complex
in moncots, and cylindrical in dicots; and 4) the general pres-
ence (dicots) versus absence (monocots) of a vascular cambium.
While the monocots (e.g., grasses, bananas, lilies, tulips) do form
a single evolutionary lineage, all remaining flowering plants are
A. B. dicots, indicating that the ancestral plant was dicotyledonous.
Recent molecular phylogenetic data have resolved the evolution
of the angiosperms, enabling us to better understand the evolu-
tion of vegetative and floral morphology throughout the flower-
ing plant lineage (citation)
The evolutionary origins of angiosperms continue to be debated
but there is general consensus that they probably evolved from an
unknown group of gymnosperms during the late Triassic. During
the subsequent 220+ million years they underwent an explosive
radiation to become the dominant vegetation on the earth today.
Flowering plants exhibit every life form known in the plant king-
dom, extending from trees to vines to geophytic plants as well
C. D. as succulents, aquatics, epiphytes, and parasites. Because they
exhibit this tremendous range of form and occupy such a diver-
sity of habitats, most of this book will address flowering plant
diversity and adaptation.

F. Morphological Convergences between Plant

E. Groups that are Unrelated Evolutionarily

G.
To this point, this chapter has been devoted to a broad review of
the systematic, evolutionary relationships of the plant kingdom
FIGURE 2.40 Morphology of Gnetum latifolium (Class Gnetopsida) A. as a basis for the comparative morphological analysis that fol-
Male plant with terminal microsporangiate inflorescence. B. Enlargement lows. Now that we have identified the major “pigeonholes” that
of terminal male inflorescence. C. Part of a male inflorescence showing con- the variety of plants belong in, it is interesting and informative
nate nature of bracts and individual male flowers in their axils. D. Branch to look at morphological phenomena that transcend taxonomic
with laterally inserted female inflorescences. E. Detail of a portion of a boundaries. For example, consider the convergence in shape or
female inflorescence. F. Detail of an individual male flower. Longisection
morphology between plants that are completely unrelated sys-
through a male flower. (From Lotsy, 1911.)
tematically. In the next chapter we will exploit these convergen-
ces to learn about the structural organization of higher plants.
microsporangia are borne on foliar appendages on the same It was the great German plant morphologist, Karl von Goebel
specialized branch or shoot segment (Figure 2.33A). This spe- and Bergdolt (1928), who drew attention to the widespread
cialized reproductive short shoot is called the flower, and thus convergence in external shape across higher and lower plants.
the angiosperms are known as the flowering plants. The great The particular morphological expression he noted was the fron-
variations in floral structure exhibited by angiosperms represent dose habit he termed “araucarioid” (because of its fundamental
adaptations to a variety of pollination mechanisms including ani- expression in the lateral branches of the coniferous gymnosperm
mal vectors to transfer pollen grains from the microsporangia of genus Araucaria). Araucaria excelsa, for example, produces
one flower to the stigmatic surfaces of another. We will explore lateral branches that have a distinctive feather-like morphology
the fundamentals of floral morphology and the basis for their (Figure 2.42A). Each lateral branch has a broadened, planated
structural variation in Chapter 17. appearance because its lateral branches grow in a single, hori-
Two major groups of angiosperms have been recognized and zontal plane even though leaves are initiated around the entire
used to characterize major morphological differences. circumference of the stem. Like those of most other seed plants,
The monocots share the presence of a single cotyledon or the lateral branches Araucaria form in the axils of leaves.
seed leaf, initiated as the first leaf of the shoot during embryo However, whether there are buds in the axils of all leaves or not
development. All other angiosperms are referred to as “dicots,” (Burrows, 1987), only those in two rows at the lateral flanks of the
as a pair of cotyledons arise simultaneously during embryogen- shoot grow out to form conspicuous branches. If such a branch
esis (Figure 2.33Q,R). While cotyledon number is one of the is removed and planted in a pot, it will retain its horizontal (or
40 Kaplan’s Principles of Plant Morphology

FIGURE 2.41 Morphology of Welwitschia mirabilis (Class Gnetopsida) as seen growing in the Namib Desert in southwest Africa. A. A young (10- to
20-year-old) plant. B. Maturing 100- to 200-year-old female plant. (From Weier et al., 1982.)

plagiotropic) growth habit (Goebel, 1928). Such experimenta- frondose in form reminiscent of a fern leaf and, like Araucaria,
tion indicates that the growth pattern of this planated branch sys- has leaves inserted around the circumference of the stem. In con-
tem in Araucaria is not a consequence of where the branch arises trast to Araucaria, its “araucarioid” habit is a result of second-
in relation to the shoot but is an intrinsically determined feature ary torsion of the long shoot lateral branches into a single plane
that cannot be altered by changing the environment or removing instead of selected leaves exhibiting branches. Asparagus also
the branch from the parent plant. differs because its leaves are non-green, scale-like organs and
This araucarioid habit is found in a wide variety of unrelated its determinate, flattened branches, called phylloclades are its
plant species across the entire plant kingdom. Among flower- photosynthetic organs (leaf-like stems; see Chapter 11). Thus
ing plants, for example, this type of shoot morphology is seen this convergence in araucarioid habit in different plant groups
in the monocotyledonous asparagus fern, Asparagus plumosus represents differences in emphasis and degree of expression of
(Figure 2.42B). Like Araucaria, the shoot of Asparagus is different shoot components.
The Cast of Characters 41

A. B.

C.

D.

FIGURE 2.42 The occurrence of the “araucarioid” habit across plant taxonomic lines. A. Araucaria excelsa, a gymnosperm (conifer). B. Asparagus
plumosus, an angiosperm (Magnoliophyta) in the monocotyledonidae. C. Hylocomium splendens, a bryophyte. D. Selaginella umbrosa, a Lycophyte
(Lycopsida).

Even selected Bryophyta can exhibit this araucarioid shoot Once we are aware of the existence of this distinctive expres-
habit. The moss Hylocomium splendens has an aerial shoot sys- sion of shoot morphology, we can find it in other members of
tem reminiscent of that of the asparagus fern (Figure 2.42C). the plant kingdom. For example, shoots in the clubmoss genus
While obviously smaller, each successive shoot segment exhibits Selaginella develop this frond-like morphology (Figure 2.42D).
a horizontal or plagiotropic growth habit with branching only It also can be found in of the coniferous cypress family
occurring in a single plane (Figure 2.42C). What makes this (Cupressaceae), for example in both the cypress Cupressus and
convergence all the more remarkable is that it is exhibited by arbor vita Thuja (Figure 2.43A). In the ferns (Class Filicopsida)
the haploid, gametophytic phase of the moss and not the diploid it is the individual leaf component which is elaborated and
sporophyte phase of the seed plants Asparagus and Araucaria. highly branched and converges in form with whole shoots
Thus such convergences in shoot morphology transcend not only of other plant species. Even the algae can exhibit this type of
taxonomic and phylogenetic boundaries but also the phases of frondose habit. For example, certain Floridiophycean reds
plant life history as well. (Division Rhodophyta), such as members of the genera Ptilota
42 Kaplan’s Principles of Plant Morphology

A. B. C. D.

FIGURE 2.43 “Araucarioid” habit in different plant taxonomic groups. A. Thuja plicata, a gymnosperma (conifer). B. Ptilota hypnoides (Rhodophyta, red
algae). C. Microcladia boreale (Rhodophyta, red algae). D. Bryopsis plumosus (Chlorophyta).

and Microcladia (Figure 2.43B,C), develop strikingly beautiful the relationship between cell geometry and tissue arrangements
fronds that resemble the shoots of Asparagus. The same can be and the shape of organisms. Even though these species may
seen in the green algae (Chlorophyta). The marine alga Bryopsis converge in external shape, their cell alignments can be quite
plumosus, for example, has a pinnate, feather-like morphology in different. These observations have important implications for
which there is a central axis bearing lateral branches with each understanding the basis of the determination of form in plants
of the laterals bearing its own set of laterals (Figure 2.43D). The and the role of multicellularity in that determination. We will
whole branching system produces a frond-like habit which, looks also use morphological convergences in the algae as a basis for
like the araucarioid plants we have described. gaining a more profound understanding of the organography of
In the next chapter we will study the fundamental cellular higher plants.
arrangement of some of these organisms in order and evaluate
3
The Relationship between Morphology and Anatomy in Plants

CONTENTS
Basic Modes of Multicellular Construction in Plants.............................................................................................................................43
Colonial or Coenobial Forms.............................................................................................................................................................43
Filamentous Forms.............................................................................................................................................................................48
Parenchymatous Forms...................................................................................................................................................................... 51
True Parenchyma.......................................................................................................................................................................... 51
Pseudoparenchyma.......................................................................................................................................................................53
Acellular or Tubular Forms of Construction: Coenocytes.................................................................................................................59
The Organ Level of Organization...........................................................................................................................................................62
Question of the Relationship of Cell Arrangements to the Generation of Shape in Multicellular Higher Plants..................................63
The Biological Significance of Multicellularity in Plants.......................................................................................................................68
Conclusions.............................................................................................................................................................................................70
Summary: Updates and Observations................................................................................................................................................70

At the end of Chapter 2 we presented examples of plants which algae (Chlorophyta). In this phylum one can find everything
were unrelated systematically or evolutionarily, but which exhibit from spherical colonial forms, branched and unbranched fila-
a similarity of overall body shape. If you analyze the structure ments to parenchymatous and even tubular, unicellular bodies
of these respective organisms in greater detail, especially micro- (Figure 3.1). Interestingly, this remarkable diversity of construc-
scopically, you see that, despite a similarity in overall morphology, tion modes all seems to start with a single, flagellated cell type
some have significantly different arrangements of their cells and and proceeds along three principal lines of body plan develop-
tissues. Traditionally, the cell has been considered the “building ment: 1) the colonial line (Figure 3.1A,B), 2) the filamentous-
block of the organism” and an organism’s morphology simply the parenchymatous line (Figure 3.1A–C), and 3) the siphonous or
byproduct of how its cells are arranged. The occurrence of organ- tubular line (Figure 3.1A–D). Even though these lines are no
isms with similar shapes but differing internal structure raises longer viewed as the simple phylogenetic pathways that they once
the fundamental question of the relationship of the anatomical to were (Bold and Wynne, 1985), they are useful in our present con-
morphological levels of organization in plants. Or, phrased in a sideration of the alternative modes of plant construction.
different way, are cells really the building blocks of plant form?
Since most texts on plant structure emphasize the anatomical
or cell to tissue level of organization, they begin with the assump- Colonial or Coenobial Forms
tion that cell arrangement is the cause of the form. However, in The biflagellate unicell Chlamydomonas is a typical eukaryote
a book that is morphologically oriented and proceeds from a possessing a well-defined nucleus, mitochondria, and endomem-
whole-plant perspective down to the anatomical level, assump- brane system surrounded by a large, cup-shaped chloroplast that
tions about the relationship between these two levels are not dominates the volume of the cell which imparts its predominant
made, and one can examine their connection in an unbiased green coloring (Figure 3.2A–C). Each cell contains a concentra-
manner. In this chapter we describe the varying types of tissue tion of carotenoid pigments in the chloroplast called the eyespot
construction and geometries and consider their functional signif- or stigma (Figure 3.2C). The stigma is considered to be a photo-
icance using the algal and fungal groups we characterized in the sensitive region and has been implicated in the phototactic (move-
preceding chapter as examples. We then try to answer the basic ment toward light) responses exhibited by Chlamydomonas cells.
question we have raised about the relationship between these If, instead of dividing to form several free Chlamydomonas
different levels of plant organization. Analysis of these simpler cells in the process of asexual reproduction (Figure 2.6A–D),
species will permit us to gain a more profound understanding of its daughter cells remain attached in various geometric con-
the basic structural and developmental features of higher plants. figurations, then we have the development of colonial multicel-
lular organisms (Figure 3.1A,B). As will be evident from the
analysis of members of this series, such multicellular species
Basic Modes of Multicellular are, in fact, not merely the simple aggregations of individual
Chlamydomonas cells that the term colony implies but are actu-
Construction in Plants
ally highly differentiated individuals exhibiting an organismal
A group that exhibits a remarkable diversity of modes of tissue unity with a high degree of differentiation. The term coenobium,
construction which is instructive for our purposes is the green which is defined as a colony with a fixed number of cells that is

43
44 Kaplan’s Principles of Plant Morphology

FIGURE 3.1 General scheme of evolution of body plans in Chlorophyta, showing the three major lines, beginning with a Chlamydomonas unicell and
leading to the: (1) motile spherical line; (2) filamentous-parenchymatous line; and (3) siphonous-tubular line. (From Norstog and Long, 1976.)

specified at its origin and not augmented subsequently (Bold and having large stigmas and those at the posterior or trailing end
Wynne, 1985), more accurately expresses the truly organismal either lacking or having inconspicuous eyespots (Figure 3.4).
nature of these multicellular forms. Such an anterior-posterior gradient is even more manifest in
If we begin with the smallest and simplest example of these coenobia of the genus Pleodorina. In P. illinoiensis, for example,
coenobia, in the genus Gonium, we see an organism consisting of the 32 cells comprising the colony, not only do the four cells
of from 4 to 32 Chlamydomonas-like cells in a curved, plate- at the anterior end have larger stigmas than those at the rear, but
like disc united in a common mucilaginous matrix (Figure 3.3). the anterior cells also are significantly smaller than the remain-
All cells of a Gonium coenobium are capable of forming deriva- ing 28 (Figure 3.5). Only the larger cells at the posterior end
tive colonies (called autocolonies) through vegetative reproduc- of the coenobium in P. illinoiensis are capable of giving rise to
tion, and gametes for sexual reproduction. Furthermore, there autocolonies. When there is such a specialization of function
is no polarity to the colony, hence no definable anterior and in coenobia, the larger, reproductive cells are called Gonidia.
posterior ends. Gonidia in P. illinoiensis differ not only in size and position but
By contrast, the genus Pandorina exhibits a distinct polarity also in function.
to its ellipsoidal coenobium. Like Gonium, species of Pandorina Such a structural and functional dimorphism is expressed even
can range from 16 to 32 biflagellate cells and all cells of a colony more markedly in another species of Pleodorina, P. californica,
are able to form autocolonies and/or gametes. (Figure 3.4). The a larger coenobium consisting of a greater number of cells (128).
polarity of the coenobium is expressed by a gradient in eyespot The cells at the anterior end of the colony, which are smaller
size with those cells at the anterior or forward swimming portion with conspicuous eyespots, serve a vegetative function while the
The Relationship between Morphology and Anatomy in Plants 45

FIGURE 3.3 Motile colony of Gonium in which the 16 Chlamydomonas-

like cells are arranged in the form of a flattened plate, bounded by a common
wall matrix (mx). Equivalent-sized eyespots are evident in all of the cells
A. and there is no sign of an anterior-posterior polarity. (From Scagel et al.,
1965.)

f
ey

c.v.

s. py
n.
a mx p

pl.

cy. py.

B.

FIGURE 3.2 Structure of the biflagellate unicell of Chlamydomonas

eugametos. A. Diagram of cell ultrastructure, showing various organelles,
including cup-shaped chloroplast, prominent nucleus, mitochondria, and
endomembrane system. B. Median optical section showing nucleus (n), plas- FIGURE 3.4 Motile colony of Pandorina which exhibits an anterior-pos-
tid (p), and cytoplasm (c). Surface view showing flagellae (f), contractile terior gradient largely in the gradient in eyespot size. Cells at the anterior
vacuoles for water regulation (cv), pyrenoid or starch-forming center in the end (a) have larger eyespots than those at the posterior (p). ey, eyespot or
chloroplast (p), and the eyespot or stigma (s) region differentiated in the plas- stigma; mx, wall matrix; py, pyrenoid. (From Scagel et al., 1965.)
tid. (A from Clark, 1972; B, C from Bold et al., 1980).

large gonidial cells at the posterior end, with less conspicuous inserted at the periphery of a giant sphere that is so large that it
eyespots, are specialized for reproduction (Figure 3.6). can be seen with the unaided eye (Figure 3.7A). Not only are the
The culmination of this tendency toward cell specialization purely vegetative or somatic cells at the anterior end significantly
and anterior posterior gradient is exemplified by the enormous smaller than the gonidia at the rear, they also are significantly
(relatively speaking) coenobia in the genus Volvox. Different spe- greater in number (Figure 3.7B). The reproductive cells exhibit
cies of Volvox consist of 1,000 to 50,000 chlamydomonad cells not only the aforementioned eyespot reduction, they also lack
46 Kaplan’s Principles of Plant Morphology

p a p a

A. B.

FIGURE 3.5 Pleodorina illinoiensis showing marked anterior-posterior differentiation with smaller vegetative cells (v) at the anterior end and larger
gonidial or reproductive cells (g) at the posterior end. (A, drawing from Fritsch, 1935; B, photograph from Bold and Wynne, 1985.)

flagellae. Hence they are even more specialized for reproduction The general deductions we can draw from this elementary anal-
than the gonidia in Pleodorina. ysis of the volvocine or colonial line of green algae are: 1) despite
In the mature colonies of certain species of Volvox (e.g., in V. an overall similarity in organismal shape, there can be differing
globator and to a lesser extent in V. aureus [Figure 3.7]), the degrees of internal or histological specialization, suggesting the
constituent cells exhibit cytoplasmic strands or plasmodesmata independence of morphological and anatomical levels of organi-
(sing. plasmodesma) (from the Greek plasmos meaning that zation; and 2) differing degrees of functional specialization are
formed and desmos meaning a bond), connecting the proto- related more to cell differentiation than to the morphology of the
plasts of adjacent cells (Figure 3.7C–F). Even if such plasmo- organism. Even though these themes are expressed in very sim-
desmata are not evident in the mature spheroid (Figure 3.7G–I), ple ways in this group, they are concepts we will see repeated in
they are present during the early development of the colony and group after group and therefore are of fundamental significance.
became either excessively stretched or broken as additional cell Other Volvocales give further evidence of the independence
wall material is added. The existence of plasmodesmata in such of external form from internal differentiation, but in alternative
colonial organisms indicates the bases for their integrated swim- ways. For example, the coenobium in the genus Platydorina
ming and physiological behavior. It also underscores the fun- exhibits a more complex external shape than the other mem-
damental continuity of their protoplasts, despite their apparent bers of this order but without the accompanying cell differentia-
multicellularity. tion and specialization in function. The anterior-posterior axis

C.

B.

A.

D.

FIGURE 3.6 Pleodorina californica. A, B. Photographs of whole coenobia, showing half of the constituent cells being small vegetative cells at the anterior
end (a) and half being large gonidial cells at the posterior end (p). C. Detail of median optical section through a small vegetative cell, showing its enlarged
eyespot. D. Median optical view of large gonidial cell from posterior half with reduced, almost inconspicuous eyespot. (From Bold and Wynne, 1985;
photographs courtesy of Professor Richard C. Starr.)
The Relationship between Morphology and Anatomy in Plants 47

FIGURE 3.7 Structure of the motile colony of Volvox. A. Surface view of coenobium of Volvox globator. B. Coenobium of V. mononae, exhibiting enlarged
daughter colonies at posterior end of sphere. C, D. Surface views of protoplast of V. globator showing thick plasmodesmata or cytoplasmic connections
(c, chloroplast; m, wall matrix; v, vacuole). E. Section through periphery of coenobium of V. globator. F. Surface view of cells of V. aureus showing finer
plasmodesmata. G, H. Surface and sectional views of coenobium of V. tertius where plasmodesmata are no longer evident but occurred in the early stages
of colony development. Median section through the colony of V. aureus showing wall matrix material extended deeply into the center of the coenobium.
(From Fritsch, 1935.)

of Platydorina caudata is expressed by the development of a

mammillate processes from the posterior end rather than dif-
ferences in cell structure between its two ends (Figure 3.8A).
Transectionally, Platydorina is a flattened plate, like Gonium,
but with an additional twist (Figure 3.8B). In terms of cell spe- w a
cialization and function, Platydorina is at the same level as m
Gonium but with a greater elaboration of morphology.
Finally, we can ask if this spherical-colonial theme expressed
in these free-swimming, freshwater algae is significant in the
evolution of the ground plan for land plants of the type discussed
in Chapter 1 (Figure. 1.7). The answer is probably no. From an
evolutionary perspective such a spheroidal morphology is prob- p
p
ably a dead end, adapted exclusively to the aqueous medium in
A. B.
which these organisms live. Its evolutionary restriction undoubt-
edly stems from functional and mechanical limitations for pho- FIGURE 3.8 Platydorina caudata showing anterior-posterior differen-
tosynthetic organisms that result from this type of spherical tiation due to development of mammillate projections at posterior end. A.
morphology. Surface view. B. Side view. (From Fritsch, 1935.)
48 Kaplan’s Principles of Plant Morphology

Given that photosynthesis is a process that depends upon the production is distinctly apical and a marked basipetal gradi-
exposure of large green surfaces to intercept maximum amounts ent in cell maturation along the length of each filament axis is
of light and effect the exchange of gasses, a spheroidal form is readily apparent (Figure 3.10A).
only effective in organisms of limited size. Surface area increases Branching of a filament increases the surface area for respira-
as the square of a linear dimension, whereas volume increases tion and photosynthesis. Branch initiation usually occurs when
as a cube of that dimension. With the proportional growth that a cell at or near the tip of the parent filament divides either
results in a sphere, volume will increase at a more rapid rate than obliquely or at right angles to the long axis of the parent filament
surface. If cells divide in all directions as this ball increases in rather than transversely, giving rise to this new axis of exten-
size, ultimately there will a marked difference in the environ- sion (Figure 3.9D,E). As the branch grows, it will produce its
ment between the cells at the interior and those at its surface. own derivative lineage of cells (Figure 3.9F,G). Microthamnion
Photosynthetic cells at the periphery will wind up feeding an exhibits a branched, filamentous growth form in which the
ever-increasing mass of cells at the sphere’s center. The rate of branches are identical in cell structure and growth to that of the
surface growth will lag progressively behind that of volume so parent filament (Figure 3.11).
that the ratio of surface to internal cells will drop and the organ- Even though a filamentous mode construction seems relatively
ism will no longer be self-supporting nutritionally. This problem simple, it doesn’t necessarily exclude the possibilities of higher
is overcome in Volvox by the restriction of cells to its periphery degrees of differentiation and specialization of function among
(Figure 3.7E,H,I). its component branches. For example, certain filamentous algae
In addition, in motile organisms such as Volvox, colony move- exhibit the phenomenon of heterotrichy (from the Greek hetero
ment is dependent strictly on the cells at its surface. As the colony meaning other and trichous [trichome] meaning growth of hair
grows more rapidly in volume, its mass increases disproportion- or a hair). A heterotrichous system is composed of both erect
ately. A reduced surface-to-volume ratio would mean that the rel- (orthotropic) and prostrate (plagiotropic) growing filament sys-
atively few swimming surface cells would be available to propel tems. The constituent filaments of such heterotrichous systems
this continually increasing mass through the aqueous medium to can differ in their growth direction and exhibit differences in the
achieve optimal light interception and gaseous exchange. nature of their cells and organelles. Thus heterotrichy may have
As we will see when we look at other modes of construc- both positional and qualitative expressions.
tion in the algae, these problems of surface-to-volume ratio and A clear example of the heterotrichous habit is the green
their biological consequences for autotrophs are reduced by an genus Stigeoclonium. Its heterotrichy is expressed by its sys-
emphasis on surface growth in filamentous forms. Since higher tem of plagiotropic filaments that extend horizontally across the
plants essentially exhibit a spindle type of axial construction that substratum, giving off orthotropic or upwardly directed pho-
is a derivative of filamentous growth (Figure 1.7), it is obvious tosynthetic filament branches and downwardly directed, color-
that the spheroidal morphology of the volvocine line has been of less rhizoid branches which serve to anchor it to its substratum
limited significance in land plant evolution. (Figure 3.12A). The upwardly directed trichomes have elongate
cells with conspicuous parietal chloroplasts (Figure 3.12B) and
typically terminate in a pointed cell or an elongate, clear hya-
Filamentous Forms
line cell (Figure 3.12A). Cells of the prostrate system have
Filamentous growth represents the emphasis on growth in sur- similar plastids but are shorter than the cells of the upright fila-
face rather than volume. While a filamentous morphology is ments (Figure 3.12A). Rhizoid cells differ from those of all
particularly advantageous for photoautotrophs because of the other filaments by their narrower diameter and colorless nature
aforementioned exchange problems, this kind of development (Figure 3.12A).
has structural limitations of its own, as we shall come to see. Despite its simplicity of construction, Stigeoclonium displays
By definition, a filament is a single line or chain of cells interesting analogies to the architecture of higher land plants. The
whose growth is confined to a single plane, extension in prostrate system, for example, behaves like the horizontal, vege-
length (Figure 3.9A–C). Correlated with this longitudi- tative spread of a rhizome or runner system producing erect, pho-
nal extension, the addition of new cells occurs by the inser- tosynthetic shoots as it colonizes the soil surface (Figure 3.12A).
tion of new cell walls perpendicular to the long axis of the The rhizoids would then be analogs of roots functioning not only
filament (Figure 3.9A–C). An example of a green alga with for anchorage but also for the possible uptake of mineral ele-
a simple, unbranched, filamentous type of construction is the ments from the substratum.
genus Ulothrix (Figure 3.10A). Cell shape and chloroplast Within Chlorophyta one can find a number of variants on this
characteristics are similar throughout the filament with the heterotrichous theme with differing degrees of development of
exception of the basal cell that is modified as a holdfast or the prostrate versus erect portions of the thallus. For example, in
attachment cell (Figure 3.10A). New cells are added to the fila- the genus Coleochaete, the prostrate portion is accentuated and
ment by divisions either at the tip—so-called apical growth develops as a flattened disc or crust closely appressed to the sub-
(Figure 3.9A–C)—or at any position along the filament’s stratum (Figure 3.13). The vertical component is expressed only
length—diffuse or intercalary growth (meaning inserted as individual setae or hairs emerging at right angles from the
between; in this case between two cells that are not dividing). crustose plate (Figure 3.13). Members of many algal groups (e.g.,
Filaments exhibiting apical growth will, as a result, show a Rhodophyta, Phaeophyta) exhibit an initial crustose, prostrate
gradient in cell size and maturation along its length. In the case development followed by vertical filaments emerging from their
of Ulothrix, division is intercalary and there is no evidence of a surface. Thus this form of heterotrichy is a widespread construc-
gradient (Figure 3.10A). In the Florideophycean red algae, cell tional theme that is undoubtedly significant for establishment on
The Relationship between Morphology and Anatomy in Plants 49

A1

A1

A. B. C.

A A A A

D. E. F. G.

FIGURE 3.9 Diagrams illustrating filamentous mode of growth unbranched filament in A–C and branched filament in D–G.
50 Kaplan’s Principles of Plant Morphology

A.
FIGURE 3.11 Branched filamentous habit exhibited by green alga
Microthamnion kutzingianum. (From Bold and Wynne, 1985.)

B. B.

FIGURE 3.10 Unbranched filaments of Ulothrix zonata showing the

plant’s habit attached to a rock substratum in A and structure of constituent
cells with one parietal chloroplast per cell in B. (From Bold and Wynne,
1985.)

the surface of a flat substratum in an aquatic medium, whether it

be freshwater or marine.
Finally, conversely, in the genus Microthamnion, it is the pros-
trate component which is poorly developed, seemingly reduced
to the single holdfast cell with a tapering base, whereas the
upright portion is an elaborately branched filamentous system
(Figure 3.11).
At first glance it would seem that a plate-like expansion, such
as that exhibited by Coleochaete, diverges significantly from the
filamentous theme we have emphasized in this section. However,
it is a very simple developmental change to convert a uniseriate
A.
filament into a uniseriate cell plate. It involves merely a change
in the plane of expansion of the filament. Instead of growing in
length, cells of the filament grow at right angles to that plane and
FIGURE 3.12 Heterotrichous, branched filamentous growth form exhib-
parallel to the substratum.
ited by the green alga Stigeoclonium. A. Note the differentiation into pros-
While a filamentous body does expose a large surface area for trate, plagiotropically growing system and orthotropic filaments terminating
gas exchange, uptake of mineral elements and reception of light, it in elongate hairs. B. Detail of chloroplast morphology in a cell from an erect
must depend on the surrounding water for its mechanical support. filament. (From Chadefaud, 1960.)
The Relationship between Morphology and Anatomy in Plants 51

FIGURE 3.13 Uniseriate crustose thallus in the genus Coleochaetae, where heterotrichy is expressed by the prostrate system being developed into a flat-
tened disc and the upright portion expressed only as uniseriate hairs. (From Scagel et al., 1965.)

With its emphasis on growth in volume, a three-dimensional by the brown alga Sphacelaria plumula. The tip of each fila-
tissue mass, such as Volvox, can be self- supporting. Because ment in the thallus of Sphacelaria is dominated by an elon-
higher plants must be both self-supporting and photosynthetic gate, conspicuously vacuolate apical cell (“a” in Figure 3.15A).
in their land habitat, they represent a compromise between the Transverse division of this apical cell produces cells from its
opposing tendencies of surface and volume growth. They exhibit proximal cutting face associated with the increase in filament
the extension in length characteristic of a filament but grow in length (Figure 3.15A). Depending upon the species, some three
volume to satisfy mechanical demands of self-support. They do
this by forming a three-dimensional tissue mass called a paren-
chyma, which, on the one hand, can satisfy the biomechanical
requirements of support while, being elaborated secondarily into
expanded surfaces for functional specialization that we define as
the plant organs.

Parenchymatous Forms
The term parenchyma refers to a three-dimensional tissue mass
where the emphasis is on growth in mass and volume rather than
growth in surface. Any tissue mass greater than one cell in thick-
ness usually is considered to be a parenchyma. Definition of a tis-
sue as parenchymatous does not, however, depend on the shape
of the organ or organism it is part of.
Traditionally, two types of parenchyma have been recognized
on the basis of their developmental origins: 1) true parenchyma
and 2) pseudoparenchyma or false parenchyma. At maturity
these two types of tissue can look so similar in sectional views
that it is virtually impossible to tell them apart; they can be
distinguished definitively only by developmental investigations.
The contrast between these two tissue types can best illustrated
by algae and fungi.

True Parenchyma
True parenchyma arises by the subdivision and growth in vol-
FIGURE 3.14 Diagrammatic comparisons between the modes of origin
ume of cells derived from a single cell lineage or cell file of: A. A true parenchyma by three-dimensional growth from a single cell
(Figure 3.14A). An example of true parenchyma develop- lineage, and B. Pseudoparenchyma formation by a secondary aggregation
ment and its relationship to filamentous growth is illustrated of individual filaments.
52 Kaplan’s Principles of Plant Morphology

2
p
3
i
4
br

A.

1 1

B. C. D. E. 2

FIGURE 3.15 True parenchyma formation in the brown alga Sphacelaria plumula. a. Apical cell and numbers 1–4 mark the successive segments of the
apical cell of the main axis. B–E transverse sections of successive segments of the axis showing their parenchymatous nature. (From Fritsch, 1935.)

or more cells distant from the apical cell, a filament cell will in the mustard family (Cruciferae) shows an initial filamen-
undergo one or more vertical divisions producing a transverse tous growth (Figure 3.17B–G), followed by the formation of
nest of cells within the boundary of the original parent filament a three-dimensional parenchymatous mass at its distal pole
cell wall (Figure 3.15A–E). Even though these cell derivatives (Figure 3.17I–Z). It is this parenchyma that will subsequently
in Sphacelaria do not enlarge, they are true parenchyma because be molded into the major organ systems that comprise the body
they represent potential growth in volume from a single filamen- of the higher plant. In fact, it is only evidence from embryogen-
tous cell lineage. esis that definitively demonstrates that seed plants have a true
Another clear example of true parenchyma formation is exhib- parenchyma because it is the only stage where the formation of
ited by the green alga Fritschiella tuberosa. Figure 3.16 illus- parenchyma from a single cell lineage occurs. Once the apical
trates the stages of development of a young germling. Following meristems have been differentiated, they are already parenchy-
a period of linear, filamentous extension (Figure 3.16A,B) matous and they merely perpetuate the parenchymatous con-
the most distal apical cells form a terminal parenchyma struction initiated in embryogeny.
mass by dividing at right angles to the filament’s long axis A comparison of the terminal growing regions of the bodies
(Figure 3.16C,D). Continued vertical partitioning of the more of the brown alga Sphaceleria and a vascular land plant such
proximal cells of the filament results in the formation of a three- as the horsetail Equisetum indicates how similar their general
dimensional cushion which is a true parenchyma because it was developmental patterns are despite a seemingly great difference
derived from the growth in volume of derivatives a single cell in degree of development of the mature organisms. The distal
lineage. Parenchymatous or filamentous aerial branches grow poles of both Sphacelaria and Equisetum are dominated by
out from that cushion to form the erect photosynthetic filaments large, conspicuous apical cells that are the ultimate source of
(Figure 3.16F). cells for both plant bodies (Figure 3.18A,B). The apical cells of
The bodies of vascular land plants and bryophytes are also these two species differ significantly in shape, reflecting differ-
examples of a true parenchyma. For example, the embryonic spo- ent timings of the onset of parenchyma formation. In the case
rophyte of the flowering plant species Capsella bursa-pastoris of Sphacelaria, we have an elongate apical cell whose principal
The Relationship between Morphology and Anatomy in Plants 53

c
d
a

A. B. C. D. E. F. G. H.

I. J. K. L. M. N. O.

c
d

P. Q. R. S. T. U. V.

d
FIGURE 3.16 True parenchyma formation during the development of the
green alga Fritschiella tuberosa. (From Wardlaw, 1955.)

role is the production of derivative cells which in turn give rise to

parenchyma some distance from the apical cell (Figure 3.18A).
By contrast, in Equisetum, the apical cell has a tetrahedral-
W. X. Y. Z. Z1. Z2.
pyramidal shape with derivatives being produced from each of
its lateral cutting faces (Figure 3.18B). Therefore in Equisetum
the apical cell is involved directly in parenchyma formation FIGURE 3.17 True parenchyma formation during embryo development in
rather than at a distance in its derivatives. Hence the difference the flowering plant Capsella bursa-pastoris. A. Unfertilized egg in megaga-
metophyte in ovule. B. Enlarging zygote. C Unequal transverse first division
between the apical meristems of these two plants is simply a
of zygote. D–G. Filamentous growth. H. Initiation of parenchyma forma-
matter of the relative timing of the onset of parenchymatization. tion in most distal cell of filament. I–P. Elongation of proximal filamentous
This comparison emphasizes the fundamental similarity in plant suspensor and growth in volume of the distal parenchymatous body. Q–Z.
body formation in species with distinct apical growth and serves Development of the parenchymatous body into the major organ regions of
to connect the higher plants with growth patterns exhibited by the plant body. (From Schaffner, 1906.)
many algae.
basidiomycetes) and the vegetative thallus of lichens, where the
fungus forms the majority of the parenchymatous body.
Pseudoparenchyma
You may recall that in Chapter 2, we discussed the overall
In contrast to true parenchyma in which the generation of a morphology of fungi in relation to their absorptive mode of
three-dimensional tissue mass is by growth in volume of tissue nutrition. We noted that as organisms which live inside of their
derived from a single cell lineage, a false parenchyma is one food source, the feeding phase of a fungus consists of an elabo-
derived from the secondary aggregation of many individually rately branched, filamentous system called a mycelium, exposing
growing filaments or cell linages to form a compact tissue vol- a maximum surface area for nutrient digestion and absorption
ume (Figure 3.14B). The structure of such a false parenchyma is (Figure 3.19). On the other hand, during its reproductive phase
analogous to that of an electrical cable. If you make a cross sec- the fungus develops a three-dimensional parenchymatous fruit-
tion through such a cable, you see that it, in turn, is a compound ing body to elevate the spore-bearing portion out of the food
structure composed of many individual electrical wires. In the source and help project the spores into the turbulent layer of the
case of a pseudoparenchyma, the individual filaments can be so air for dispersal (Figure 3.20A). It is here that a false paren-
compressed that in sectional view it is nearly impossible to distin- chyma serves as a significant mechanical support analogous to
guish it from a true parenchyma (Figure 3.14B, 3.20B) except in the stem of a tree holding the photosynthetic foliage in space.
regions where the strands are separated from one another slightly Studies of fungal fruiting body development have demon-
(Figure 3.20B,C). The best examples of pseudoparenchyma are strated its pseudoparenchymatous nature. At the time of initia-
found in the fruiting bodies of the higher fungi (ascomycetes and tion, the previously freely growing and ramifying hyphal strands
54 Kaplan’s Principles of Plant Morphology

ce

A B

FIGURE 3.18 Comparisons of the apical meristems and relative rates of true parenchyma formation in A, the brown alga Sphacelaria plumigera and B,
the vascular plant Equisetum. Note the prolonged filamentous development followed by parenchyma formation in Sphacelaria and the immediate process of
parenchyma formation at the apical meristem of Equisetum. (A from Troll, 1959; B from Smith, 1938.)

are stimulated to aggregate and grow in a coordinated fashion,

producing a unified fruiting body (Figures 3.20A–C, 3.21A–C).
The initial hyphal aggregation produces a small, knob-like pri-
s mordium (Figures 3.21A,B, 3.22A,B) which then expands and
undergoes a complex morphogenesis to produce the mushroom
that pushes above the soil level (Figures 3.21C–G, 3.22C,D).
A.
The biological coordination of fungal hyphae to produce such a
complex three-dimensional unit must stand as one of the won-
ders of developmental biology and suggests a developmental
unity which transcends the individual parts. Given this unique
change in growth pattern from a series of independently growing
filamentous tubes to a compact tissue mass of significant vol-
ume, pseudoparenchyma formation would seem to be the only
way that such a transition between these two disparate growth
modes could be effected.
s Members of subclass Floridiophycideae also exhibit a remark-
able range of morphology, extending from those species com-
posed of elaborately branched, freely filamentous systems, such
as Callithamnion and Antithamnion (Figure 3.23A,B), to those
that are parenchymatous and exhibit degrees of organographic
differentiation that can parallel that of vascular land plants (e.g.
Leveillia jungermannioides, Figure 3.35A,B). Microscopic
examination of these pseudoparenchymatous forms reveals that
they exhibit a fundamentally filamentous arrangement of their
cells that falls into two basic types: uniaxial and multiaxial.
B.
The uniaxial type of thallus construction is characterized by
a single central filament axis which is then considered to be the
source of lateral filaments comprising the tissue at the organ’s
FIGURE 3.19 Stages in fungal mycelium development showing its very
periphery (Figure 3.24B). The main axis of this filamentous
extensive ramifying nature providing a large surface area for nutrient diges-
tion and absorption. A. Penicillium glaucum. B. Coprinus sterquilinus. S system is capped by an obvious apical cell considered to be
indicates the position of the spore that germinated to produce this hyphal the ultimate source of the main filament and all its branches
growth. (From Troll, 1959.) (Figure 3.24B). The entire uniaxial system is surrounded by
The Relationship between Morphology and Anatomy in Plants 55

+
Sp
Sp −

A.

B. C.

FIGURE 3.20 A. Diagram of the pseudoparenchymatous nature of the fruiting body of a basidiomycetous fungus showing how the parenchyma is a result
of the aggregation of freely growing vegetative hyphal. Basidia-bearing basidiospores represent the tips of the hyphal filaments. B. Block diagram of the
three-dimensional form of a pseudoparenchyma or a fungal fruiting body. C. Longitudinal section through the button stage of the toadstool genus Mycena
showing how much a pseudoparenchyma can resemble a true parenchyma in sectional view. (A, B from Troll, 1959; C from Corner, 1964.)

0.5 MM
0.02 MM

0.05 MM

A. B. C.

2 MM
>3 CM >3 CM

D. E. F. G.

FIGURE 3.21 Stages in the development of the fruiting body of the mushroom Flammulina velutipes, from aggregation of hyphae (A) to the upgrowth of
the coordinated hyphae (B) followed by morphological differentiation (C–G). (From Williams et al., 1985.)
56 Kaplan’s Principles of Plant Morphology

C.

250 µm

10 µm
A.
D.

50 µm
250 µm
B.

FIGURE 3.22 Scanning electron micrographs of pseudoparenchyma formation and fruiting body formation in the basidiomycetous Flammulina velutipes.
A. Aggregation of individual hyphal branches to form a pseudoparenchyma. B. Initial coordinated upgrowth of hyphal mass. C, D. Differentiation of cap
and stipe regions. (From Williams et al., 1985.)

A. B.

FIGURE 3.23 Morphology of freely filamentous red algal species. A. Callithamnion hooker. B. Antithamnion plumula. (From Dixon, 1973.)
The Relationship between Morphology and Anatomy in Plants 57

A. B.

FIGURE 3.24 Three-dimensional interpretation of the pseudoparenchymatous nature of the uniaxial red alga genus Chondria. A. Chondria dasyphylla.
B. Longitudinal section through the apex of Chondria tenuissima. (From Troll, 1959.)

approximated (e.g., in Caloglossa and Membranoptera) that the

lateral tissue has the appearance of a coherent, true parenchyma
(Figure 3.25A,B).
Since primary pit connections (plugged cytoplasmic strands
formed as a result of the incomplete centripetal partitioning of
red algal cells) are formed only between members of a kindred
cell lineage, then tracing the pattern of pit connections should
tell us whether we are seeing a system of independent, closely
approximated filamentous branches or a true parenchyma
A. B. C.
(Figure 3.25B,C). Unfortunately, the occurrence of so-called
“secondary” pit connections between cells of adjacent, non-
FIGURE 3.25 Habit and anatomy of the red alga Caloglossa leprieurii kindred lineages (Dixon, 1973) negates the use of pit connections
(A, B) and the interpretation of cell lineage patterns based on a filamentous, as an indicator of primary cell lineage patterns.
pseudoparenchymatous mode of construction, deduced on basis of primary In contrast to such uniaxial parenchymatous reds, those with
pit connection (C). (From Troll, 1959.) the so-called multiaxial tissue pattern do not show the domi-
nance of a single axial cell lineage, but instead show a number of
a common mucilaginous wall matrix which gives the impres- individual central strands, all of which are traceable to the sum-
sion that such parenchymatous reds are really Antithamnion- mit of a thallus axis and terminating in its own apical initial cell
like filamentous systems which have been secondarily encased (Figure 3.26A,B). Each of these central lineages in turn gives
in a common envelope (compare Figure 3.23 with 3.24B), rise to its own lateral branches along its length. (Figure 3.26B).
hence their interpretation as a pseudoparenchyma. The lat- Such a multiaxial system and its branches are also encased in
eral branches of such a uniaxial system may be so closely a matrix of common wall material (Figures 3.26B, 3.28), and

A. B.

FIGURE 3.26 Basic construction of a multiaxial cell lineage pattern in the red algae. A. Diagrammatic representation showing numerous independent
central cell lineages instead of one. B. Actual specimen of a multiaxial red, Furcellaria fastigata. (From Troll, 1959.)
58 Kaplan’s Principles of Plant Morphology

FIGURE 3.27 Relationship of uniaxial cell lineage patterns to thallus

shape in various parenchymatic Rhodophyta with both radial (A and B,
D and E) and bilaterally symmetrical (C) species. Arrows indicate hypo-
thetical evolutionary lines and structural relationships. (From Scagel et al.,
1965.)

it is this type of image that has been the basis for also calling
such a three-dimensional body a pseudoparenchyma (compare
Figure 3.26 with Figure 3.14B). FIGURE 3.28 Relationship of multiaxial cell lineage patterns and exter-
Regardless of the difference in internal arrangement of nal morphology in parenchymatic Rhodophyta for both bilateral and radial
cells between uniaxial and multiaxial pseudoparenchymatic thallus transectional symmetries (A and B). Arrows indicate hypothetical
Rhodophyta, both groups can show similarities in external evolutionary lines and structural relationships. (From Scagel et al., 1965.)
morphology. Figures 3.27 and 3.28, for example, illustrate the
relationship of cell lineage patterns to external shape in both uni- growth in volume which conforms to our previous definition of a
axial and (Figure 3.27) and multiaxial (Figure 3.28) species. true parenchyma, not a pseudoparenchyma (Figure 3.29).
From these diagrams it is clear that both forms of construction Furthermore, Bugnon (1961) has indicated that if one follows
can be associated with a similar range in morphology, including the developmental history of cell lineages in a uniaxial red,
the differentiation of lateral appendages as well as convergences the pattern of segmentation does not correspond to the model
in types of transectional symmetry. Thus the Florideophycidae of a central axial strand producing lateral branches. For exam-
illustrate graphically the principle that we noted previously in ple, in the two uniaxial species, Hypoglossum woodwardii and
connection with the green algae, that external shape is indepen- Delesseria sanguinea, illustrated in Figure 3.30A and B, the
dent of internal structure. apical cell is continuous not only with the central axial strand,
From a developmental perspective, pseudoparenchyma in the but caps the entire protoplasmic mass derived from it. By mark-
red algae is not the same as we have characterized in the fungi, edly unequal division, their apical cells produce broadly crescen-
and there is a question of whether it should be called pseudopa- tic to lenticular proximal derivatives that subsequently undergo
renchyma at all. In contrast to the situation in the fungi where segmentation to form both the central axial row and lateral cells
parenchymatous structures are clearly the product of a secondary (Figure 3.30A,B). Hence the laterals are not branch derivatives
union of originally independently growing tubes, at no stage of of the central lineage as occurs in a freely filamentous form, such
development of a red algal parenchyma, whether uniaxial or mul- as Antithamnion (Figure 3.23), but all three cells are division
tiaxial, does such a fusion take place. Instead, initially uniseriate products of a broad apical cell derivative (Figure 3.30). Thus
filaments will proliferate from a crustose thallus and branch as delimitation of the axial central cell row depends upon the seg-
they grow out. As they grow in breadth, there is a concomitant mentation of the two lateral derivatives and not vice versa. While
The Relationship between Morphology and Anatomy in Plants 59

the final cell lineage product in these uniaxial reds resembles

that of a filamentous system, its developmental origin is different
and merely a convergence with that pattern.
Such evidence suggests that the tissue masses of the red algae
are true parenchyma and that the only basis for calling them
A. B. C. pseudoparenchymatous is the superficial similarity of their cell
lineage patterns to those in freely filamentous species. Thus, at
best, the notion of pseudoparenchyma in the Rhodophyta is a
comparative morphological abstraction and not the developmen-
tally based concept that we see in the fungi.
D.

Acellular or Tubular Forms of

Construction: Coenocytes
E. F. Another interesting and instructive group of algae are those
whose bodies are not multicellular, but essentially consist of
multinucleate tubes. Such organisms are also called coenocytes
(from the Greek word coenos meaning common and cytos mean-
ing a hollow vessel) or siphonous algae because of their lack of
compartmentation into cells. As mentioned in Chapter 2, their
multinucleate character is due to the uncoupling of nuclear divi-
sion (karyokinesis) from cytoplasmic partitioning (cytokinesis).
G. H. I. Cytokinesis does occur in certain regions and at certain times in
these organisms, but when it occurs, it generally results in wall-
ing off large amounts of cytoplasm and nuclei rather than a single
nucleus and its associated cytoplasm.
Some members exhibit remarkably complex shapes without
being cleaved into multicells. Thus they are the most dramatic
illustration of the principle of the independence of morphol-
ogy from cell and/or tissue geometry. For example, the pin-
nately organized marine green alga Bryopsis corticulans we
illustrated at the end of Chapter 2 is an example of a species
J. K. exhibiting an “Araucarioid” frondose habit but is coenocytic.
Its body consists of an inconspicuous, filamentous, and little-
FIGURE 3.29 Early stages of parenchymatic red algal embryo develop-
ment demonstrating the true parenchyma nature of their plant bodies. A–D.
branched plagiotropic axis, bearing anchoring rhizoids on its
Polysiphonia nigrescens. E–I. Ceramium rubrum. J, K. Cystoclonium pur- undersurface and much-branched orthotropic axes on its upper
purascens. (From Wardlaw, 1955.) side (Figure 3.31A). These erect axes typically consist of a
naked proximal stipe-like region followed by a bipinnately
branched region bearing lateral branches disposed in a single
plane (Figure 3.31A), although some species may exhibit radi-
ally organized pinnae. The branches are initiated in an acropetal

FIGURE 3.30 Cell lineage patterns in the apical meristems of the uniaxial Rhodophyta. A. Hypoglossum woodwardii. B. Delesseria sanguinea. (From
Dixon, 1973.)
60 Kaplan’s Principles of Plant Morphology

FIGURE 3.31 Plant body structure in the siphonous green alga Bryopsis corticulans. A. Overall habit showing rhizomatous basal part and erect fronds.
B. Basal portion of pinnules showing emergence of rhizoidal outgrowths. C. Coenocytic cytoplasm in a branch showing an abundance of chloroplasts which
mask the nuclei. D. Apex of a female plant with branches differentiated as gametangia bearing gametes. Note lack of cross walls except at bases of branches.
Organism is a tube whose complex morphology cannot be the result of cell division. E. Cross wall at base of branch. F. Male gamete. G. Female gamete.
(From Smith, 1955.)

(from the Greek words acros meaning apex and peto meaning differentiation similar to that of Bryopsis (Figure 3.33A). Other
I seek) succession, with the youngest closest to the summit and species, by contrast, show much greater elaboration of these
the oldest toward the base (Figure 3.31D). The main axis in erect shoots. In C. verticillata, the appendages are cylindrical
turn bears second-order branches which typically end in deter- and appear whorled in their arrangement (Figure 3.33B); in C.
minate laterals of a similar two-ranked or bipinnate pattern taxifolia and C. chemnitzia they resemble the lobes of a pinnate
(Figure 3.31A). Microscopic examination reveals this entire leaf (Figure 3.33C,D), whereas in C. prolifera their blades are
elaborate body to consist of a single, multinucleate cell (Figure simple and undissected (Figure 3.33E). In C. cuppressoides the
3.31D). Prior to their abscission, cell wall partitions form only at fronds are bipinnate (Figure 3.33F).
the base of branches and prevent protoplasmic bleeding from the Within this group of siphonous or tubular green algae, there
site of branch fall (Figure 3.31E). are species that are intermediate between full coenocytes con-
Another coenocytic relative of Bryopsis which shows even sisting of single, multinucleate cells, such as we have just char-
greater morphological complexity and remarkable convergence acterized in Bryopsis and Caulerpa (Figure 3.34A), and species
with the organography of higher plants is the siphonous green such as Spongomorpha that are conventionally multicellular,
marine genus Caulerpa. The body of Caulerpa is differentiated i.e., consisting of numerous uninucleate cells (Figure 3.34C).
into a prostrate, rhizomatous portion that grows plagiotropi- Cladophora is such an intermediate because it consists of
cally over the substratum, producing root-like rhizoids that grow branching filaments like those of the coenocytic Derbesia but is
downward and erect branches that grow upward and resemble partitioned into cellular subunits, each of which is multinucleate
leafy shoots (Figure 3.32A). The structural diversity of the erect (Figure 3.34B). Starting with the completely coenocytic condi-
branches and their degree of convergence with shoots of higher tion in Derbesia, where karyokinesis occurs without cytokinesis
plant is simply amazing in a multinucleate, single-celled plant (Figure 3.34A), the situation in Cladophora can be produced
(Figure 3.32B). For example, in Caulerpa fastigata the upright if cross walls are laid down after a certain number of nuclei
shoots are irregularly branched filaments, exhibiting a degree of had been produced (Figure 3.34B). If we then coupled nuclear
The Relationship between Morphology and Anatomy in Plants 61

Cyi
n

A. B.

FIGURE 3.32 Morphology and anatomy of coenocytic green algae, Caulerpa prolifera. A. Organography showing upright fronds, attached to the hori-
zontal rhizome and rhizoids growing down into the substratum. B. Anatomy showing the coenocytic nature of this species with multinuclei (n) in an unseg-
mented cytoplasm. Cyt, cytoplasm; n, nucleus; w, wall. (From Kaussmann, 1963.)

s s
r r

A. B. C.

r
r
a
s

D. E. F.

FIGURE 3.33 Morphological diversity in the siphonous green alga Caulerpa. A. C. fastigata. B. C. verticillata. C. C. taxifolia. D. C. chemnitzia. E. C. prolifera.
F. C. cupressoides. (From Fritsch, 1935.)
62 Kaplan’s Principles of Plant Morphology

A. B. C.

FIGURE 3.34 Transitions between the multinucleate and multicellular conditions found in members of order Cladophorales in green algae. A. Complete
coenocyte as in Derbasia. B. Partially chambered but multinucleate condition in Cladophora. C. Multicellular state found in Spongomorpha. (A, B from
Troll, 1959; C from Bold and Wynne, 1985.)

division with cytoplasmic partitioning, we would arrive at the and tissue types, so-called organs in plants are simply regional
uninucleate, multicellular condition we find in Spongomorpha specializations, outpouchings, or extensions in space that serve
(Figure 3.34C). Such intermediates between multinucleate and to expand the surface area of the plant’s body. Their principal
multicellular species are to be found not only in members of the role is to position the specific tissues of the plant’s body in a par-
Chlorophyta but also in the Rhodophyta (e.g., Griffithsia) as well ticular local environment (whether the soil or the air) to carry out
as in vascular plants. In both gymnosperms and angiosperms, that special biological function. Plant organs and organ systems
both embryos and their nutritive tissue can exhibit coenocytic are not defined by their particular functions or their possession of
initial phases which secondarily become multicellular by wall particular tissue or cell types. The organs of a higher plant have
insertion. The widespread occurrence of the multinucleate con- the same types of cells and tissues. The occurrence of analo-
dition in the plant kingdom provides a different perspective on gies or convergences in function that we have noted in Chapter 1
multicellularity in plants and what it means both developmen- underscores the lack of specificity of organ roles.
tally and functionally. From our survey of the morphology of a range of algal species,
it can be concluded that organ differentiation is independent
of the arrangement of cell and tissue types and even multicel-
lularity itself. For example, the various siphonous greens, such
The Organ Level of Organization
as Bryopsis and Caulerpa, exhibit organ differentiation that con-
Now that we have characterized the varying relationships of cel- verges with that of higher plants without being cut up into cells
lularity to organismal shape and their biological consequences, at all. Similarly, certain Florideophyceae (Rhodophyta) exhibit
we will look at the next level of organization, the organ level. By a degree of organographic differentiation that is notable for its
taking a broad comparative approach we can provide not only a convergence with that of higher plants even though it is based on
basic understanding of what organs are both conceptually and a different cell lineage pattern.
functionally, but also what their relationship is to the cell and For example, the body of the Rhodomelaceous species
tissue levels we have just described. Leveillea jungermannioides is clearly differentiated into leaves,
In contrast to organs in animals, which are structures that have stems and roots and even has axillary insertion of its shoot
specific biological roles and are composed of specialized cells branches like that of seed plants (Figure 3.35A,B). The shoot
The Relationship between Morphology and Anatomy in Plants 63

FIGURE 3.35 Organography of the Rhodomelaceous red alga Leveillia jungermannioides. A. Drawing of organography of plant showing its dorsiventral
shoot with leaves in a two-ranked phyllotaxis (L), axillary shoots (b) and root-like holdfasts initiated from the stem’s ventral surface. (From Kylin, 1956.).
B. Photograph of an unbranched specimen.

of this species has a marked dorsiventral symmetry with leaves It is interesting that the association between the fungus and the
borne in two rows along the dorsal surface (Figure 3.35B). Root- alga induces a unique pattern of development not expressed when
like holdfasts are initiated in a row from the ventral surface of its either of the partners develop alone. Hence the physiological and
stem and function in anchorage and perhaps nutrient absorption biochemical interaction between these two unrelated organisms
(Figures 3.35B, 3.37). Anatomical analysis shows that despite produces a morphogenetic pattern that is singular and about
this organographic convergence, Leveillea is a typical uniaxial whose basic control we know very little.
red and this characteristic is especially evident if you study its An example of the remarkable kind of organographic differ-
structure in the region of the terminal meristem. Not only is entiation that can be expressed in lichens is shown in Cladonia
the uniaxial pattern evident in the stem but also in the develop- verticillata. Its body consists of vertically extended stems bear-
ing leaves (Figure 3.36). Interestingly the ventral holdfasts are ing whorls of appendages or cups at each node (Figure 3.38A).
multiaxial (Figure 3.37). Hence both kinds of red algal “paren- While the actual mode of growth and development obviously dif-
chyma” cell lineage patterns can be found in different organs of fers in detail from that of higher plants, the degree of similarity
the same individual. is striking, and it emphasizes the existence of some overriding
It is remarkable that such organographic differentiation can be organizing principle leading to the development of a complex
found not only in a range of parenchymatic types but is even morphology in an organism consisting of a diversity of parts.
expressed in pseudoparenchymatous bodies such as those of
lichens. Lichens are interesting organisms. They represent a
mutualistic symbiosis between a fungus and a unicellular photo-
troph, typically either a green alga or a blue-green bacterium. In Question of the Relationship of Cell
this relationship the alga supplies the carbon source through pho- Arrangements to the Generation of
tosynthesis and the fungus provides the bulk of the plant body
Shape in Multicellular Higher Plants
which serves as both a protection and a source of water and min-
eral elements for the symbiont. Like the fungal fruiting bodies, Now that we have described the various kinds of cell and tis-
the lichen thallus is a pseudoparenchyma which owes its origin sue geometries found in a broad range of the plant kingdom and
to the secondary aggregation of fungal hyphae (Figure 3.38B). have examined their biological implications, we want to use that
64 Kaplan’s Principles of Plant Morphology

FIGURE 3.36 Detail of terminal meristem of shoot of the red alga Leveillea jungermanniodes showing stages in leaf development and of axillary
branches. Note stems are inserted in leaf axils.

R R

FIGURE 3.37 Detail of the embryonic part of the shoot illustrating stages of the initiation and early development of the multiaxial holdfasts (R) from the
ventral surface.
The Relationship between Morphology and Anatomy in Plants 65

A. B.

FIGURE 3.38 A. Body of the lichen Cladonia verticillata. B. Transection of the lichen thallus of the genus Parmelia illustrating its pseudoparenchyma-
tous nature. a, algal symbiont. (A from Goebel, 1928; B from Scagel et al., 1965.)

information to try to answer the question we posed at the begin- higher plants and yet do not consist of cellular subunits at all!
ning of this chapter, namely, is the shape of plants merely the And it is bolstered especially by some of the red algae, such
consequence of cell and tissue arrangements or are they indepen- as Leveillea, which also exhibit organographic differentiation
dent of one another? nearly identical to that of higher plants but with a uniaxial mode
If we return to the examples of convergence in external form of tissue construction.
between members of unrelated groups of organisms we intro- Such broad comparative evidence was the basis of the great
duced at the end of Chapter 2 and link them now with the ana- plant morphologist Wilhelm Hofmeister’s rejection in 1867
tomical information from this chapter, we can see that despite a of Schleiden and Schwann’s (1839) “Cell Doctrine” for plants.
superficial similarity in their “araucarioid” habit, these organisms Hofmeister concluded that formation of cells in plants is a con-
exhibit radically different arrangements of their cell lineages. sequence of general growth, not its cause. There have been many
For example, the conifers Araucaria and Thuja, the flowering plant biologists who have agreed with his opinion since that time
plant Asparagus, the clubmoss Selaginella, and the true moss (Sinnott, 1960).
Hylocomium are all constructed of a true parenchyma but with More recently, experimental evidence has supported
their own distinctive cell lineage patterns. By contrast, Bryopsis Hofmeister’s view. Working at the Oak Ridge National
is a coenocyte and the red algae Ptilota and Microcladia are par- Laboratory, Alan Haber, William Carrier, and Donald Foard
enchymatous but with a filamentous alignment of their tissues (1961) produced what they termed as “gamma plantlets” by
different from that of the land plants. subjecting ungerminated wheat grains to high (800 kr) chronic
This comparative information alone suggests that there is NO doses of Cobalt 60 source gamma irradiation. They then studied
strict relationship between cell arrangements and organismal the anatomical features of seedling leaf development in the irra-
shape. This conclusion is graphically demonstrated in the coe- diated and unirradiated controls.
nocytic species, especially the genus Caulerpa, whose species As a result of this irradiation treatment, cell division was elim-
exhibit some remarkable convergences with the organography inated while all other physiological and growth features were
66 Kaplan’s Principles of Plant Morphology

52 EPIDERMIS 51 EPIDERMIS 149

137 145 133
150 UNIRRAD. CONTROLS
49 MESOPHYLL 51 MESOPHYLL 429
100
128 119 138
60

40
GAMMA -
PLANTLETS
LEAF LENGTH (mm)

20 1mm

10
800 kr 0 kr
(10 days) (3 days)
6

4
C.
3 EMBRYO
2 (0 DAYS)
1.5

1.0
0.7

1 1.5 2 3 5 1 1.5 2 3 5
LEAF WIDTH (mm)
A. B. D. E.

FIGURE 3.39 Comparison of growth and anatomical features of first foliage leaves of control and gamma plantlets of wheat, Triticum vulgare. A, B.
Comparison of log–log allometric plots for growth of first foliage leaf of unirradiated controls (A) and gamma plantlets (B). C–E. Comparison of anatomi-
cal features of first foliage leaf in the ungerminated grains, and the irradiated and unirradiated controls for wheat Triticum vulgare. (From Haber, 1962.)

nearly normal. While the first foliage leaf in the gamma plantlets it might be difficult to see an obvious structural relationship
grew more slowly, it exhibited the same type of polarized growth between the siphonous algae and higher plants. It is also pos-
as the first leaf of the control and hence developed the same basic sible to dismiss the morphological complexity of Bryopsis and
shape (Figure 3.39A,B). Cell counts in both the epidermis and Caulerpa as simply being anomalous and hence irrelevant to
mesophyll along the length and width of leaves of both the irra- the interpretation of the growth and development of land plants.
diated and control seedlings and their comparison with those With a limited perspective, it might also be easy to dismiss Haber
of the first leaf of an ungerminated grain demonstrated that the et al.’s (1961) results as experimental artifacts that really tell us
polarized form of the leaf of gamma plantlets grew without cell nothing about higher plant modes of construction and morpho-
division; longitudinal and transverse cell numbers were virtu- genesis. But a more detailed analysis of the nature of the basic
ally identical to those in the first foliage leaf primordium in the construction of vascular plants makes it clear that there is in fact a
ungerminated seed (Figure 3.39C–E). Haber (1962) summa- more fundamental connection between coenocytic and multicel-
rized the interpretation of their results in Figure 3.39 contrasting lular higher plants than one would at first expect and suggests that
the two principal theories of the relationship of cell division to the gamma plantlet research is relevant to an understanding of
the generation of organ form in plants. the relationship between cellularity and morphogenesis in plants.
Results of the gamma plantlet research clearly supported Despite their predominant multicellularity, higher plants
Theory 2 and also support what we have seen in the numerous exhibit coenocytic phases of development that we have men-
examples examined in this chapter, namely that morphology is tioned above, including endosperm and megagametophyte
independent of cell and tissue arrangement. For all intents and development in flowering plants and gymnosperms and even
purposes, Haber et al. (1961) had converted the first leaf of wheat proembryo development in coniferous gymnosperms. In all
into a developmental coenocyte because they had uncoupled these cases, karyokinesis and cytokinesis are separated in
morphogenesis or shape generation from cell division. time so that nuclear proliferation occurs first, followed by
Since the obvious multicellularity in vascular plants and the wall formation so that ultimately each nucleus and its imme-
initiation and growth of organs in higher plants normally is inex- diately surrounding cytoplasm are delimited as a single cell
tricably linked with the mitotic division of cells, at first glance (Figure 2.39D–G, P–Q).
The Relationship between Morphology and Anatomy in Plants 67

non-protoplasmic portions of the plant body. Furthermore, the

process of cytokinesis by cell plate formation which, in effect,
is a secondary chambering or partitioning of a unified protoplast
rather than a process of cleavage of cells from one another, also is
an expression of the fundamental unity of the plant’s protoplasm,
with cellularization being a secondary phenomenon. Such an
interpretation has been expressed by Wolfgang Hagemann (1978,
1982) in his concept of the “phragmoblastem” in which this spe-
cial coenocytic type of wall partitioning is seen to be the result
of a phragmoplast type of cell division mechanism.
A fundamental and consistent model of plant multicellularity
recognizes a developmental and constructional linkage between
siphonous algae and multicellular plants. Instead of viewing the
higher plant body as consisting of individual cells that have been
stacked together, analogous to bricks used to build an edifice,
FIGURE 3.40 Phragmoblasteme type of cell partitioning mechanism
found in higher plants whereby a cell plate arises as the result of fusion of
this model views the higher plant protoplast as being compart-
Golgi-derived vesicles (G) first at the cell center and then spread centrip- mentalized secondarily into cells. The analogy would be having
etally until they fuse with the parent cell wall. D, dictyosome; E, trapped two houses that have the same external shape or architecture but
endoplasmic reticulum at site of plasmodesmata; G, Golgi vesicles; M, differ as to how they are chambered internally into rooms. While
microtubules; N, nucleus; Z, cell plate. (From Hagemann, 1982.) room distribution and shape may be constrained by the external
shape of the house, room partitioning and shape are not strictly
However, more significantly, multicellular plants are in fact dependent upon building shape. Conversely, house shape is not a
both structurally and functionally coenocytic organisms. When a result of room shape or distribution. Plant cells are analogous to
higher plant cell divides into two cells by mitosis, partitioning of the rooms in a house and exhibit the same independent relation-
that original parent cell at telophase involves formation of a cell ship to the organism’s external shape.
plate across the phragmoplast microtubules (Figure 2.7F). The To make this model of plant construction more explicit
cell plate arises from the coalescence of Golgi-derived, mem- and clearer, Figure 3.41 has taken the basic shape of a shoot
brane-bound vesicles which initially fuse in the center of the par- of Bryopsis (Figure 3.41A) and redrawn it with its proto-
ent cell and then continue to unite centrifugally until they reach plast partitioned in the uniaxial multicellular pattern of a red
the periphery of the surrounding parent cell wall (Figure 3.40). alga (Figure 3.41B) and the cell lineage pattern of a vascular
The vesicles contain the precursors of the middle lamella which plant (Figure 3.41C). Such models illustrate the independence
upon fusion polymerize to form the initial cross-wall; the vesicu- between plant shape and internal structure and express the type
lar membranes unite to form the plasma membrane on each side of convergence in external form that we have documented to
of the newly inserted partition (Figure 3.40). The phragmoplast occur in unrelated members of the plant kingdom.
microtubules are considered to serve as templates and lines of According to such a model, the cells of a plant are not viewed
contact for the transport of Golgi vesicles from the periphery to as the cause of growth but simply internal markers of that growth.
in the center of the cell. As the fusing vesicles extend the cell They are analogous to the ink marks you place on the outside of a
plate laterally, the early microtubules at the center are thought to plant body in order to determine its locus of growth. In the same
disassemble and reassemble at the periphery of the parent cell to way that you would not look for the cause of the displacement of
serve as templates for vesicles added there (Figure 3.40). those external marks in the ink marks themselves, one doesn’t
At points where strands of endoplasmic reticulum become
entrapped between adjacent fusing vesicles, interruptions in the
cell plate occur, and hence at these sites the cytoplasm is con-
tinuous between the two adjacent daughter cells. These micro-
scopic cytoplasmic connections are the plasmodesmata we have
already encountered in our consideration of Volvox at the begin-
ning of this chapter. Using both dye transfer experiments and
microelectrode studies, plasmodesmata have been demonstrated
to be the sites of transport of small molecules between adjacent
plant cells.
Plasmodesmata in higher plants represent a fundamental con-
tinuity of the protoplasm of a higher plant through these micro-
scopic, cytoplasmic channels. Hence the partitioning of the higher
plant into multicells is incomplete and they too are actually coe-
nocytes. Such a physiological unity of the higher plant protoplast
has long been recognized by plant physiologists in the areas of
FIGURE 3.41 Model of plant multicellularity where all three plant types
water and mineral transport by their use of the terms symplast to exhibit the overall shape of a Bryopsis coenocyte (A) but then have their
refer to the interconnected protoplasm of the plant and apoplast protoplasts secondarily chambered into cell lineages typical of a uniaxial
to refer to the cell wall and intercellular space systems, i.e. the red alga (B) or a vascular plant (C).
68 Kaplan’s Principles of Plant Morphology

One of the primary roles of multicellularity is mechanical sup-

port. The honeycomb network of intersecting rigid cell walls is
undoubtedly a major factor permitting plants to be self-standing
in a land environment. We see such a diversity of patterns of cel-
lularity preserved in the course of evolution in the algae because
the aquatic environment has not selected against any of these
alternatives. However, once plants invaded the land, presumably
only the multicellular, parenchymatous type of body construc-
tion supplied the kind of three-dimensional support that allowed
them to function as free-standing photoautotrophs. Thus as
Hagemann (1982) has suggested, the development of “cells” as
we know them in plants with their own set of organelles and one
nucleus was the price paid for the erection of such a wall stabi-
lizing system. Hence the concept of the “cell” in plants is of an
entirely different nature from that of animals.
Support for such interpretations comes from analogies to walls
that we find in some of the larger siphonous algae. For example
Caulerpa (Figure 3.43A), which we have previously demon-
strated to be a giant coenocyte, nevertheless develops a periph-
eral network of wall ingrowths or trabeculae that protrude into
the cell lumen and undoubtedly provide an additional measure
of support in these relatively large (up to about 30 cm in length)
marine algae. Trabeculae are produced in greater density in the
prostrate “rhizomatous” portion (Figure 3.43B), but are also
found in the erect fronds (Figure 3.43C,D). Similar kinds of
strands have also been reported in some of the larger species of
FIGURE 3.42 Apical meristem of the uniaxial red alga Platysiphonia. its close relative Bryopsis (Fritsch, 1935).
(From Bold and Wynne, 1985.) In addition to its biomechanical role in support, Hagemann
(1982) has suggested that the intersecting wall honeycomb in
view the cause of growth in the cellular subdivisions of the plants multicellular plants is also important for water transport from
body. The plant is growing up through its cells rather than the roots to shoots in the land habitat. In contrast to the algae whose
other way around. bodies are typically surrounded and bathed by water, land plants
It is interesting that once one adopts this outlook on plant of significant size and stature must depend on the internal trans-
multicellularity, a whole host of developmental morphological port of water. Certainly apoplastic transport of water and min-
questions are viewed from an entirely different perspective. For eral elements is an important pathway across roots and across
example, if we look again at the apical meristematic region of a the leaf to the atmosphere via transpiration, which, in addition to
uniaxial thallus of a red algal genus such as Platysiphonia shown the mechanical stability element, also may have influenced how
in Figure 3.42, its protoplast looks like a unified structure which large these organisms could become in this new environment.
is secondarily being segmented; the apical cell looks like a cap Finally, the cleavage of the plant protoplast into multicells
fitted over the entire protoplast as a unit. It is only after par- obviously is of prime significance as a primary source of cell
ticular patterns of cell division and the subsequent cell products specialization and function. Since we have shown that it is prin-
secrete increasingly thickened walls around themselves that the cipally the cell to tissue levels of organization that execute the
filamentous geometry and pseudoparenchymatous appearance of various functions of the plant, it is expressed most markedly in
its body becomes apparent. The existence of such a protoplasmic the diversity of cell types that one finds specialized for those
unity leaves little doubt that we are dealing with a true paren- functions. The development of special tissues for photosynthesis,
chyma in these species. transport, and storage as well as mechanical support is a way of
providing an increased internal surface area and at the same time
solving the problem of physiological differences between outside
and inside of a three-dimensional parenchymatous tissue mass.
By concentrating photosynthetic tissues at the periphery of the
The Biological Significance of sphere, the light interception and gas exchange problems that a
spherical tissue mass are avoided. At the same time those cells
Multicellularity in Plants
at the interior can serve a role in food storage and transport in
If we conclude that multicellularity in plants is not the cause of addition to contributing to mechanical support.
their growth or shape but merely one of the correlates of a plant’s If you look at a cross section of a plant axis, whether from a
morphogenesis, what then is the value of having the plant’s pro- vascular plant or a red or brown alga, and hence independent
toplast cleaved into these subunits we traditionally have called of what the cell lineage patterns are, they all show a similar
cells? Here again, we can draw upon our broad comparative per- expression of the tissue and cell-type zonation just mentioned
spective of other plant groups for insights. (Figure 3.44A–C). This is particularly striking in the red algae
The Relationship between Morphology and Anatomy in Plants 69

ps

ax

co

A.

A.

ax

t ps

co

B.

B. C.
c t t

ps

D.
s
co

FIGURE 3.43 A. Morphology of coenocytic marine green alga, Caulerpa

prolifera. B. Transection of prostate rhizomatous axis showing abundance
of wall ingrowths (t). C. Longisection of assimilator blade showing less ax
dense trabeculae. D. Part of thickened wall with wall ingrowths shown. (A
from Troll, 1959; B–D from Fritsch, 1935.)

(Figure 3.44A), which traditionally have been viewed as hav-

ing a relatively low level of cell specialization and tissue devel-
opment (Whittaker, 1969), i.e. just a step removed from freely C.
filamentous forms. It is clear, however, that regardless of what
the pattern of generation of cells has been in members of each FIGURE 3.44 Anatomical comparison of histological zonation between
of these evolutionary lines, that there are some overriding func- a red alga Aghardiella (A), a brown alga Desmarestia (B), and a flowering
plant (Helianthus annuus). (C). Notice in all three cases the existence of
tional characteristics that result in tissue zonations in these spe-
small photosynthetic (ps) cells at the periphery, then larger cortical storage
cies that are nearly identical to that of a higher plant (compare cells (co) and then conducting strands at or near the axis center (ax). (A, B
Figure 3.44A,B with 3.44C). from Scagel et al., 1965; C from Troll, 1959.)
70 Kaplan’s Principles of Plant Morphology

Conclusions SUMMARY: UPDATES AND OBSERVATIONS

Having established that there is, indeed, a fundamental and Dr. Raymund Chan
broadly-based independence between the anatomical and mor- In this chapter, Kaplan asks whether the shape of a plant
phological levels of plant organization, it now becomes justifi- is merely the consequence of cell and tissue arrangements.
able to treat morphology on its own, especially since it has been He argues that single cells are not really the building
so neglected in the recent past. Undoubtedly the basis of the blocks of plant form, as the external shape is independent
neglect was the assumption that anatomy was the basis of mor- of internal structure; i.e., morphology is independent of
phology and that it seemed more profitable to study its cause than cell and tissue arrangement. Also, organ differentiation is
its superficial expression. Hopefully this chapter has laid that independent of the arrangement of cell and tissue types
bias to rest and we can now give the subject of plant morphology and even of multicellularity itself. Kaplan thus illustrates
the attention it deserves. that, since the final plant form is not simply the result of
internal anatomy, plant morphology should be studied on
its own without bias.
4
Plant Embryogenesis: The Origin of Morphological
Organization during Development

CONTENTS
Concept of Embryogenesis in Plants......................................................................................................................................................71
The Context of Embryogenesis...............................................................................................................................................................72
The Spatial Relationships between Embryos and Their Nutritive Sources in Vascular Plants..........................................................72
Pteridophytes and Lycophytes (Spore-Bearing Vascular Plants)..................................................................................................72
Seed Plants.................................................................................................................................................................................... 74
Temporal Relationships between Embryos and Their Nutritive Sources in Vascular Plants.............................................................77
A Description of Embryogenesis in Vascular Plants..............................................................................................................................79
Seed Plants.........................................................................................................................................................................................79
Non-Monocot (“Dicot”) Angiosperms and Gymnosperms..........................................................................................................79
Monocotyledons.................................................................................................................................................................................86
Lycophytes and Pteridophytes...........................................................................................................................................................93
Lycophytes....................................................................................................................................................................................93
Pteridopytes.......................................................................................................................................................................................98
Psilotopsida...................................................................................................................................................................................98
Sphenopsida..................................................................................................................................................................................99
Pteridopsida..................................................................................................................................................................................99
Principles of Embryogenesis...................................................................................................................................................................99
The Relationship between Embryo Morphology and the Subsequent Architecture of the Plant..........................................................100

We now begin a study that is the focus of this book, namely plant development. This involves determining when the primary
an analysis of the fundamental morphological principles that meristems of the plant body, the shoot and root apex, first appear
account for the major variations in plant form. In this analysis in ontogeny and the kind of activity they manifest in their earliest
our perspective will be ontogenetic, using the developmental stages. We also are interested in what ways the morphology of
history of an idealized plant (Figure 1.7) as our framework. the embryonic plant is related to and/or predicts the architecture
Starting with the origin of an individual plant from fertilization, of the larger, fully developed plant. While the embryos of plants
we will follow the development of its shoot and root systems as are in no way miniatures of the adult, one can see in the embryo
a basis for determining how morphological diversity in these positional relationships of organs that foretell the architecture of
major organ components comes about. the adult plant. We will examine that expression in several clear
In this chapter begin by asking how and when the basic ground examples. But before going into the details of embryogenesis
plan we have characterized for higher plants (Figure 1.7) has itself, we need to review the concept of embryo development in
its inception. The earliest phases of plant development, called plants and how it relates to that in animals.
embryogenesis, begin with the initiation of higher plant orga-
nization from the single-celled, fertilized egg or zygote and
proceed through the stages of its elaboration into a multicellular
young plant with rudiments of all the organ systems.
Concept of Embryogenesis in Plants
Traditionally, most presentations of plant embryogenesis have
focused on the anatomical aspects, principally the cell lineage Since the focus of this book is principally the morphology of vas-
patterns associated with the generation of plant form (Johansen, cular plants (Tracheophyta), embryogenesis here refers to the ear-
1950; Wardlaw, 1955; Natesh and Rau, 1984). Historically, the liest phases of development of the diploid, sporophyte phase, or
impetus for such cell linage investigations came from studies of the dominant phase, of their life histories. In contrast to embryo-
animals where there has been a concern for reconstructing the genesis in most higher animals where organ formation is con-
developmental fate of certain cells in the young embryo or even fined to the earliest phases of development and where subsequent
certain zones in the egg. Having suggested in the preceding chap- development to adulthood consists principally of the enlarge-
ter that cell lineage patterns are not the cause of form in plants, in ment and maturation of those organ rudiments, plant embryonic
this chapter we will emphasize instead the morphological aspects development is not so confined and therefore is more difficult
of embryo development. We will be concerned with the more to delimit. Because of the existence of apical meristems at their
general problems of how the organ systems become defined and extremities, plants continue to initiate new organs and incre-
when their characteristic topography is first established during ments of growth throughout their lives. They have embryonic

71
72 Kaplan’s Principles of Plant Morphology

regions for their entire existence. In fact, virtually all of a plant’s

physiology, including nutrient and water uptake and transport are The Context of Embryogenesis
dependent upon the existence of growing regions which serve as
sinks for these substances. While plants do exhibit periods of Before delving into the details of embryo differentiation itself,
cessation of growth or dormancy where a low level of metabolic it is important to review briefly some of the characteristics of
activity is sustained at the cell level, in general, much of their the local environment in which the embryo develops, because
whole-plant physiological activities are linked inextricably to it obviously plays a significant but as yet unspecified role in the
their continuing growth. mode of morphogenesis that occurs.
Given such long-lived embryonic activity, it is impossible to
give a complete account of a plant’s morphology or development
until it has ceased organ formation at the end of its life. This is The Spatial Relationships between Embryos and
much less of a problem for annual plants which complete their life Their Nutritive Sources in Vascular Plants
history during one growing season and hence have a reasonably Pteridophytes and Lycophytes
circumscribable size and extent of organ formation. It becomes (Spore-Bearing Vascular Plants)
an almost impossible task, however, in dealing with long-lived
perennial species, such as a 3000- to 4000-year-old redwood. In most members of the spore-bearing (or non-seed bearing) vas-
Not only are such plants infinitely larger and structurally more cular plants, the embryonic sporophyte develops initially inside
complex, but in lifespan they obviously exceed the lives of the the archegonium, within the tissues of the parent gametophyte
plant morphologists who may want to study them. Fortunately, plant. Although variable in different species, the archegonia
a certain amount of repetition exists between seasonal cycles of of most pteridophytes have their venter or basal egg-bearing
plant development that allows one to generalize from the study regions embedded to varying degrees in the parenchyma of the
of a more limited phase of the life of the plant to the full devel- gametophyte with the neck or sperm-receiving region project-
opmental expression of its morphology. ing from the gametophyte surface (Figures 2.26GH; 2.28I,J;
Such extended embryonic activity therefore makes it impos- 2.30H,I; 2.32G,H; 2.33J,L). As the young sporophyte grows,
sible to define the concept of an embryo in plants. Hence while it expands increasingly into the parenchyma of the parent game-
we can define the beginning of embryogenesis as marked by tophyte which serves as the initial source of its nutrition until
fertilization, delimitation of its termination is impossible and it becomes an independent, self-nourishing plant (Figures
always artificial. In the case of seed plants, where the seed plus 2.26N,O; 2.28L–N; 2.30 O–P; 2.32M,N; 2.33O,P).
or minus the surrounding parent sporophytic tissue is the unit Despite this general relationship of embryos to their parent
of dispersal to a new habitat, and where development is arrested gametophyte, members of the respective lineages differ mark-
with the onset of dormancy prior to this dispersal, it has been tra- edly in the basic orientation of their embryos with reference to
ditional to characterize embryogenesis as development up to the the parent gametophyte. Two principal types of embryo polar-
time of seed dormancy. While this may be a workable definition ity have been defined: endoscopic and exoscopic. In endo-
for most seed plants, it does not work for embryo delimitation scopic polarity, the shoot tip of the embryo grows toward the
in non-seed plants, where the meiospore rather than the sporan- tissues of the parent gametophyte (Figure 4.1A), whereas in
gium is the unit of dispersal and where there is no dormancy in exoscopic polarity, the initial direction of sporophyte shoot
young sporophyte development. It also is not a workable defini- growth is away from the tissues of the parent gametophyte
tion for seed plants such as viviparous mangroves (Chapter 6) (Figure 4.1B). Seed plant embryos (gymnosperms and angio-
which have no dormancy period, or species that disperse their sperms) have an endoscopic polarity and their shoot poles grow
seeds from the parent plant before actual dormancy sets in and into the gametophytic or gametophyte-derived nutritive tissue
in which the contained embryo is fully developed (e.g., coconut (Figures 4.1B, 4.3). As we shall see in Chapter 5, emergence
palm, Figure 4.11; Chapter 5). of seed plant embryos from the seed is initiated by growth of
Moreover, the degree of embryo development at the time of the primary root out through the micropyle, i.e. the opening
dormancy also is too variable to offer anything but an arbitrary between the integuments.
delimitation. In angiosperms alone there is a tremendous range Traditionally these differences in embryo polarity have been
of variability in the degree of morphological complexity exhib- considered to have their earliest expression at the time of the
ited by the sporophyte at the onset of dormancy. It extends from first division of the zygote. In the case of an embryo with an
embryos of grasses which exhibit not only the primordia of sev- endoscopic polarity, the first zygotic division is transverse to
eral leaves in their terminal buds, but also many shoot-borne the long axis of the archegonium and derivatives of the apical
root primordia, to embryos of orchids which, at seed maturity, cell (i.e., that cell oriented toward the neck of the archegonium)
typically develop only to a spherical parenchymatic stage with ultimately form the foot and/or root pole, whereas derivatives
no sign of leaf or root differentiation (Chapter 5). Yet despite of the basal cell (i.e., that oriented toward the venter) form the
these problems of circumscription, unique organogenetic events shoot (Figure 4.2B,C). By contrast, in an exoscopic embryo, the
occur at these earliest stages of plant ontogeny that are critical to developmental fates of apical and basal cells at the two-celled
our understanding of plant development at the later stages. For stage are just the reverse; the shoot pole is derived from the distal
these reasons it is worth looking at these earliest processes of cell in the archegonial neck rather than the proximal cell in the
organogenesis and meristem differentiation comparatively in a venter (Figure 4.2A). Depending upon whether a suspensor is
range of species. developed, the so-called basal cell can develop into either the
Plant Embryogenesis 73

suspensor or the foot (Figure 4.2B,C). A suspensor is typically

Archegonial neck
a filament that elongates early in embryogeny to place the devel-
Shoot oping embryo into a more central position in the surrounding
gametophytic tissue. We will have more to say about the other
Root biological roles of the suspensor when we discuss embryogenesis
Foot in detail below.
Unfortunately, not all plants whose embryos ultimately exhibit
Megagametophyte either endoscopic or exoscopic polarity show a consistent cor-
relation of this polarity with the plane of the first zygotic divi-
A.
sion. For example, in the clubmoss Selaginella, whose embryos
are all endoscopic with reference to their nutritive source and
Archegonial neck
develop suspensors, the plane of their first division may be either
Suspensor parallel or perpendicular to the long axis of the archegonium
(Figure 4.34A,B, H–J). Similarly, in the quillwort Isoetes,
Root Foot also a member of the Lycophyta, the plane of first division may
be variable, even parallel to oblique to the axis of the archego-
Megagametophyte nium, yet the ultimate orientation of the embryo is exoscopic
Shoot (Figure 4.35A,B,D,L). The same seems to be true for various
species of the horsetail Equisetum (Sphenopsida) whose embryo
is also exoscopic (Figure 4.32A,B,K). Thus it can be concluded
B. that the plane of the first division of the zygote does not rigidly
predict embryo polarity. For these reasons, it is better to use the
FIGURE 4.1 Orientation of fully developed embryos with reference to the
terms endoscopic and exoscopic with reference to overall embryo
gametophyte nutritive tissues and the archegonia in A, an exoscopic embryo
without suspensor with the shoot pole oriented toward the archegonial neck,
orientation in the gametophyte rather than to the plane of cell
and in B, an endoscopic embryo with a suspensor and with the shoot pole division (Figure 4.1).
oriented downward, toward the interior of the gametophyte. Gametophyte Among vascular plants, embryos in Psilotopsida (Psilotum)
tissue darkly shaded and embryo lightly shaded. and Sphenopsida (Equisetum) are exoscopic (Figures 2.28N,
2.30P; 4.31, 4.32) as are species in the genus Ophioglossum and

FIGURE 4.2 Types of polarity exhibited by the embryos of vascular plants and their putative relationship to the first division of the zygote. A. Exoscopic
polarity. B. Endoscopic polarity without a suspensor. C. Endoscopic polarity with a suspensor. D. Prone polarity of a fern embryo. E. Ultimate contributions
of embryonic sections to adult plant morphology when in prone position. In these figures the apical cell that gives rise to the shoot pole is black whereas the
basal cell that either gives rise to foot and root is hatched or stippled where it becomes a suspensor. a, apical cell; b, basal cell; s, suspensor. (From Foster
and Gifford, 1974.)
74 Kaplan’s Principles of Plant Morphology

Here the first dividing wall of the zygote is parallel rather than
transverse to the long axis of the archegonium and hence the
so-called apical and basal cells lie adjacent to one another rather
than being superposed (Figure 4.2D,E). Such embryonic polar-
ity has been termed prone because the shoot and root poles of
the fern embryo ultimately lie in a horizontal plane, parallel
Suspensor su to the long axis, on the underside of the parent gametophyte
I I
Embryonic cell em (Figure 4.4). Such prone embryos also lack a suspensor and
their first leaf and root emerge from the undersurface or ven-
tral side of the gametophyte rather than penetrating internal
tissues as endoscopic sporophytes typically do (Figure 4.4F).
In addition to the leptosporangiate ferns, such prone embryo
A. polarity is also reported in some members of the eusporangiate
Ophioglossaceae.

Seed Plants
In the gymnosperms and angiosperms, embryogenesis takes
place within the confines of the ovule. As reviewed in Chapter
su 2, the ovule is an integumented megasporangium in which the
I I functional megaspore is retained in the megasporangium or
h
Embryo II II nucellus and the megagametophyte tissue developing from it is
e nourished by the diploid, sporophytic nucellar tissue. After fer-
tilization of the zygote, the embryo will grow at the expense of
nutrients supplied either by the megagametophyte tissue, as in
the gymnosperms (Figure 2.38) or at the expense of a fertilized
B.
derivative of that female gametophyte tissue, the endosperm, as
in angiosperms (Figure 2.39). Usually, development of the ovule
until the time of seed maturity and dormancy occurs on the par-
ent sporophytic plant which supplies the developing seed with its
ultimate source of nutrients from the photosynthetic activity of
its shoot system.
Ovule morphology, especially in flowering plants, can be
varied and in turn can exert some influence on the shape the
su developing embryo assumes until dormancy. Ovules typically
I I are differentiated into a nucellus, integument(s), chalaza, raphe,
and funicle (Figure 4.5A,B). The nucellus is the megasporan-
Embryo II II gium and the site of differentiation of the megasporocyte which
will subsequently undergo meiosis in situ to form the four
haploid megaspores, one of which in turn will ultimately form
the megagametophyte or embryo sac (Figures 2.39; 4.5B). If
C.
the nucellus is relatively massive (Figure 4.5A) it is termed
FIGURE 4.3 Stages in the early development of an endoscopic embryo
crassinucellate (from the Latin crassus meaning thick) and if
with a suspensor. A. First division of zygote producing a suspensor initial it is thin (Figure 4.5B) it is termed tenuinucellate (from the
cell (su) directed toward the archegonial neck and an embryonic cell (em) Latin tenuis meaning narrow). Since the developing megaga-
directed toward the venter. B, C. Stages in parenchyma formation in the metophyte grows at the expense of the surrounding nucellar
embryonic initial cell. (From Foster and Gifford, 1974.) tissue, the extent to which the nucellus remains in an ovule at
the time of fertilization usually depends upon whether it was
crassinucellate or tenuinucellate; typically it will persist in
some species of Botrychium in eusporangiate ferns as well as crassinucellate ovules whereas it will be used up and absent in
Actinostachys in the leptosporangiate ferns (Bierhorst, 1968). tenuinucellate ovules.
In such exoscopic species, basal cell derivatives are involved in The integument(s) is a collar-like growth from the base of
formation of part of the embryonic first root and foot region, the the megasporangium which ultimately encloses the nucellus,
latter functioning in nutrient absorption. leaving only a narrow-diametered canal, the micropyle, as the
Endoscopic embryo polarity is exhibited by most Lycophyta nucellar entrance (Figure 4.5A,B). Development of the integu-
and seed plants as well as three genera of eusporangiate ferns ment around the nucellus is analogous to a sack with a drawstring
in the family Marattiaceae. Most leptosporangiate ferns, which being pulled up around a ball and then pulling the drawstring
comprise the largest group in division Pteridophyta, exhibit to constrict the opening (Figure 4.6A–C). In the case of the
an embryo polarity which is neither exoscopic nor endoscopic. ovule, the opening is the micropyle that ultimately becomes
Plant Embryogenesis 75

G
G

Emb
Foot

AN
A.

AN LI
B.
R1

G AN
C.

Emb
D.

Foot

Foot
AN

SA
L1
SA

L1
R1 R1

AN
E. F.

FIGURE 4.4 A–C, E and F. Stages of embryo development in the fern Pteridium aquilinum and D, Pteris serrulata, showing the relationship or the embryo
to the gametophyte tissue and the morphology of germination of the embryo from the gametophyte tissue. AN, archegonial neck; Emb, embryo; G, gameto-
phyte; L1, leaf one; R1, first root; SA, shoot apex. (From Hofmeister, 1851.)

narrowed to the tiny canal in the mature, pollen-receptive ovule straight (Figures 4.7A; 4.9A,F). Orthotropous ovules are found
(Figure 4.5A,B). in some angiosperms and many gymnosperms.
Ovules in flowering plants may have one, two, or even no By contrast, ovules of the majority of flowering plants exhibit
integuments, whereas those of gymnosperms typically have some degree of curvature which alters the positional relationship
a single integument. Where a second integument is devel- between chalaza and micropyle. For example, in the most wide-
oped in angiosperms, the inner is usually initiated before and spread type, the anatropous ovule (from the Greek ana meaning
sometimes simultaneously with the outer (Bouman, 1984) up and tropous meaning turning) unequal growth occurring in
(Figures 4.6A–C; 4.8D,E). The integuments protect and nour- the raphe on the convex side of the ovule primordium results
ish the nucellus and its contents, and, along with the chalaza and in the micropyle being turned through 180 degrees and lying
raphe, form the seed coat in the mature seed (Figure 4.5). adjacent to the funicle (Figures 4.7C; 4.8). Since embryo sac
The ovule is attached to the carpel wall by the funicle or stalk or megagametophyte enlargement does not take place until
(Figure 4.5A). The part of the funicle that runs parallel with the after the curvature occurs, the female gametophyte is uncurved
nucellus is called the raphe (Figure 4.5A). The chalaza is the (Figures 4.7C; 4.9B,G).
region between the nucellus and the raphe where the integuments The so-called hemitropous type (from the Greek hemi mean-
are inserted (Figure 4.5A,B). Even though funicle, raphe, and ing half) is intermediate between orthotropous and anatropous
chalaza can be delimited positionally, they form a continuous tis- ovules because the growth curvature in the raphe only occurs
sue that, with the integuments, ultimately becomes differentiated through 90 degrees. As a result, the micropyle is oriented hori-
as part of the seed coat. zontally or at right angles to the funicle (Figures 4.7B; 4.9E,J).
Ovules in which the micropyle is located 180 degrees or Here again, because embryo sac elongation occurs after curva-
directly opposite the chalaza are uncurved, and are called orthot- ture of the ovule primordium, the megagametophyte remains
ropous (from Greek ortho meaning straight and tropous mean- straight (Figure 4.9B,G).
ing a turning). In orthotropous ovules, the megagametophyte or In the two other types of curved ovules, the amphitropous
future space in which the embryo will grow is correspondingly and campylotropous (from Greek amphi- meaning around and
76 Kaplan’s Principles of Plant Morphology

Micropyle
Funicle
Inner integument

Micropyle Outer
integument
Nucellus
Exostome
Endostome
Synapsids
Raphe
bundle

Outer
integument
Raphe Inner Egg Central cell
integument
Nucellus
Embryo
sac
Chalaza

Antipodals

Chalaza

A. B.

FIGURE 4.5 A. Three-dimensional block diagram of a bitegmic, anatropous ovule with segments removed to show the internal structure and the major
regions. B. Median longisection of the bitegmic ovule of Lilium tigrinum showing the structure of the mature megagametophyte and its relationship to the
other components of the ovule. (A from Bouman, 1984; B from Esau, 1977.)

FIGURE 4.6 Scanning electron micrographs showing stages of ovule development in: A. Passiflora racemosa, showing the beginning of the anatropous
curvature and the initiation of the inner and outer integuments. B and D. Successive stages of ovules of Passiflora verspitilio showing curvature and mature
anatropous ovular structure respectively. C. Developmental stages of the ovules of Agrostemma gracile. (From Bouman, 1984.)
Plant Embryogenesis 77

the megagametophyte that contains it and the endosperm nutri-

tive tissue, embryos in campylotropous ovules will also be curved
(Figure 4.9H). It has been suggested that the development of a
curved embryo sac may be advantageous in developing a larger
(i.e., a longer) embryo in that same ovular space (Bouman, 1984).
As we will see in Chapter 5, embryo curvature can also occur
late in embryogenesis whether the embryo sac is curved or not.

Temporal Relationships between Embryos and

Their Nutritive Sources in Vascular Plants
The timing of development of the young sporophyte in relation to
the nutrient tissue that feeds it is significant in the development of
embryos in seed plants. Since the early nutrition of a new, diploid
plant is heterotrophic and dependent upon food sources available
from the parent plant, it is essential that the nutrient tissue be
generated prior to development of the embryo. In the case of pte-
ridophytes this is not a problem because extensive development
of gametophyte parenchyma occurs before the archegonia and
contained eggs are differentiated. Among seed plants, this is true
FIGURE 4.7 Diagrammatic longisectional views or the main types of in the ovules of gymnosperms, where there is an extensive devel-
ovules. The position and shape of the embryo sac (megagametophyte) is opment of the megagametophyte tissue before the archegonia—
shown by hatching. A. Orthotropous. B. Hemitropous. C. Anatropous. D. with their large egg cells—are differentiated and long before the
Campylotropous. E. Amphitropous. (From Foster and Gifford, 1974.) sperm carrying pollen reaches the archegonia. While it is true
that by the time the pollen lands on the nucellus of the ovule of
pine (Pinus), for example, the megasporocyte is just undergoing
campylos meaning a turn) (Figure 4.7D,E) growth curvature meiosis to form the tetrad of megaspores (Figure 2.44F), ger-
isn’t confined to the raphe region but also occurs in the chalaza mination and subsequent growth of the pollen tubes through the
(Figure 4.9D,E,I,J). In the campylotropous type that additional nucellus is so slow that by the time the tubes have reached the
curvature is not associated with curvature of the embryo sac archegonia, the megametophyte that will nourish the embryo is
(Figure 4.7D), whereas in the amphitropous type, megagame- fully developed (Figure 2.44G).
tophyte differentiation occurs during curvature and hence the The situation is altogether different in angiosperms. It will be
ovular cavity is bent to varying degrees (Figure 4.7E). Since recalled from Chapter 2 that female gametophyte or embryo sac
elongation of the young sporophyte is constrained by the shape of development in the flowering plants is extremely rudimentary.

Ch Ch
II

Nu

A. II
Nu

D.
ch
OI
R
B. OI
Nu
II
II

II mi
II
Nu F

C. E. F.

FIGURE 4.8 Median longitudinal sections of the stages of the development of an anatropous ovule in Nigella damascena, showing the growth curvature
and mode of initiation of the integuments. Ch, chalaza; F, funicle; II, inner integument; Mi, micropyle; Nu, nucellus; OI, outer integument. (From Bouman,
1978.)
78 Kaplan’s Principles of Plant Morphology

E
ES

Mi
I
F
A. F B. C. F D. Mi E.

Mi
E

Mi

Co
Hi H
Ed Hi Mi Hi Hi
Mi
F. G. Mi H. I. J.

FIGURE 4.9 Relationship of the developing embryo to the shape of the ovule. A–E. Early developmental stages in the following ovule types: A.
Orthotropous, B. Anatropous, C. Amphitropous, D. Campylotropous, and E. Hemitropous. In these diagrams the outline of the embryo sac is given as well
as the initial form of the early embryo. F–G. Same ovules but with mature, fully expanded embryos showing their shape in relation to ovule structure and
the nutritive tissue. Co, cotyledon; E, embryo; Ed, endosperm; ES, embryo sac; F, funicle; H, hypocotyl; Hi, hilum or scar of funicle; after seed is abscised;
Mi, micropyle. (From Goebel, 1933.)

In contrast to the hundreds of cells comprising fully developed and a corresponding ovule and seed development which is infi-
female gametophytes in gymnosperms, megagametophytes in nitely more rapid than that of gymnosperms.
ovules of angiosperms consist typically of only seven cells and Depending on the species, endosperm is either cellular from
eight nuclei (Figure 4.5B). At the micropylar pole are the two inception or initially free-nuclear followed by the insertion of
synergids and the egg cell with three antipodals at the chalazal walls to make it multicellular (Figure 2.39P–R). A vivid illustra-
pole (Figure 4.5B). The synergids play a role in pollen tube pen- tion of the difference in physical consistency between free-nuclear
etration of the embryo sac and sperm transfer. The antipodals
are not known to have any particular function and are assumed
to be sterile cell remnants of a more elaborated female gameto-
phyte. The large central cell, comprising the largest volume of
the gametophyte, is binucleate, and, along with the egg, also will
be fertilized (Figure 4.5B). The central cell forms the triploid
nutritive tissue, the endosperm.
Since fertilization of the diploid central cell occurs at the same
time as the egg, in contrast to the gymnosperms, the embryo’s
nutritive tissue in angiosperms originates at virtually the same
time as the embryo itself. Since development of the embryo is
dependent on the former, there has to be some time disjunction
between embryo and endosperm development during early devel-
opment of angiosperm seeds.
This lag time is depicted graphically in Figure 4.10 for
the development of the seed of the pea plant, Pisum sativum
(Fabaceae), where the relative volumes of endosperm, embryo,
and ovule as a whole are plotted against a series of ovule devel-
opmental stages (Marinos, 1970). It can be seen that up to stage
19, ovule and endosperm have comparable volumes. However,
the endosperm subsequently shows a relatively rapid expan-
sion to its full volume at stage 22, whereas the embryo shows
no expansion at all. However, past stage 22 the embryo enters
its log phase of development while the endosperm declines ulti-
mately to a ground level. The intersection of the embryo and
endosperm curves at stage 24 is indirect evidence of the utiliza-
tion of endosperm in embryo growth (Figure 4.10). Hence even
though angiosperm ovule development does not exhibit the more
conventional buildup of gametophyte nutritive tissue prior to FIGURE 4.10 Changes in volume of endosperm, embryo, and ovule in the
embryogenesis, the earlier and more rapid development of the developing seed of pea, Pisum sativum, plotted as a function of seed devel-
endosperm ultimately provides a substratum for embryo growth opmental stages. (From Marinos, 1970.)
Plant Embryogenesis 79

LE WE

Co
Co
WE
WE

FI F2 F2

A. B. LE C.

FIGURE 4.11 Structure and stages of germination of the seed of the coconut palm, Cocos nucifera, showing the differing types of endosperm and the
relationship of the developing embryo and seedling to those nutritive sources. A. Median longisection through a mature fruit showing the reduced embryo
(E) and walled (WE) versus liquid (LE) endosperm. F1 and F2 represent the fibrous and hard inner fruit wall layers respectively. B, C. The embryo’s shoot
has emerged from the seed and the cotyledon (Co), functioning as a nutrient absorbing haustorium, has gradually absorbed the liquid endosperm and filled
up its space in the ovule cavity. (From Troll, 1959.)

and cellular endosperm can be seen in the nature of endosperm of In Capsella, zygote elongation prior to the division into apical
the coconut palm, Cocos nucifera. Since wall formation begins at and basal cells is minimal (Figure 3.7B–D). By contrast, in
the periphery of the free-nuclear endosperm mass and proceeds Downingia (Campanulaceae), the zygote undergoes a signifi-
centripetally, there is a larger central portion that is free-nuclear cant elongation prior to its first division, becoming an extended,
while that at the periphery is cellular. The so-called “milk” or contorted tube (Figure 4.12A–D). When the first division in the
liquid of the coconut is the free-nuclear stage, whereas the so- Downingia zygote does finally occur, it is markedly unequal,
called “meat” is the cellular endosperm at the seed periphery producing a very small apical cell and a very elongated basal cell
(Figure 4.11A). At the time the coconut fruit falls from the tree, (Figure 4.12E).
the majority of the volume of the ovule consists of the central Characteristically, the earliest growth of the embryo is filamen-
mass of nuclear endosperm with a surrounding peripheral shell tous and has been called a proembryo. However, with the onset
of cellular endosperm (“meat”) (Figure 4.11A). At this stage the of terminal parenchyma formation by the initiation of three-
embryo is minuscule and barely evident at the micropylar end of dimensional growth in the apical cell and its derivatives, we have
the ovule (Figure 4.11A). When the young coconut plant ger- the delineation of the distal parenchyma as the embryo proper
minates, not only will the shoot system emerge, but the single and the proximal filament as the suspensor (Figure 4.13A).
cotyledon will enlarge as a haustorial organ, absorbing all of the Given that a major role of the so-called suspensor is to thrust
liquid endosperm and filling the ovular cavity where the “milk” the embryo into a central position in the endosperm or nutritive
previously existed (Figure 4.11B,C). Thus in later stages of seed- gametophyte tissue, a more accurate term would be to call it a
ling development, all that remains of the endosperm is the cellular pusher. The German term for suspensor, embryoträger (liter-
storage endosperm at the seed periphery (Figure 4.11C). The lat- ally, embryo carrier), also is more descriptive. During early
ter ultimately will be broken down and absorbed by the haustorial embryogeny the suspensor is the most rapidly developing region
cotyledon to supply additional nutrients to the young seedling. of the embryo, elongating quickly and carrying the embryo
proper deeper into the nutritive endosperm (Figure 4.14).
Evidence that suspensor length is correlated with the depth of
nutritive tissues can be seen from observations of embryogen-
A Description of Embryogenesis esis in some gymnosperms, especially conifers such as Pinus.
in Vascular Plants The ovules of conifers are long with an elongated megagameto-
Seed Plants phyte. The egg-bearing archegonia are borne at the micropylar
surface of the female gametophyte, a considerable distance from
Non-Monocot (“Dicot”) Angiosperms the central part of the gametophyte (Figure 4.15H). Following
and Gymnosperms fertilization, the zygote of Pinus undergoes a period of nuclear
division followed by wall insertion at the eight-nucleate stage
Embryogenesis in all flowering plants begins with the fer-
(Figure 4.15A,B). Subsequent cell division occurs in such a way
tilization of the egg cell at the micropylar pole of the ovule
as to form four superposed tiers of cells, each four cells in width
(Figure 4.5B). Here we focus on the non-monocots, as the single
(Figure 4.15C,D). Beginning at the apex of the proembryo, the
cotyledon of the monocot embryo makes this lineage compara-
tiers have been named the apical tier (A) the suspensor tier (S),
tively different from the remaining angiosperm lineages (here
the rosette tier (R) and the open tier (O) (Figure 4.15D,E). The
collectively referred to as “dicots”). In the time interval between
latter is called “open” because its protoplast is continuous with
fertilization and its first division, the axial nature of the dicot
the original cytoplasm of the egg cell bounded by the archego-
flowering plant embryo is expressed by the endoscopic elonga-
nial jacket (Figure 4.15H).
tion of the zygote parallel to the long axis of the gametophyte.
80 Kaplan’s Principles of Plant Morphology

50 µ

50 µ
A.

Z
Z

C.

B. D. E.

FIGURE 4.12 Early development of the zygote (Z) and cellular endosperm in Downingia pulchella, showing the significant elongation the zygote of this
species undergoes prior to the first transverse division. Two-celled proembryo stage showing the marked inequality of the first division. (From Kaplan,
1969.)

By a series of subsequent transverse divisions, the apical cell toward the micropyle can result in the crushing of the suspensor
gives rise to a succession of two embryonal tiers (e1 and e2 in (Figure 4.14E,F).
Figure 4.15E) and the body of the embryo proper. The two Turning now to the development of the embryo proper, a
embryonal tiers along with the suspensor tier undergo a tremen- good example is in the crucifer species Capsella bursa-pastoris
dous elongation functioning together as a suspensor unit which (Brassicaceae), a widespread weedy annual dicotyledonous flow-
literally thrusts the embryo proper out of the confines of the ering plant. Delimitation of the embryo proper from the subja-
archegonium and deep into the center of the megagametophyte cent suspensor in Capsella is marked by the initiation of true
tissue (Figure 4.15G,H). parenchyma in the apical cell (Figure 4.13A). The latter is first
In addition to embryo displacement, the suspensor in angio- expressed by the cell division plane occurring at right angles to
sperms also has been implicated in nutrient transport from the the transverse division plane that predominated in the initial fila-
micropylar end of the ovule to the embryo proper. Evidence for mentous growth (Figure 4.13A). Subsequent growth in volume
its transport role comes both from structural studies (Schulz and of this parenchymatous mass clearly delimits the embryo proper
Jensen, 1969; Simoncioli, 1974, and Yeung and Clutter, 1978) from the subjacent filamentous suspensor and has been called the
and from autoradiographic studies of the uptake of radioactively globular stage of embryo development (Figure 4.13B,C).
labeled 14-C-sucrose into developing bean pods in Phaseolus This so-called globular or spherical stage is very transitory
(Fabaceae) (Yeung, 1980). In the latter investigations it could in Capsella, however, and the distal pole of the embryo proper
be shown that in the stages of embryogeny preceding cotyledon soon flattens out and subsequently appears concave in median
enlargement, the suspensor is the preferential pathway for sugar longitudinal section as a result of a pair of lateral outgrowths
transport. Later, when the first leaves expand, the cotyledons (Figure 4.13D,E). The outgrowths are the primordia of the first
became the major locus of nutrient uptake. There also have been two leaves of the primary shoot, the so-called seed leaves or
suggestions of the role of the suspensor in synthesis and trans- cotyledons. In this embryo the two cotyledons arise simultane-
port of various growth regulators, especially gibberellic acid, ously, and their simultaneous origin is indicated by their equiva-
but evidence for this is equivocal and controversial at this time. lent length during their early development (Figure 4.13E–H). In
Once the suspensor has reached its full extent and the body of the later stages of development, the cotyledons of Capsella will grow
embryo enlarges, the suspensor atrophies and plays no further unequally in relation to embryo curvature within the curved
role in embryogeny. Elongation of the hypocotyl-root axis back embryo sac (Figure 4.13I,J).
Plant Embryogenesis 81

SA
Co Co
Co
Outgrowth of the two cotyledon primordia so dominates the
Ep
early growth of the embryo proper, that the latter assumes a
Su
RA
heart shape (Figure 4.13E,F). However, soon after the initial
oblique expansion of the cotyledons, the subjacent stem region,

SA
Su or what is called the hypocotyl-root axis (hypocotyl from Greek
A. Hg-R
B. hypo meaning below and cotyl referring to the cotyledons—i.e.,
Hg-R
the stem region below the point of insertion of the cotyledons)
C.
D.
itself begins to elongate and the embryo no longer appears heart
E.
F. RA shaped (Figure 4.13G,H). The reason the subjacent axial region
is referred to by the compound term hypocotyl-root is because
Su
at this early stage of embryogenesis, it is difficult to delimit a
G.
precise boundary between these two superposed but distinctive
zones. Only in the later phases of development is it possible to
determine just how much of this axial region becomes hypocotyl,
H. or the lowest internode of the shoot, and how much becomes pri-
EA mary root (Chapter 5).
EA
Not all dicot embryos develop a heart shape associated with
cotyledon initiation. Some, like that in Downingia, show sig-
nificant elongation of the hypocotyl-root axis prior to cotyledon
initiation (Figure 4.16A–D) rather than after as in Capsella. In
comparison with Capsella, the embryo of Downingia exhibits
precocious elongation in its hypocotyl-root region so that its
embryo has a cylindrical rather than globular shape prior to
Hg-R
cotyledon initiation (Figure 4.16A–D). When the cotyledons
finally do arise, they not only consume a smaller proportion of
the lateral parts of the distal pole of the embryo, but they also do
not become very elongated in the mature embryo at dormancy
(compare Figure 4.17A,B with Figure 4.13E–J).
Su At about the time the cotyledons become protuberant in
Capsella, the apical meristem of the primary root, or radicle,
RA first becomes evident. Root apex differentiation is expressed
I. RC most conspicuously by periclinal (insertion of dividing walls par-
allel to a given surface) subdivision of the primordial epidermis
or protoderm across the juncture of the embryo proper with the
J.
suspensor to form the primordial root cap (Figure 4.13D). As
the embryo continues to enlarge prior to dormancy, the root cap
FIGURE 4.13 Median longitudinal sections through the stages of embryo
development in Capsella bursa-pastoris, cut in the plane of insertion of thickens by additional periclinal divisions so that by the time of
the two cotyledons. Co, cotyledons; EA, epicotyl apex; EP, embryo proper; seed dormancy a conspicuous, several-layered cap is developed
Hy-R, hypocotyl-root axis; RA, root apex or radicle; RC, root cap; SA, shoot (Figure 4.13J). Thus the embryos of Capsella and virtually all
apex, SU; suspensor. (From Schaffner, 1906.)

Embryo proper

Suspensor

16
18
A. B. C. 20

Embryo proper

Suspensor
D. 21-22 E. 23 F. 24

FIGURE 4.14 Post-fertilization development of the ovule of pea, Pisum sativum, showing the relative rate of suspensor (white) versus embryo proper
(black) enlargement. Numbers represent arbitrary developmental stages. (From Marinos, 1970.)
82 Kaplan’s Principles of Plant Morphology

Archegonium

12-Celled
8-Celled
A. 4-nucleate proembryo B. C.
Rosette cells

O
R I

Open tier (O) H

Rosette tier (R) Primary

Suspensor tier (S) suspensor
First cells (S)
Apical tier (A)
embryonal
16-Celled tubes (e1) A
D. E.

S
Rosette cells
e1

e2
A
F.

S I

Su Nu
EP

e1

e2
H.

G. Embryo

FIGURE 4.15 Stages in early embryogenesis and suspensor development in conifer embryos. A–G. Embryogenesis in pine Pinus, showing organization
of tiers and their differential elongation as a suspensor. H. Median longisection through a fertilized ovule of Podocarpus totara, illustrating the degree of
penetration of the megagametophyte tissue by the suspensor. A, archegonium; EP, embryo proper; I, integument; M, megagametophyte; Nu, nucellus; Su,
suspensor. (A–G from Buchholz, 1931; H from Buchholz, 1941.)
Plant Embryogenesis 83

seed plants, including the gymnosperms, are distinctly bipolar; Because of early delimitation of the root cap, there has been
i.e., their shoot and root poles are diametrically opposed and they little disagreement as to how and when the primary root apex or
forecast the bipolarity or opposite directions of growth that shoot radicle has its origin during embryogeny. However, interpreta-
and root systems will take in their post-germination development tion of the time and mode of origin of the shoot apex has been
(Figures 1.7; 4.40A–C). more controversial. In the past, most workers described the cot-
During the early globular stages of embryogenesis, the cells yledons as arising from the distal pole of the globular embryo
of the embryo appear uniformly densely cytoplasmic and hence prior to the inception of the shoot apex. The shoot apex was then
characteristically embryonic (Figure 4.16A–C). However, with described as a dome that appeared between the cotyledons, after
the intercalation of the hypocotyl-root axis, the embryonic shoot the latter had grown in length (Figure 4.13I,J). Once differenti-
and root poles become progressively separated by an interven- ated, the late-appearing shoot apex is the source of subsequently
ing zone of increasing tissue differentiation and maturation initiated leaves.
(Figure 4.13G–J; 4.16C,D; 4.17A,B). Differential vacuolation More recent studies of embryogenesis have demonstrated,
and enlargement of cells in the hypocotyl-root axis progressively however, that the entire distal pole of the spherical embryo
delimits the peripheral cortical tissue from the central provascu- becomes differentiated and functions as the shoot apex prior
lar tissue or precursor of the conducting tissues (Figures 4.13F– to cotyledon initiation. Therefore the cotyledons, like all other
I; 4.16D; 4.17A). By contrast, cells of the apical meristems of the classes of appendages formed by the shoot, are also products of
primary shoot and root retain their densely cytoplasmic, embry- a shoot apical meristem.
onic character that will characterize those regions as long as they Evidence for the timing of differentiation of the shoot apex is
remain active as meristems (Figure 4.13H,I; 4.17A). based on the occurrence of a distinctive qualitative anatomical

IZ

MZ
MZ

RA

RA A. B.

MZ IZ MZ

IZ

MZ MZ

Hy-R

RA

RC

Su C. D.

FIGURE 4.16 Median longisections of the embryo proper of Downingia pulchella, illustrating the precocious elongation of the hypocotyl-root axis and the
timing of differentiation of the shoot apical meristem in terms of cytohistological zonation. Hy-R, hypocotyl-root axis; IZ, initial zone; MZ, morphogenetic
zone; RA, root apex; RC, root cap; Su, suspensor. (From Kaplan, 1969.)
84 Kaplan’s Principles of Plant Morphology

Co Co

IZ

IZ

Hy-R
Hy-R

Rc

RC
Su
A. B.
Su

FIGURE 4.17 Median longisections of late stages of embryogenesis in Downingia pulchella, showing in A the origin of the two cotyledons from the
morphogenetic zone of the shoot apex and B, the structure of the mature, dormant embryo with the deposition of protein body storage particles in its cells
and those of the surrounding endosperm storage tissue. Co, cotyledons; Hy-R, hypocotyl root axis; IZ, initial zone; RC, root cap; Su, suspensor. (From
Kaplan, 1969.)

pattern that all shoot apices exhibit regardless of the particular IZ

taxonomic group they are members of or the pattern of lineages
of cells that their meristems possess. Such a pattern has been MZ
MZ
termed a cytohistological zonation because it is expressed by
subtle differences in size, degree of vacuolation, and hence den-
sity of staining of the cytoplasm, as well as differing degrees
of size and chromosomal staining of the nuclei and nucleoli of
cells in the different regions of the shoot apex. For example, in
the median longitudinal section of the vegetative shoot apex of
the cactus flowering plant Echinocereus reichenbachii shown
in Figure 4.18, the cells at the summit of the apical dome are
slightly larger, less densely staining, and, in other plant groups,
have been shown to divide less frequently (Gifford and Corson,
1971) than the more densely cytoplasmic cells around the
periphery of the dome. These cells of the so-called Initial Zone
(Figure 4.18) are interpreted to be the apical initials or perpetu-
ally embryonic cells that are the ultimate and continuing source
of all cells of the shoot, including the more densely cytoplasmic
FIGURE 4.18 Median longisection of the shoot apical meristem of
cells of the Morphogenetic Zone on the meristem’s flank which
Echinocereus reichenbachii, showing the conspicuous cytohistological
is the site leaf and branch origin (Figure 4.19). Hagemann (1967) zonation comprising a more vacuolate initial zone (IZ) and more densely
has emphasized that this same type of meristem zonation can cytoplasmic eumeristematic morphogenesis zone (MZ) from which leaf pri-
be found in the shoot apices of ferns with a conspicuous apical mordia are initiated. (From Boke, 1951.)
Plant Embryogenesis 85

A. 400 µ

FIGURE 4.19 Diagrammatic representation of the zonation of the shoot

apex, showing the central initial zone (I) and peripheral zone of morphogen-
esis (M) where leaves and branches arise. (From Hagemann, 1967.)

cell and derivative cell lineage pattern (Figure 4.20B), those of

flowering plants with a more layered or tunica-corpus pattern
of cell lineages (Figure 4.20C), or even a gymnosperm whose
cell lineage pattern is more complex and difficult to characterize
(Figure 4.20A).
Such an apical meristem zonation can also be expressed to
400 µ
varying degrees at the distal pole of the globular embryo of B.
some species prior to the inception of the cotyledons and is the
marker of when the shoot apex has its origin during embryo-
genesis. For example, apical zonation is expressed in a spherical
embryo of Downingia by the larger, less chromatic nature of the
nuclei of the initial zone in contrast with the denser, more chro-
matic nature of nuclei in cells at the periphery (Figure 4.16B).
As its shoot apex broadens, just prior to cotyledon emergence,
this zonation becomes more conspicuous, with the more densely
cytoplasmic morphogenetic zone that the cotyledons will emerge
from, forming a pair of lateral shoulders bordering the initial
zone (Figure 4.16C,D). In fact, the morphogenetic zone repre-
sents a histological differentiation or prefiguration of the leaf pri-
mordium before it becomes an emergent, three-dimensional leaf
organ (Hagemann, 1960). Thus it becomes impossible to sepa-
rate apical meristem enlargement and structure from the lateral
organs it is going to form.
Since cotyledon primordia are large relative to the size of C. 400 µ
the meristem from which they originate, they consume a large
proportion of the meristem periphery, leaving only the initial FIGURE 4.20 Median longitudinal sections of the shoot apical meristems
zone between them as the source of meristem regeneration prior of A, the gymnosperm, Ginkgo biloba; B, the fern Adiantum edgeworthii;
to initiation of the next leaf pair (Figure 4.17A,B). Since the and C, the angiosperm Cheiranthus cheiri. In each case there is a different
next pair of leaves in such dicots will arise at right angles to cell lineage pattern but the same cytohistological zonation is superimposed
the plane of the cotyledons, expansion of the shoot apex to its them. Cells of the initial zone have stippled nuclei whereas those of the zone
of morphogenesis have black nuclei. (From Hagemann, 1967.)
next maximal size will also occur at right angles to the coty-
ledonary plane. For this reason, in median sections cut in the
plane of the two cotyledons, the subsequently enlarging shoot end of the pine embryo broadens and develops a cytohistologi-
apex will appear as a narrow dome between the first leaves cal zonation similar to but even more conspicuous than that we
(Figures 4.17B; 4.13H–J) whereas it actually has a greater have just described for the dicot Downingia (Figure 4.22C,D).
width at right angles to that plane. In Pinus, the initial zone of the embryonic apex becomes dis-
Even more striking evidence of the differentiation of the tinguished not only by the more vacuolate nature of its cells but
shoot apex before cotyledon initiation can be seen in the devel- also by its early projection as a conical tip (Figures 4.21D,E;
opment of the embryo in the gymnosperm, white pine, Pinus 4.22C,D). Emergence of the initial zone then delimits it from
strobus (Spurr, 1949). This species initiates on average nine the broad, shoulder-like morphogenetic zone around its perim-
cotyledons around the periphery of the distal pole of its embryo eter (Figures 4.21C–E; 4.22C,D). Like Downingia, the morpho-
(Figure 4.21, level 17). Prior to cotyledon inception, the distal genetic zone prefigures the sites of future cotyledon emergence
86 Kaplan’s Principles of Plant Morphology

Co

8 15 16
9 17
R R 10
R 11
12 IZ
R
13 Co
14

Hy-R
Su Su
Su

R
A. B. C. D. E. F.
Su

RC

G.

Su
8 9 10 11

15

12 13 14 16 17

FIGURE 4.21 A–G. Median longitudinal sections through successfully older embryos of white pine, Pinus strobus. 8–17, transections taken through the
embryos at the levels shown in parts D and E. Co, cotyledons; Hy-R, hypocotyl-root axis; IZ, initial zone; R, root; Rc, root cap; Su, suspensor. (From Spurr,
1949.)

in pine but instead of being restricted to two opposite loci as Monocotyledons

in a dicot embryo, in Pinus it forms a complete collar around
the initial zone with the nine cotyledons emerging along nine As their name suggests, monocotyledonous angiosperms typi-
radii (Figure 4.21, level 17). Once the cotyledons have enlarged, cally differ from their dicotyledonous counterparts in initiating
they surround the conical initial zone which will function in a single cotyledon as the first leaf of their shoots rather than a
subsequent leaf and stem initiation after embryo germination pair. The initiation of a single first leaf in monocots is related
(Figures 4.21F,G; 4.22E). to the phyllotaxis or pattern of leaf arrangement that shoots of
Like that of the dicotyledons, the embryo of Pinus is bipo- monocots exhibit in contrast to that of dicots. In the dicots, early
lar with the primary root apex or radicle located adjacent to the development of the shoot typically exhibits leaves arranged in
suspensor, exactly opposite the shoot apex (Figures 4.21C–G; pairs at a node. The inception of two cotyledons at the same time
4.22A–D). Also like flowering plants, root apex differentiation is the first expression of this opposite or whorled phyllotactic pat-
is expressed most markedly by the development of the root cap. tern (Chapter 7). Shoots of monocots, on the other hand, exhibit a
Cap development in the pine embryo, however, is much more single leaf per node during early shoot growth, and this likewise
extensive than that of dicots, and, at maturity, its radicle exhibits is foretold by the single cotyledon in their embryos.
a very thick, multilayered cap that is almost as deep as the hypo- Embryogenesis in monocots follows the general pattern we
cotyl-root axis is long (Figure 4.21G). Because the first root and have just described for dicots, however with some differences
shoot apices are so clearly defined in the embryo of Pinus, it can in organogenesis, especially of the shoot. For example, the grass
be demonstrated that the two primary meristems differentiate at Zea mays develops only a few-celled filament before the onset of
virtually the same time (Figure 4.22C), and that seems to be parenchyma formation from its distal cell tiers (Figure 4.24A).
true for the majority of the flowering plant embryos. The suspensor in Zea is thickened and multiseriate but its ultimate
Plant Embryogenesis 87

IZ

MZ
MZ
HS

RC

A. B. C.

IZ IZ

MZ
MZ

P
PO

D. E.

FIGURE 4.22 A–E. Details of median longisections of late developing embryos of white pine, Pinus strobus, showing stages of origin of the zonation of
the shoot apex and root apex. HS, hypocotyl shoot; IZ, initial zone; MZ, morphogenesis zone; PC, procambium or precursory vascular tissue; R, primary
root or radicle; RC, root cap. (From Spurr, 1949.)

delimitation from the body of the embryo proper is more a prod- the shoot is a slight lateral indentation between these two sec-
uct of the widening of the base of the body of the embryo proper, tors (arrow in Figure 4.24C). It is only by following subsequent
especially the base of the cotyledon than the contrast between development that one sees that the slight bulge below that notch
filamentous and parenchymatous growth (Figure 4.23A–C). expands laterally as a convex apical meristem which initiates the
The single cotyledon in Zea arises very early in embryogeny subsequent leaves of the shoot and comes to take a more vertical
and looks to comprise the entire distal end of the embryo; the orientation (Figures 4.23A–K; 4.24C–I).
only demarcation between the seemingly terminal cotyledon Following its delimitation from the shoot apex, the cotyledon
and the apical meristem that will continue the development of not only grows vertically in length, but also circumferentially
88 Kaplan’s Principles of Plant Morphology

shoot apex or is its terminality merely an extreme expression of

the size relationships of first leaf to its meristem and the subse-
quent direction of apical regeneration in a shoot system with a
Co
Co Co Co two-ranked, alternate phyllotaxis? In order to answer this ques-
SA tion, we have to adopt a comparative developmental perspective.
C
For example, in the embryo of another monocot, Ottelia
Su R1 alismoides (Hydrocharitaceae), the relationship between coty-
ledon initiation and distal pole of the embryo seems closer to
A. Su
R1 the more conventional relationship of leaf to shoot apex that we
Su
B. are familiar with. Proceeding from a globular stage, the single
Su cotyledon of Ottelia appears first as an asymmetric, oblique out-
C. growth from a lateral portion of the apical pole of the embryo
proper (Figure 4.25A). Associated with some growth in thick-
D.
ness, subsequent cotyledon elongation is predominantly erect
(Figure 4.25B,C). It is clear that in Ottelia, cotyledon initiation
c does not consume the entire distal pole of the embryo as it seems
l1 to in Zea but leaves a small lateral meristematic residue that
l2 continues to enlarge. This meristem will function as the shoot
apex of the epicotyl, initiating successive foliage leaves in a two-
ranked phyllotaxis. Ottelia is also of interest because the root
apex arises at the juncture of the suspensor before cotyledon ini-
F. E.
G. tiation just as it does in Capsella and Downingia.
An even more conventional expression of the relationship of
H. cotyledon to its parent shoot apex can be seen in a close relative
of Ottelia, Stratiotes aloides (Hydrocharitaceae), described by
Baude (1956). Even though the cotyledon of Stratiotes is also
large relative to the globular embryo stage it is initiated from, it is
clearly lateral in origin and leaves a conventionally convex apical
dome dominating the summit of the embryo (Figure 4.26A–E).
In fact, subsequent leaves of the epicotyl are likewise initi-
ated from the lower flanks of the domed shoot apex just as is
the cotyledon (Figure 4.26E). These two examples suggest that
the seeming terminality of the cotyledon in grasses and other
monocot embryos is merely a consequence of its size relative to
I. J. K.
the parent apical meristem and its site of inception at the virtual
summit of that shoot apex rather than at the meristem’s periphery.
FIGURE 4.23 A–K. Outline drawings of median longitudinal sections of
the stages of embryogenesis in corn. Zea mays. C, coleoptile; Co, cotyledon;
These conclusions are further supported by the study of cotyle-
11, 12, first leaf, second leaf; R1, first root; SA, shoot apex Su, suspensor. don initiation in dicotyledonous flowering plants which are truly
(From Randolph, 1936.) monocotyledonoid; i.e., they normally bear only a single cotyle-
don in their embryos rather than the conventional pair. Barbara
Haccius (1954; 1959; Haccius and Hartl-Baude, 1957) has dem-
around the shoot apex in the form of a sheath termed the cole- onstrated the occurrence of such “monocotyledonoid” dicots in a
optile (Figure 4.23D–H). We will have more to say about the wide range of species including Claytonia virginica (Portulaceae),
homology of the parts of the grass embryo when we discuss the Pinguicula vulgaris and P. alpina (Lentibulariaceae), Anemone
morphology of its germination in Chapter 5. appenina (Ranunculaceae), Cyclamen persicum (Primulaceae)
Another feature in which embryogenesis in Zea differs from as well as many members of the parsley family, Umbelliferae.
that of the dicots we have just described is the relatively late dif- For each species, Haccius has documented that their monocotylar
ferentiation of its first root. In contrast to Capsella, Downingia, condition is not the result of fusion of the two normal cotyledons
and Pinus, where the first root primordium differentiates before into one syncotylous appendage, but by the actual suppression of
the cotyledons arise, that in Zea arises after cotyledon initiation the other cotyledon.
(Figure 4.23B). Moreover, the first root arises deeply within When the stages of cotyledon initiation in these “monocoty-
stem tissue rather than superficially at the juncture of the sus- ledonoid” dicots are investigated, as one might predict they are
pensor (Figure 4.23B,C). Thus while seeming to have a bipolar remarkably similar to that in true monocotyledons. Figures 4.27
embryo organogenesis, root origin seems different in the grasses. and 4.28 illustrate such stages in embryos of Claytonia and
Despite a seeming similarity in their early embryogenesis in Anemone, showing that they are virtually identical to the stages
monocotyledonous angiosperms, we have a problem in organo- of initiation described for Ottelia, for example (Figure 4.25). In
genesis that we did not encounter in the other seed plant embryos the case of two species of Pinguicula, the truly lateral, appen-
we have described. Is the cotyledon of monocots really a ter- dicular nature of the single cotyledon is even more evident. Like
minal organ that does not arise as a lateral appendage from the Downingia, cotyledon initiation in Pinguicula is relatively late
Plant Embryogenesis 89

Co
Co

SA
SA

Su
Su
Su

A. B. C.

D.

E.

F. Co

Co SA

SA

SA

R1

Su
G. H. I.

FIGURE 4.24 A–C, G–I. Median longisections of the stages of cotyledon initiation and early development in the embryo of Zea mays. D–F. Transections
of shoot pole at time of cotyledon inception. Arrow in C, G, and H demarcates boundary between cotyledon and initial zone of the regenerated shoot apex.
Co, cotyledon; R1, first root primordium; SA, shoot apex; Su, suspensor. (From Randolph, 1936.)

from a more cylindrical than spherical embryo. Because of the monocotyly (development of a single cotyledon), and acotyly
smaller size of the cotyledon relative to its parent meristem, there (the complete suppression of cotyledon development).
is no doubt of its appendicular developmental origin like the sub- At concentration ranges of 600–1200 ppm Haccius was able to
sequently initiated leaves of the shoot (Figure 4.29). induce the majority of treated seeds to produce monocot embryos.
Haccius (1960) has also provided an interesting experimen- When these “monocotyledonoid” forms were examined develop-
tal confirmation of these interpretations of monocot cotyle- mentally, their modes of cotyledon initiation exhibited the same
don initiation, using Eranthis hiemalis of the buttercup family dominance and asymmetric growth of the single cotyledon from
Ranunculaceae. The normal seedling of E. hiemalis has a pair of the embryo as well as the subsequent lateral regeneration of the
equally developed cotyledons that are fused laterally into a tube shoot apex we have described for monocotyledonous plants.
(Chapter 5). By soaking young seeds of Eranthis in a range of However, when two cotyledons were initiated, whether they
concentrations of phenylboric acid, Haccius was able to induce a were equally (i.e., isocotylous) (Figure 4.30A,D) or unequally
range of alternative cotyledon developmental expressions, includ- developed (i.e., anisocotylous) (Figure 4.30B,C,E), they were
ing choricotyly (two separate but equally developed cotyledons), initiated symmetrically from the terminal part embryo and left
anisocotyly (development of separate but unequal cotyledons), a residue of the shoot apex between them (Figure 4.30A–C).
90 Kaplan’s Principles of Plant Morphology

co

co

sa

sa

sa
co

l
b s

b
A. B. C.

FIGURE 4.25 A, B. Median longisections of stages in single cotyledon initiation in Ottelia alismoides. C. Transection. co, cotyledon; sa, shoot apex.
(From Haccius, 1952.)

SA

Co

B. Co

su
A.

SA

SA L1
SA SA Co L1
Co L1 L1 Co

C. D. E. F.

FIGURE 4.26 A–F. Median longisections of the embryo of Stratiotes aloides, showing the truly lateral mode of cotyledon initiation in relation to marked
axial extension. Co, cotyledon; L1, first foliage leaf; SA, shoot apex, Su, suspensor. (From Baude, 1956.)
Plant Embryogenesis 91

Co
Co

SA D. X

225 ×
IZ
Co IZ (SA)

E.

B.

35 ×

A. C.

F.

Co
Co
IZ
MZ
SA 17 ×
H.
RC

SA

175 ×
RC

G. I.

FIGURE 4.27 A–I. Median longisections of the stages of single cotyledon initiation in the dicotyledonous Claytonia virginica. A–C. Details of inception.
D–F. Outline drawings of whole embryos. G, I. Anatomical details of apical meristem regeneration of an advanced stage shown in outline drawing in part
H. Co, cotyledon; IZ, initial zone; MZ, morphogenetic zone; RC, root cap; SA, shoot apex. (From Haccius, 1954.)

Thus by experimental manipulation of embryo development in the inception, the more lateral apical meristem regeneration will
a conventional dicotyledonous plant, Haccius was able to show appear. The more lateral the site of leaf inception, the more ver-
that the relationship between cotyledon initiation and shoot apex tical subsequent expansion and regeneration of the shoot apex
depends upon whether one or two appendages are initiated rather will be. We will see these varying relationships between locus
than a fundamentally different process during embryogenesis. of leaf initiation and shoot apex growth expressed in the subse-
The apparent terminality of cotyledon inception we noted in Zea quent studies of a variety of shoot systems. Their description and
is only one extreme of the range of expression of the relation- analysis will demonstrate that the process of cotyledon initiation
ship between the locus of leaf initiation and how much of the does not differ significantly from these overall patterns of shoot
apical meristem is utilized in that initiation. The more summital development.
92 Kaplan’s Principles of Plant Morphology

Co SA Co
Co
Co Co SA
SA

SA Co
Co SA

B. D. A. B. C.
S
Co SA
200× S

A. D. C.

E.
G.
F.
Co
Co
Co Co
Rh
SA SA
20× Co
S
E.

SA
20×
90×
F. G.

H. I. J.
FIGURE 4.28 Median longisections of stages of embryogenesis in the
monocotylar dicotyledon Anemone apennina, showing the initiation of the
single cotyledon (A–D) and its subsequent vertical growth and enlargement FIGURE 4.29 Median longisections of single cotyledon initiation in the
(E–G). Co, cotyledon; SA, shoot apex. (From Haccius and Fischer, 1959.) dicotyledons Pinguicula alpina (A–D) and P. vulgaris (F–J). Co, cotyledon;
SA, shoot apex. (From Haccius and Hartl-Baude, 1957.)

Co
Co1

Co2

SA

SA Co2

A. B. C.

Co Co1 Co1

L1

L1

Co2

D. E. F. G.

FIGURE 4.30 Median longisections of young (A–C) and older (D–G) embryos of Eranthis hiemalis which have been treated with phenylboric acid to
induce the following types of variants. Choricotyly (A and D), Anisocotyly (B, C, E), Monocotyly (F), and Acotyly (G). (From Haccius, 1960.)
Plant Embryogenesis 93

Lycophytes and Pteridophytes a

a a
s
Because the early-diverging vascular plants exhibit a variety of ac ac
i E.
organographic relationships expressed during their embryogen- A.
f
esis and therefore are useful in our assessment of the relationship
of embryogenesis to plant architecture here and in later sections C.
a a
of the book, we want to describe the course of embryo develop-
s
ment in these lineages at this point. Since the process is markedly
different in representatives of each of these classes, we will have p
f

to take a more descriptive approach for each group. However, B.

F. D.
once we have characterized embryogenesis of the Lycophytes
and Pteridophytes as a whole, we will combine that data with
that of seed plants in order to deduce some general principles of
embryogenesis.

Lycophytes
Lycophyta
g
Most members of the Lycophytes have an endoscopic embryo polar- Foot
Foot
H. G.
ity but differ in the extent and mode of development of a suspensor
in those early stages. For example, in Huperzia selago, parenchyma a

formation has its onset in the apical cell immediately after the first am
transverse division (Figure 4.33A,B). The basal cell functions as
the suspensor but does not supply more than an initial thrust of
the sporophyte into subjacent gametophyte because it enlarges to
only a limited extent (Figure 4.33B–D). The majority of expan- g
I.
sion of the embryo into the gametophyte is a result of growth of
the embryo proper rather than in the suspensor (Figure 4.33C,D). a

Thus at later stages of development the suspensor of H. selago is

evident only as a single, enlarged cell at the basal pole of embryo
(Figure 4.33E). Perhaps in correlation with the flattened, discoidal
shape of the parent gametophyte, subsequent enlargement of the
embryo proper is horizontal and curvature of the shoot pole means J.
a
that it ultimately emerges from the lateral rather than the ventral
surface of the gametophyte (Figure 4.33D,E).
One of the earliest signs of differentiation in the embryo of
H. selago is the significant enlargement of cells at the basal
(i.e., lateral) part of the embryo proper adjacent to the suspen-
sor. These cells comprise the future foot region, which early in
development constitutes more than half of total embryo length
g
(Figure 4.33D). The smaller-celled, more embryonic tissues K. L.
represent the future shoot pole, where, after a period of further
elongation, the first leaf is initiated from the well-defined shoot FIGURE 4.31 Median longisections of stages of embryogenesis in
apex (Figure 4.33D,E). Characteristically, the first root in H. members of class Psilopsida. A–H. Tmesipteris tannensis. I–L. Psilotum
selago arises laterally and exogenously (i.e., externally) at a slight triquetrum. Both species are exoscopic and exhibit neither leaf nor root
angle with the shoot apex, and at the point of curvature between development at these stages. a, archegonium; ac, apical cell; am, apical meri-
the shoot and foot (Figure 4.33E), like that of Equisetum (see stem; g, gametophyte. Arrows in D and G represent position of shoot apex
prior to cessation of growth with the inception of lateral branching. (A–H
below), the embryo of Huperzia is unipolar.
from Holloway, 1921; I–L from Holloway, 1939.)
Embryogeny in the related heterosporous clubmoss Selaginella
is similar to that in Huperzia but shows some features that
are unique and worthy of comparative note. Like Lycopodium into the megagametophyte nutritive tissue (Figure 4.34B,C;
embryo polarity in Selaginella is endoscopic. However, follow- I–K). Thus it is not a basal cell–originated suspensor that plays
ing the initial division of the zygote in S. poulteri, S. kraussi- the role of embryo embedment but rather the protoplasmic cavity
ana, and S. galeottei, the basal cell in turn is walled off from of the archegonium. In fact, what is traditionally labeled as the
an enucleate portion of the cytoplasm in the venter of the suspensor proper in these species of Selaginella is only a few-
archegonium (Figure 4.34A,B,H,I). It is the latter archego- celled structure like that in Huperzia which does not contribute
nial cytoplasm and surrounding wall, called the “embryo tube” significantly to embryo displacement at all (Figure 4.34C,G,L);
(embryoschlauch in German) that undergoes a tremendous and a single suspensor cell is barely evident in the older embryo of S.
tortuous elongation, thrusting the few-celled proembryo deep galeotti (Figure 4.34L).
94 Kaplan’s Principles of Plant Morphology

a A

C.

A. B.

D. E. F.

First leaf sheath

Shoot apex
SA
Leaf

G.
Gametophyte

SA

A
ls
ls

Root SA
ls
K. Foot ls

r1
RE

H. I. f

J. r1

FIGURE 4.32 Stages in embryogenesis in the genus Equisetum. A–G. E. debile. C, H–J. E. arvense. A, archegonium; F, foot; ls, leaf sheath; rl, first root;
SA, shoot apex (A, B, D–J from Campbel1, 1928; K from Smith, 1955; all the rest from Sadebeck, 1878.)
Plant Embryogenesis 95

su su
su

A. e B.

C. SA

SA
L1
a
a

su
su

SA
R1

G
D. E. F
F

FIGURE 4.33 Embryogenesis in Huperzia (Lycopodiales). A. First division of the zygote of H. phlegmaria. B–E. H. selago. Gametophyte tissue shaded;
embryo unshaded. a, archegonium; F, foot; G, gametophyte; L1, first leaf; R1, first root; S, shoot pole; SA, shoot apex; Su, suspensor. (A from Treub, 1886;
B–E from Bruchmann, 1910.)

Following its initial vertical displacement, the apical cell the oppositely situated foot toward the center of the gametophyte
undergoes the typical parenchyma formation in the origin of the (Figure 4.35L). Furthermore, the orientation of the first division
embryo proper (Figure 4.34C–F). Interestingly, at some stage in of the zygote can be variable with reference to the long axis of
their early development, the body of the embryo of Selaginella the archegonium. It has been reported to be either at right angles
undergoes a curvature so that its principal direction of elonga- or parallel to the archegonium (Figure 4.35B,D).
tion is horizontal within the megagametophyte or at right angles Without suspensor differentiation, the zygote of Isoetes goes
to the long axis of the original archegonium (Figure 4.34C,G). directly to the formation of a parenchyma (Figure 4.35A–F).
Longitudinal growth of the embryo proper is then bidirectional Organogenesis occurs so early in its development that there is
from the point of insertion of the suspensor (Figure 4.34F,G). no significant axial extension prior to the initiation of the first
Growth to one side of the suspensor becomes enlarged as the organ components, leaf, root, and foot. Precocious outgrowth of
suctorial foot whereas that to the other develops as the shoot the first leaf and the first root opposite it imparts to the early
pole consisting of the apical meristem and its most recently embryo of Isoetes the shape of an asymmetric, slightly concave
initiated leaves (Figure 4.34F,G). Like Huperzia, the first root cup, with the leaf forming the higher rim of that cup and the root
is initiated exogenously and at varying angles from the young primordium the other, lower side (Figure 4.35H,I). In subse-
stem region and from either the dorsal or ventral stem surfaces quent stages the basal foot swells up and the first leaf expands in
(Figure 4.34G). a predominantly lateral direction (Figure 4.35J). The first root,
Embryogeny in the heterosporous Isoetes differs significantly which is recognizable as a bulge opposite the leaf, is defined
from what we have described for all other Lycophytes. Not only qualitatively by the cell lineages of its cap and is exogenous in
is there no development or even sign of a suspensor but for all origin (Figure 4.35K). In its earliest stages at least, the embryo
intents and purposes embryo polarity ultimately seems exoscopic of Isoetes appears horizontally broadened rather than vertically
with the shoot oriented toward the neck of the archegonium and extended (Figure 4.35L).
96 Kaplan’s Principles of Plant Morphology

a a
a a

g
g

A. B. su

g
e
C.

SA su
F
su L2

SA
su su
L1

D. E. F. G.

a
a R1
a
a
es
es

H.
e
e
I.
g
su K.

F
J. SA

L. L1

FIGURE 4.34 Embryogenesis in Selaginella. A–G. S. poulteri. H–L. S. galeotti. Shaded tissue gametophyte, unshaded sporophytic embryo. Note signifi-
cant displacement of embryo toward center of megagametophyte tissue by elongation of embryo tube. a, archegonium; E, embryo proper; ES, embryo tube;
F, foot; G, gametophyte; L1, L2, leaves in order of inception; R1, first root; SA, shoot apex; SU, suspensor. (A–C, H–K from Bruchmann, 1912.)

An important question is, when in embryogenesis does the Isoetes has been considered to originate after the first leaf and
shoot apex in Isoetes arise? Like the condition described in root have been defined and in the space between them (Paolillo,
monocotyledonous angiosperms, at first glance it may look 1963) (Figure 4.35K). However, if one views the early paren-
like the first leaf is really a terminal organ differentiated from chyma mass formed in Isoetes as the equivalent of the apical
the spherical embryo stage without reference to the shoot apex meristem, then, like the cotyledon in the monocots, the first leaf
(Figure 4.35H). In fact, like the monocots, the shoot apex of of Isoetes also originates in a semi-lateral, summital position
Plant Embryogenesis 97

a
an

A. B. C.

an an an
D. E. F.

L1

SA L1
L1
lig
SA lig
SA
R1
R1

an
an
an
F F

G. H. F I.

L2
SA L2 lig
L1 SA an
g
R2 R1 L1
R1
F
R1
g

F
J. F K. L.

FIGURE 4.35 Stages in embryo development in Isoetes. A–C. Zygote and early parenchyma formation in I. echinospora. D–L. Stages of parenchymatiza-
tion and early organogenesis including leaf initiation (G, H) and root inception (I, J) in I. lithophila. L. Orientation of embryo in mature megaspore. Shaded
tissue gametophyte. an, archegonial neck; F, foot; Lig, ligule; L1, leaf one; L2, leaf two; R1, root one; R2, root two; SA, shoot apex. (A–C from Campbell,
1940; D–L from La Motte, 1935.)

(Figure 4.35G,H). Like all the leaves of its shoot, the first leaf shoot apex (Figure 4.35H,I). The first root then arises opposite
of Isoetes initiates a glandular epidermal outgrowth called a lig- and slightly proximal to the leaf, leaving a small sector of cells
ule from its adaxial (ad from Greek meaning toward and axial between them representing the initial zone that will regenerate
meaning stem, i.e. the side adjacent to the stem) surface. The the shoot apex to its maximal size prior to the inception of leaf 2
ligule arises very early at the base of the first leaf and demar- (Figure 4.35J–K).
cates the boundary between the leaf and the remains of the
98 Kaplan’s Principles of Plant Morphology

100 µm
SA
SA L1 R1

E.
A. L1
SA
F E. R1 R1 L1 R1
L1
D. B.

F
SA

R1
L1
F.
SA

R1

G. L1 50 µm

FIGURE 4.36 Embryogenesis in ferns. A–E. Hypolepis repens, showing early stages of parenchyma formation and first signs of differentiation of the shoot
pole, root, and foot. F, G. Later stages in Pityogramme calomelanos showing enlargement or first leaf and further definition of the shoot apex as wel1 as
elongation of the first root. F, root; L1, leaf one; R1 root one; SA, shoot apex. (From Hagemann, 1982.)

Pteridopytes the case of Psilotum and Tmesipteris where there is no root for-
mation and the shoot does not initiate leaves until considerably
Psilotopsida later in development, the only signs of embryonic differentiation
Members of this Pteridophyte lineage have embryos with an exo- following the development of an axial parenchyma is the delin-
scopic polarity that do not develop a suspensor. Hence they do eation of the basal foot and the apical shoot pole (Figure 4.31).
not show an initial filamentous phase followed by parenchyma The foot becomes evident by the cellular processes that protrude
formation. Instead, true parenchyma formation occurs right from into the tissues of the parent gametophyte and are assumed to
inception and the axial polarity of the developing embryo occurs be the sites of nutrient uptake (Figure 4.31D,H). The shoot at
at varying times later in embryogeny (Figure 4.31A–E,I–K). In the opposite pole is expressed by the differentiation of an apical

A. B. C. D.

FIGURE 4.37 Leaf series in Cyclamen persicum. A. Cotyledon. B. Leaf 3. C. Leaf 5. D. Leaf 7. (From Hagemann, 1959.)
Plant Embryogenesis 99

cell lineage configuration characteristic of the shoot apices of the tilting that we see in shoots with a two-ranked or distichous leaf
later development of these plants (Figure 4.31D,L). arrangement (see Chapter 7). At the time that the first leaf grows
The shoot pole of the embryo of Tmesipteris tannensis branches out, the first root also elongates and exhibits a well-defined cap
during its emergence from the neck of the archegonium. In this and tetrahedral apical cell just beneath the cap (Figure 4.36F,G).
process the summit of the shoot develops into a parenchymatous Like the other Pteridophytes we have described, the first root is
mass and two branch apices are differentiated slightly below and not situated directly opposite the shoot pole but emerges at an
lateral to it (Figure 4.31D). Following further elongation of the angle (Figure 4.36G). The angularity of first root outgrowth can
sporophyte out of the confines of the archegonium and gameto- be seen in the curvature of the vascular strand connecting root
phyte, these two lateral branch primordia grow out horizontally and shoot (Figures 4.36G; 4.4F). Thus the embryos of ferns are
while the distal pole of the embryo ceases growth as a parenchy- also unipolar in contrast to the bipolarity of those of seed plants.
matic pad (Figure 4.31G).

Sphenopsida Principles of Embryogenesis

Having just surveyed in some detail embryogenesis in a range of
There is little detailed information on exoscopic embryo devel-
vascular plants, what general morphological deductions can we
opment in the horsetail genus Equisetum. What is available also
draw about the process that are common to this group regardless
indicates a complete lack of any filamentous development and
of their taxonomic affinities?
the direct formation of a parenchymatous sphere which sub-
Proceeding from the fertilized zygote, the most common devel-
sequently shows an axial polarity with the earliest definition
opmental event is the formation of a true parenchyma mass out
of organ regions (Figure 4.32A–C). At a very early globular
of which the major organ components, root and shoot, become
stage, differentiation of the shoot and first root is expressed by
molded. Parenchyma formation may be preceded by a period of
the delineation of the wedge-shaped apical cells of their future
filamentous growth, but if it is, the filament serves as the sus-
meristems (Figure 4.32D–G). The first root apex is not oriented
pensor whose principal role early in embryogenesis seems to be
directly opposite the shoot pole but at a more lateral, basal site,
the displacement of the body of the embryo proper into a rela-
whereas the nutrient absorbing foot is also basal and lateral but
tively central position in the surrounding nutritive tissue (either
on the side opposite the first root (Figure 4.32G,I). Hence in
gametophytic or endospermic depending upon the group). Based
contrast to the Psilotopsida, where foot development encom-
on contemporary studies of suspensor ultrastructure and func-
passes the entire basal pole of the embryo, that in Equisetum
tion it also can play a role in nutrient transport, but this has not
involves only a lateral portion of it. Evidence of the activity of the
been evaluated in a range of species, especially Lycophytes and
distal pole as a shoot apex is the early formation of the first leaf
Pteridophytes where it can be well-developed (e.g. Selaginella)
whorl from its lateral derivatives (Figure 4.32I,J). Subsequent
and can even be associated with gametophyte tissue degradation
development of the horsetail embryo out of the archegonium
(Figure 4.34K).
shows a more obvious expression of these organographic rela-
Suspensor length seems to be correlated with the depth of the
tionships (Figure 4.32K).
nutritive tissue, and this correlation supports its role in embryo
displacement. In those species that have exoscopic polarity and
where the principal growth of the embryo is away from the nutri-
Pteridopsida
ent source rather than into it, no suspensor is developed.
Interestingly, embryo development in leptosporangiate ferns The extent of suspensor elongation does not seem to depend
exhibits certain parallels to what we have just described for upon cell division per se nor how many cellular subunits it pos-
Isoetes in division Lycophyta. Like the latter, ferns develop no sesses; major displacements can occur whether it consists princi-
suspensor during embryogeny. The zygote becomes cleaved pally of one cell (Selaginella), a few cells (Pinus), or many cells
directly into a multicellular parenchyma with a transverse or (Downingia and Capsella). It simply reinforces the lack of corre-
prone polarity (Figure 4.36A,B). The tissue on the dorsal side lation between cell partitioning and morphogenesis that we have
(i.e., toward the venter side of the archegonium adjacent to the noted in Chapter 3.
parenchyma of the parent gametophyte) of an early globular The same may be said for development of the embryo proper;
embryo is the earliest to differentiate into vacuolating enlarg- there does not seem to be a precise correlation between the ori-
ing cells of the suctorial foot (Figure 4.36B–F). At about the entation of cell lineages and cell fates and the differentiation of
same time as the foot differentiates, one sees the earliest defini- the major organ components. Only where there is an initial fila-
tion of the wedge-shaped initial cells of the first leaf and root (L mentous growth to produce a suspensor which exhibits a devel-
and R, Figure 4.36B,C). The drawings that have been published opmental fate separate and reasonably predictable from that of
suggest that leaf and root apical initial cells become expressed the embryo proper does developmental fate at the cellular level
before that of the shoot apex (Figure 4.36B). However, by the seem to have any consistency, and therefore meaning. It suggests
time the leaf primordium actually protrudes slightly, the shoot that, in the past, too much attention was devoted to deducing cell
apical initial cell can be discerned (Figure 4.36C). fate maps at the expense of the more general aspects of embryo
With subsequent vertical growth and slight adaxial curva- organogenesis and development.
ture, elongation of the first leaf is associated with the shoot apex One of the principal areas where there has been no consistency
being drawn up along with it and appearing canted at an angle of evaluation or interpretation has been the question as to when
(Figure 4.36E–G). Thus it shows the same type of alternate the shoot apex arises during embryo development and whether
100 Kaplan’s Principles of Plant Morphology

the first leaf initiated by the shoot pole of the embryo arises from difference in cotyledon function, the greater the difference in
an apical meristem. Part of the problem is because most plant morphology and vice versa. Given that the embryos of some seed
morphologist’s experience in dealing with shoot apical meristem plants can have first leaves that are functionally distinctive from
structure and activity comes from the study of well-developed the later-formed appendages, it seems best to reserve the term
vegetative shoot tips where the limits of the apical dome are cotyledon for the first leaf/leaf pair of seed plants, with the
defined by the leaf products that surround it. Interpretations are understanding that there can be differing degrees of distinction
more tentative when dealing with the embryo before any leaves in various species.
have originated. For these reasons shoot apex origin has tended Some evidence that the distinctive characteristics of cotyle-
to have been described as occurring at some time after the incep- dons are linked to their position as the first leaves of the shoot
tion of the first leaf or leaves, because the latter provide the afore- can be seen in the experimental work by Haccius (1960) cited
mentioned delimitation of the meristem that most investigators above. In her experimental suppression of one of the two cotyle-
are used to. dons to produce monocotyly with phenylboric acid treatments in
Since the distal or future shoot pole of the embryo has none of Eranthis hiemalis, Haccius also reported the induction of a cer-
the delimiting features of the older shoot, it has been necessary tain number of “acotylar” embryos where both cotyledons had
to look for qualitative expressions of apical meristem definition been suppressed (Figure 4.30G). In these instances, the subse-
before the first leaves have originated. In some species it has been quent leaves did not develop as cotyledons, but instead retained
possible to show that the cytohistological zonation of the vegetative their own distinctive foliage leaf characteristics that they exhibit
apex is manifest before the first leaves originate. Whether this is a in the untreated condition. Thus it would seem that in seed plants
widespread phenomenon is difficult to say, because at this time so that exhibit a morphological difference between cotyledons and
few investigators have seriously looked at this question. Looking later-formed leaves, that the characteristics of cotyledons are
from a broad perspective, as we shall see subsequently, the prin- products of their unique position in the shoot and is another rea-
cipal function of the shoot apex over the span of its existence is son for restricting use of the term cotyledon to the seed plants.
leaf initiation. Therefore we can say conceptually that any leaf
that arises is initiated from an apical meristem. The distal pole
of every embryo corresponds to the shoot apical meristem. The
fact that the first leaf may have varying geometric relationships The Relationship between Embryo Morphology
to that shoot apex, including even the seemingly terminal position
and the Subsequent Architecture of the Plant
of the first leaf in monocotyledonous flowering plants, does not
negate the meristem’s fundamental role in leaf initiation. When Having stated at the beginning of this chapter that the concept of
seen from this broader, more general perspective, the first leaves an embryo is impossible to define in plants because their develop-
in embryos of early diverging plant lineages, such as those in ment is a continuum from the zygote until the death of the whole
Isoetes (Lycophytes) and leptosporangiate ferns (Pteridophytes), plant, one could predict that features of the overall organography
do not seem any different in their origin than those of seed plant or architecture of the embryo would foretell the morphological
embryos, with which we are more familiar. relationships which one observes in the later, more mature plant.
Finally, there is the question of whether the first leaves ini- In fact, there are striking correlations between these phases of
tiated by the shoot apices of vascular plant embryos, whether development but rarely have they been emphasized.
spore-bearing or seed plants, should be called cotyledons. One of the most marked expressions of this connection is the
Traditionally the term cotyledon has been applied to the first relationship of root-shoot architecture in the embryo and mature
leaf or leaf pair initiated by the sporophytic shoot apex of seed plant. As we have noted in our descriptions above, the embryos
plants while the embryo is in the seed. If it has been applied to of most seed plants are bipolar; that is, the root apex is oriented
the first leaf or leaves in spore-bearing plants, it has been based 180 degrees from or directly opposite the shoot pole. When the
strictly on the equivalence of position rather than some distinc- young plant germinates, the root pole grows positively geotropi-
tive qualitative features. cally downward into the soil, forming a spatially separate root
In the case of seed plant embryos, not only are the first leaves system (primary root or tap root and its branches). By contrast,
characterized by their position, but they also can have qualitative the shoot pole exhibits a negatively geotropic response, growing
features that distinguish them from the leaves that follow. Some away from the earth and into the air (Figures 1.7; 4.38A–C).
of these distinctive features undoubtedly relate to their different As we have shown above, the plant bodies of spore-bearing
roles in nutrient storage and/or nutrient uptake as opposed to the plants differ significantly from those of seed plants. Instead of
purely assimilatory function of the subsequent leaves (Chapter developing a diametrically opposed, spatially-separate root sys-
5). These are the principal reasons they have been called cotyle- tem, Lycophytes and Pteridophytes initiate their roots strictly
dons or seed leaves. In the case of spore-bearing vascular plants, from the stem portion of the shoot (Figure 4.38D,F). The uni-
where there is no dormancy phase and where none of their leaves polar morphology of these embryos can be interpreted as the
function in either nutrient absorption or storage, changes in leaf earliest expression of this architectural difference. The fact that
form are not as abrupt as the changes between cotyledons and the first root typically grows out at some angle from the embry-
foliage leaves can be in some seed plants. On the other hand, onic axis suggests that it is a lateral product of the embryonic
there also are numerous examples of seed plants, especially stem (Figure 4.39). In fact, it expresses a pattern that will
those where the cotyledons are not storage organs, where mature continue to be exhibited in the subsequent growth of the plant
cotyledon structure is similar to that of subsequent leaves (e.g., (Figure 4.38E,F). A prime example of this type of architecture
Cyclamen persicum; Figure 4.37). Presumably the greater the can be seen in the embryo of Isoetes where the first root grows out
Plant Embryogenesis 101

Co Co Co Co
Hy

Co Co
Hy R
Hy
R L3 L4
B.
C. L2
L1
R3 R1 R2
R5 R4
D.

L3 L2
R L4

A.

L1

R3
F
A
L1 L1 R2

R1

R1 T
E. A F.

FIGURE 4.38 Comparison of shoot and root relations between allorrhizic and homorrhizic plants and their embryos. A. Idealized dicotyledonous plant
exhibiting allorhizy with spatially separated shoot and root systems developing from a bipolar embryo (B, C). D. Model of a fern exhibiting homorrhizy
where roots are strictly shoot-borne and initiated strictly from the stem region of the shoot system. E. Unipolar pteridophytic embryo in genus Equisetum,
characteristic of homorrhizic species. F. Homorrhizic relationship exhibited by a young plant of the fern Ceratopteris thalictroides. A-A, long axis of plant;
A, stem or axis; Co, cotyledon; F, foot; Hy, hypocotyl; L1, L2, L3 etc., leaves in their succession of origin; R, primary root or radicle; R1, R2, R3, etc., roots
in their sequence of origin. (From Troll, 1959.)

sa
l
l
sa
sa

s sa f
r
G.
f r
s
r E.
r
f
A. C. s

sa r
l l
sa
l

sa
s r

s f

F.
r
f
f
B. D.

FIGURE 4.39 Relationships of shoot to root in homorrhizic embryos of various lower vascular plants. A. Selaginella spinulosa. B. S. martensii.
C. Lycopodium selago. D. L. clavatum. E. L. cernuum. F. Isoetes. G. Equisetum. f, foot; l, leaf; r, root; s, suspensor; sa, shoot apex. (From Bower, 1935.)
102 Kaplan’s Principles of Plant Morphology

exactly opposite the leaf (Figure 4.35K). On this interpretation, hardly any axial extension foretelling its ultimate rosette habit.
the very condensed short axis of the Isoetes embryo would cor- Moreover, it is the leaf and root components that are the most
respond to a stem and the first root an outgrowth from that stem. elaborated organs, expressing at this early stage the dominance
The great German morphologist Karl Von Goebel was the first of these units in the plant’s later morphology (Figure 4.35J,K).
to note this correlation between plant architecture and embryo Embryos of Selaginella, Huperzia, and Lycopodium, on the
organography. Goebel coined the term allorrhizy (from the Greek other hand, are characterized by a marked axiality as a preco-
allo meaning other and rhizy meaning rooting) to refer to the first cious expression of the stem elongation that their later shoots will
condition in most seed plants where roots are initiated exclusively express (Figures 4.33, 4.34). In fact, looking at the relative timing
from a spatially separated root system and where the embryos are between leaf initiation and stem elongation, the embryo of Isoetes
bipolar. He used the term homorrhizy (from the Greek homo shows an early initiation of its leaf and a marked delay in any stem
meaning same and rhizy meaning rooting) to refer to the condition elongation whereas the other two genera of Lycophytes show the
in unipolar pteridophyte embryo where a tap root is not developed, converse (compare Figure 4.35K with Figure 4.33E and 4.34G).
and all roots must therefore arise from the same source (hence Like Isoetes, the embryos of the leptosporangiate ferns
the term homorrhizic), namely the stem. The earliest expression (Pteridopsida) show a similar emphasis on early leaf and
of the homorrhizic condition is the unipolarity of the Pteridophyte root growth at the expense of internodal extension (compare
embryo (Figure 4.39). Interestingly, some angiosperms, espe- Figure 4.36G with 4.35K). As we will see in Chapter 16, fern
cially monocots, exhibit homorrhizy in their embryos (Yamashita, shoot systems are characterized by their emphasis on leaf expan-
1976; Chapters 5 and 6) and we will want to deal with the signifi- sion and elaboration and this feature is also expressed in their
cance of this feature for their architecture in subsequent chapters. embryos. In fact, it is the early elongation of the leaf itself that
A more subtle but nevertheless striking correlation between is responsible for the photosynthetic emergence of the young
embryo organography and later plant architecture can be seen in fern sporophyte from the gametophyte and not the axis per se
the degree of elongation of the future stem region or axis of the (Figure 4.4F).
embryo. In Lycophytes, there is a significant variation in plant Finally, one of the most dramatic examples of the correla-
habit. The shoot of Isoetes, for example, is a corm-like rosette tion between embryogenesis and plant habit is expressed in the
characterized by nearly a complete suppression of internodal mycorrhizal flowering plant genus Monotropa (Monotropaceae).
elongation. It also exhibits very elongated, linear leaves, hence Monotropa hypopitys is a species that is heterotrophic and com-
its common name quillwort. By contrast, the shoots of species of pletely dependent upon a fungal symbiont for its carbon source.
Huperzia, Lycopodium, and Selaginella have marked stem elon- The plant body of Monotropa consists of an expanded root sys-
gation and much reduced, almost scale-like leaves. Looking at the tem with aerial, flowering shoots being initiated strictly from
morphology of their respective embryos before their emergence its roots (Figure 4.40A). This primacy of root development is
from the gametophyte, the young sporophyte of Isoetes shows already expressed in its embryogenesis.

SP R SP SC
EN EN R

RB
R RB
B. C. RB
R
SC
SP
RC
Srv
RB

A.
D.
R
F

SP
EN

RC

E.
0.1 mm

FIGURE 4.40 Embryo and germination stages of Monotropa hypopitys. A. Fully developed plant consisting of a root system producing shoot branches
from those roots. B–D. Stages in germination showing aborted shoot pole and well-developed root pole. E. Detail of late germination stage showing enlarged
primary root surrounded by hyphae of a mycorrhizal fungus and a well-developed root cap evident on the apex of the root. En, endosperm; F, fungus; R, root;
RB, root bud; RC, root cap; SC, seed coat; SP, shoot pole. (A from Rauh, 1937; B–E from Francke, 1934, 1935.)
Plant Embryogenesis 103

At maturity the tiny seeds of Monotropa exhibit a very sim- any further development. Thus the degree of embryo differen-
ple embryo consisting of both shoot and root poles. Cells at the tiation clearly foretells the emphasis on root expansion that is
shoot pole show no sign of cotyledon or apical meristem dif- the developmental pattern of the flowering adult. Since there
ferentiation (Figure 4.40B). By contrast, cells at the root pole is no primary shoot development, the only site of shoot origin
are smaller, more typically embryonic, and exhibit the tissue is from the roots. Looking at the development of other reduced
configuration of the root apex, including a rudimentary root cap and specialized plant species, such as parasitic flowering plants,
(Figure 4.40B–E). As soon as the root pole emerges from the we see similar examples of embryo shoot pole inhibition and the
seed, it is infected by hyphae from the mycorrhizal fungus and elaboration of the root system. Since embryo development is an
then the root pole begins to grow and expand into the elaborated obvious indicator of the fundamental developmental patterns in
root system that is the major component of the vegetative body various plant species, we will make future references to it when
(Figure 4.40C–E). The shoot pole never emerges from the con- analyzing the various deviations and specializations in plant
fines of the seed coat and ultimately aborts without undergoing structure in the remainder of this book.
5
Early Plant Development: From Seed to Seedling
to Established Plant

CONTENTS
After-Ripening in Seeds........................................................................................................................................................................ 105
Dormant State of the Seed.................................................................................................................................................................... 105
The Concepts of Seed Dormancy and Germination........................................................................................................................ 105
Structure of the Dormant Seed and the Locus of Reserve Storage..................................................................................................106
Exalbuminous Seeds...................................................................................................................................................................106
Albuminous Seeds......................................................................................................................................................................108
Divergent Seed Structure and Development in Orchids............................................................................................................. 110
Seed Germination.................................................................................................................................................................................. 112
Nature of the Process....................................................................................................................................................................... 112
Morphology of Germination............................................................................................................................................................ 112
Initial Stages in Relation to Ovule Structure.............................................................................................................................. 112
Basic Patterns of Growth During Germination........................................................................................................................... 112
Morphological Delineation between Hypocotyl and Root......................................................................................................... 117
Variations in Germination Pattern.................................................................................................................................................... 118
Eudicots...................................................................................................................................................................................... 118
Monocotyledons.......................................................................................................................................................................... 121
The Problematic Seedling of Grasses.........................................................................................................................................125
Concluding Remarks............................................................................................................................................................................. 132

In Chapter 4 we described the earliest stages of organ formation We have already described an example of after-ripening in
during embryogenesis and, in the case of seed plants, reviewed Chapter 4. In our description of endosperm development in the
the development of the young sporophyte up to the time of seed coconut palm, Cocos nucifera, we noted that when the coconut
maturity or dormancy. Beginning with the dormant seed, we now falls from the parent tree, the embryo is extremely reduced and
follow seed germination and seedling establishment. These are the cotyledon only expands to its full size after the first root has
the phases where the greatest mortality of offspring occurs, and emerged (Figure 4.11A,B). There are numerous other examples
thus are critical in the life history of a plant species. of similar types of continuous embryo development in seeds of
Since pteridophytic plants lack seeds and typically do not both gymnosperms and angiosperms. The few examples given
exhibit any dormancy but instead show a continuous develop- by Eames (1961) of the rates of development of embryos pro-
ment from the parent gametophyte generation, our focus for the vide some idea of the extent of intraseminal development in
majority of this chapter will be on seed plants. However, before such after-ripened seeds. Apparently germination will not initi-
looking at the structure of dormant seeds and their germination, ate until this more extensive embryo development has occurred
we first look at after-ripening in seeds, where instead of the under the environmental conditions required for each species
embryo showing a cessation of growth associated with dispersal (Eames,1961). The occurrence of after-ripening means that seed
from the parent plant, embryo development continues after the maturity is not a prerequisite for the release of the seed from the
seed has fallen. Despite occurring in a minority of species, it is parent plant. Along with the phenomenon of vivipary (Chapter 6),
still an interesting phenomenon that broadens our perspective on after-ripening emphasizes the artificiality of using seed disper-
the overall process of seed development. sal or dormancy as measures of the limits of embryogenesis in
seed plants.

After-Ripening in Seeds
Traditionally, after-ripening has been described physiologically, Dormant State of the Seed
usually referring to requirements for temperature, humidity, and
The Concepts of Seed Dormancy and Germination
light needed to induce germination in seeds after they have been
dispersed. The discovery of these requirements came before As described in Chapter 2, the seed plus or minus the surround-
scientists realized they were associated with continued embryo ing sporophytic tissues, i.e. the fruit wall, is the unit of disper-
development. sal for seed plants. Before it is carried to a new location distant

105
106 Kaplan’s Principles of Plant Morphology

from the parent sporophyte, the tissues of many seeds undergo nutrient matrix and how much of those nutritive tissues have been
a cessation in development associated with desiccation or dry- absorbed by the embryo by the 4time of dormancy (Figure 5.1A).
ing out. This suspension of development has been termed dor- In an exalbuminous seed, for example, growth of the embryo is
mancy. It also has been called quiescence because a low level so extensive that it absorbs virtually all of the nutrients from the
of metabolic activity (respiration) is maintained by tissues of the surrounding endosperm (or megagametophyte tissue in gymno-
seed even though growth has ceased. The hard seed coat, or testa sperms) and hence little else remains in the dormant seed. As a
(from Latin meaning brick or tile), derived from the integument, result, the embryo of an exalbuminous seed is itself the predomi-
chalaza, and raphe of the ovule provides protection and prevents nant site of nutrient deposition and accumulation. In an albumin-
further desiccation during dispersal. Once the seed has been dis- ous seed, by contrast, embryo development is more limited; the
seminated to its new site and water is available, then water is taken endosperm is not completely consumed prior to the inception of
up through the seed coat, enzymes synthesized and/or activated, dormancy. At the onset of dormancy, varying amounts of endo-
and metabolic activity and growth are resumed. Resumption of spermic tissue remain around the embryo and will be drawn upon
growth and emergence of the young sporophyte from the confines as a nutrient reservoir when the embryo germinates (see the coco-
of the seed coat is what comprises the process of germination. nut palm described in Chapter 4, Figure 4.11).
Since the initial growth and establishment of the young seed- As with any biological phenomena, there are all degrees of
ling is away from the parent plant and must be heterotrophic until intermediacy between these two seed types and rarely can an
it can unfold its own photosynthetic surfaces to be self-feeding, exalbuminous seed be found that is completely devoid of sur-
growth of the young sporophyte must depend initially upon rounding nutrient tissue. However, these two categories are use-
nutrient reserves deposited in the tissues of the seed. There are ful in defining the overall relationships of an embryo to its seed
significant differences where and how these nutrients are stored, nutritive sources.
and we now want to look at these variants.
Exalbuminous Seeds
Structure of the Dormant Seed and
Nutrient deposition in exalbuminous seeds occurs principally
the Locus of Reserve Storage
in one of two organ components of the embryo, either the leaf
As expected, the shape of the seed and the embryo contained component (i.e., the cotyledons) or the stem (i.e., the hypocotyl-
depends on the shape of the fertilized ovule from which it is devel- root axis). If nutrients are deposited in the leaf component, then
oped. In Figure 4.9 of the preceding chapter, we presented the the cotyledons are the major storage organs, and leaves of the
morphological relationships between the developing embryo and epicotyl do not exhibit much reserve deposition. Embryos in the
ovule for the range of ovule morphologies. A significant variable seeds of leguminous flowering plants have extremely large stor-
in seed structure is whether the nutrient reserves of the seed are age cotyledons that literally dwarf the embryonic axis and the
stored principally in the embryo itself or in a reserve tissue sur- epicotylar shoot contained between them (Figure 5.1B).
rounding the embryo. If the dormant seed has its reserves stored For example, the seed of the common bean plant (Phaseolus)
in the embryo with little or no surrounding nutritive tissue, then is the product of a campylotropous ovule in which the expanded
such a seed is exalbuminous (from the Latin prefix ex mean- embryo lies predominantly horizontally and the greatest propor-
ing deprived of, and albuminous the white of an egg or protein) tion of the embryo sac (ovule cavity) is occupied by the enlarged
(Figure 5.1B,C). By contrast, an albuminous seed is one that cotyledons. Looking at the seed externally, one can identify the
has considerable reserve nutrient tissue surrounding the embryo hilum or the scar of the funicle where the ovule was attached to
at dormancy (Figure 5.1D,E). the ovary wall of the leguminous fruit (Figure 5.2A,B). To one
Since the embryo grows at the expense of these surrounding side of the hilum, the raphe is expressed as a ridge running along
tissues, the difference between albuminous and exalbuminous that side of the ovule and bearing the single vascular strand that
seeds depends on the degree of embryo development relative to its carries nutrients the ovule. To the other side of the hilum is the

A B C D E

FIGURE 5.1 Diagrams of median longisections of developing and dormant seeds of angiosperms showing the degree of development of the embryo
(black), endosperm (stippled), and nucellar tissue (hatched) in: A. A predormancy developmental stage when the embryo is rudimentary, and the endosperm
has not fully digested the surrounding nucellar tissue. B. An exalbuminous seed with food storage in the cotyledons of the embryo. C. An exalbuminous
seed with food storage in the hypoctyl axis or the embryo. D. An albuminous seed. E. A perispermic seed where endosperm amount is limited but nucellar
tissue is correspondingly proliferated. (A, B, D, and E from Troll,1957.)
Early Plant Development 107

Co
Co
R

Hi
RA
Mi
RA

Co E Hy
P Co
A. B. C. D.

FIGURE 5.2 Seed structure and embryo morphology in Phaseolus multiflorus. A. Exterior of seed from lateral view. B. Exterior of seed from micropylar
view. C. Embryo after removal from exalbuminous seed, showing enlarged storage cotyledons with embryonic axis between them. D. Cross section of
embryo through the two cotyledons. Co, cotyledon; E. epicotyl; Hi, hilum or scar of seed; Hy, hypocotyl; Mi, micropyle; P, plumular leaves; R, raphe; RA,
radicle. (From Rauh, 1941.)

tiny micropyle, and adjacent to it a bulge which is the primary (Figure 5.2C). Upon germination, the proportions between
root of the embryo contained in the seed (Figure 5.2A,B). these organs will change markedly. The significant differences
When we remove the relatively thin testa, the exalbuminous in organ size in the seed condition simply reflect the differences
nature of the bean seed becomes obvious. There is no remain- in degree of enlargement between the storage and non-storage
ing endosperm and the enormous pair of storage cotyledons parts of the embryo. In some exalbuminous seeds, enlargement
dwarfs the hypocotyl-root axis (Figure 5.2C). If we tease apart of cotyledons can be so great that they become elaborately folded
the cotyledons, we can see the embryonic axis with the tiny root inside the seed and comprise the greatest proportion of seed vol-
apex at one end and the primordia of the epicotylar or plumu- ume. A dramatic example is seen in the walnut, Juglans regia
lar leaves at the other, with the short hypocotyl between them (Juglandaceae) (Figure 5.3).

Cot

Ra Cot

Ra
A. B. C. D.

E. F. G. H.
Cot

Hy + Ra
I. J. K.

FIGURE 5.3 Stages of the development of the embryo of walnut, Juglans regia, showing the great growth in surface of the cotyledons. Cot, cotyledon;
Ra, radicle. (From Troll, 1957.)
108 Kaplan’s Principles of Plant Morphology

By contrast, exalbuminous seeds which store food in the axis The differential distribution of food storage in either the leaf
rather than in the cotyledons exhibit a greatly thickened hypo- or stem components in embryos represent the same relationship
cotyl and reduced cotyledons (compare Figure 5.1C with 5.1B). as the food storage shoots in geophytic plants. Bulbs are stor-
For example, in the median longisection through the seed of the age shoots in which reserves are stored in the leaf component,
brazil nut, Bertholletia excelsa (Lecythidaceae), one can recog- whereas rhizomes are storage shoots in which food deposition
nize the shoot and root poles, but they are separated by a markedly occurs in the stem. Hence the accumulation of reserves in the
swollen hypocotyl, bearing only a microscopic pair of scale-like cotyledons is comparable to a bulbous habit, whereas deposition
cotyledons at the shoot pole (Figures. 5.4A–C; 5.4D–F). In this in the hypocotyl is analogous to the rhizomatous mode. It would
case the cotyledons undergo so little development that they are be interesting to know in what way the type of food deposition in
barely evident at all (Figure 5.4D). Embryos of some species of embryos relates to that of the later development of the individual
cacti (family Cactaceae) also have thickened embryonic stems plant species. In the case of the cacti, the swollen nature of their
(hypocotyl) and correlatively reduced cotyledons like those hypocotyl foretells the succulent stem habit they will exhibit later
found in Bertholletia. in their development. It is one more example of the relationship
of embryo development to that of the later, fully expanded plant
Cot
Cot we noted in Chapter 4.

Albuminous Seeds
Seeds that store nutrients in tissues outside of the embryo dif-
fer significantly in the developmental origin of these nutritive
Hy
tissues. Depending upon the group involved, reserves can be
stored in 1) megagametophyte tissue, 2) endosperm tissue, or 3)
perisperm tissue. While a section through an albuminous seed
with reserves stored in one of these three forms may look similar
(Figure 5.1D,E), they differ significantly in their developmental
origin and in their ploidy level.
Ra
A. B. C. Megagametophyte tissue is haploid and is found only in the
seeds of gymnosperms. Endosperm is typically triploid, and, as
we have noted previously, is the product of the fertilization of
Cot
the diploid central cell of the megagametophyte. Endosperm is
found only in angiosperms. Perisperm is diploid tissue which
Cot Cot originates by a proliferation of the nucellar (or megasporangial)
tissue of the ovule. Perispermic seeds are found only in certain
families of angiosperms, including Nymphaeaceae (water lilies),
Piperaceae (pepper family), and Zingiberaceae (ginger family)
as well as scattered representatives in a range of other flowering
E. plant families.
Perispermic seeds have endosperm development, but the
Hy endosperm is relatively small in comparison with the surround-
ing perisperm and tends to be used up in the pre-dormancy
development of the embryo (Figure 5.1E). Hence the more
Cot
massive perisperm is the site of food deposition for embryo ger-
mination (Figure 5.5A–C). The general relationship between
embryo, endosperm, and perisperm in developing seeds repre-
sents alternative modes of packaging nutrient reserves in the
Cot dormant seed. Since each of these tissues is surrounded by the
F.
other, the expansion and development of one is dependent upon
nutrient absorption from the other immediately surrounding
it. For example, in most angiosperm ovules, development and
enlargement of the embryo sac (megagametophyte) is usually at
Ra D. the expense of the surrounding nucellus. Normally, in the expan-
sion of the embryo sac, the endosperm mass derived from it is
FIGURE 5.4 Views of the seed and embryo of the Brazil nut Bertholletia so great that the surrounding nucellus is used up. This occurs
excelsa. A. Mature seed. B. Dissected whole embryo. C. Median longisec- especially early in tenuinucellate ovules with a small amount of
tion of whole embryo. D. Magnified view of median longisection of embryo, nucellar development.
showing markedly thickened hypocotyl, with inconspicuous, scale-like
cotyledons at the shoot pole and a rudimentary root apex at the opposite
If, however, the ovule has a proliferation of nucellar tissue,
pole. E. Detailed view of the overlapping cotyledons at the shoot summit. F. i.e., crassinucellate, then both megagametophyte and endosperm
Dissected view of the reduced cotyledons at the shoot pole. Cot, cotyledon; expansion may not use up the nucellus. Now, if only a limited
Hy, hypocotyl; Ra, radicle. (A–C from Rauh, 1941; D–F from Goebel, 1933.) amount of endosperm is formed, then most of that endosperm
Early Plant Development 109

Em
En

A
Pe A

Em

S
S
S
En

Pe
Em
En
Hy Pe

A. B. C.

FIGURE 5.5 Median longitudinal sections of perispermic seeds. A. Nuphar advenum (Nymphaeaceae). B. Alpinia natans (Zingiberaceae) and C. Elletaria
cardamomum (Zingiberaceae). A, aril; Em, embryo; En, endosperm; Hy, hypodermis; Pe, perisperm; S, seedcoats. (From Goebel, 1933.)

(whether free-nuclear or cellular) will be devoured by the devel- (Figure 5.6). Since these features tend to be characteristic of
oping embryo so that when seed dormancy has its inception, members of particular families of plants, their significance may
the only tissue that remains to be the site of nutrient deposition be phylogenetic rather than functional, although the functional
will be the proliferated nucellus or perisperm (Figure 5.1A,E). correlations have yet to be studied.
Hence in this type of albuminous seed, it is the nucellus that In contrast to those in exalbuminous seeds, embryos in
assumes the role of nutrient storage rather than the endosperm. albuminous seeds are generally smaller and do not have such
According to this interpretation, the perisperm would simply enlarged organs because they do not play a significant role in
represent a correlative developmental mode whereby the rela- nutrient storage. If you dissect the albuminous seed of the castor
tionships between endosperm and nucellus are shifted in favor bean Ricinus communis (Euphorbiaceae) (Figure 5.7A,B), in the
of the nucellus which serves as the site of reserve accumulation. same way that we did for the common garden bean Phaseolus
While the respective functions of endosperm and perisperm earlier, the contrast in the degree of embryo development is strik-
have not received recent evaluation with modern techniques, ing. Instead of the bulk of the seed’s space being occupied by
previous investigations suggest that, in some species at least, enlarged cotyledons, the majority is occupied by whitish endo-
endosperm and perisperm not only function at different times in sperm (Figure 5.7C,D). The whitish cotyledons in Ricinus are
embryo development but they may also differ qualitatively in the so thin that it is difficult to separate them from the surrounding
kinds of nutrients they contain. Goebel (1933) cites a cytochemi- endosperm (Figure 5.7C,D). It is only when a median longisec-
cal study of perispermic seeds in six species which suggests tion of the seed is made through the plane of the cotyledons that
that while the endosperm stores protein and fat, only starch is one can see the boundary between cotyledons and endosperm
deposited in the perisperm. However, more recent studies of seed (Figure 5.7D,E). When we follow germination in the following
cytochemistry in perispermic seeds of Yucca (Agavaceae) indi- section, we will see that the cotyledons of Ricinus play a differ-
cate that the perisperm of this species has protein and fat depo- ent role in germination and have a different developmental fate
sition but not starch (Arnott, 1962; Horner and Arnott, 1966). than those organs in Phaseolus.
The disparity between the results in Yucca and those cited by Lastly, it should be indicated that while albuminous seeds have
Goebel could be due either to taxonomic differences or to mat- the bulk of their nutrients stored in some surrounding, extra-
ters of technique. Unfortunately, the studies on Yucca did not embryonic tissue (megagametophyte, endosperm, or perisperm),
look at endosperm composition in comparison. Thus they did not this does not mean that reserves are not also stored in the body of
deal with the question of the relative roles of these two nutri- the embryo as well. As the median longisection of the dormant
tive tissues in embryo development which deserve attention using albuminous seed of Downingia in Figure 4.17B shows, not only
modern methods. are dark-staining protein bodies found in cells of the surround-
While embryos in exalbuminous seeds occupy the full volume ing endosperm but also in the body of the embryo, especially
of the seed, their proportion and position in albuminous seeds those of its cortex. Studies of the histochemistry of embryo ger-
is variable. Martin (1946) has surveyed the internal structure of mination have shown that the protein bodies stored in the embryo
seeds from 1287 genera of seed plants and classified the positions are the first to be digested, followed by those in the surrounding
of the embryo as being either 1) basal, 2) peripheral, or 3) axile, reserve tissue (Horner and Arnott, 1966; Jacobsen, 1984). Thus
depending upon the degree of development of the reserve tis- in the earliest phases of germination in albuminous seeds, the
sues and the distribution of growth in the albuminous region initial growth of the embryo may depend on its own reserves
110 Kaplan’s Principles of Plant Morphology

FIGURE 5.6 Figure showing varying relationships between the position of the embryo and its surrounding nutrient sources in albuminous seeds of flower-
ing plants. (From Martin, 1946 as reproduced in Esau, 1977.)

that are insufficient to sustain further growth. Embryos in such

albuminous seeds must break down those reserves stored in the
Sc
surrounding nutritive tissues if they are going to have sufficient
Co resources to maintain early establishment growth.
En
R Hy Divergent Seed Structure and
C C Ra C Development in Orchids
Hi
A. B. C.
Members of the tropical flowering plant family Orchidaceae
Sc exhibit a divergent mode of seed development that can be instruc-
tive in our understanding of the nutritional relationships in more
Co Co conventional seed types. The gynoecium of each orchid flower
En
contains literally millions of tiny, bitegmic (or unitegmic) tenui-
Co Co
nucellate ovules. When fertilized, they produce either no endo-
Hy
sperm or that which is initiated aborts after a few free-nuclear
Ra C Hy Ra divisions (Wirth and Withner, 1959).
D. E. Early development of the orchid embryo is similar to what we
have described in Chapter 4. However, after the definition of a
FIGURE 5.7 Seed and embryo structure in the castor bean plant Ricinus suspensor and the formation of terminal parenchyma, embryo-
communis. A. Seed from dorsal surface. B. Seed from ventral surface, show- genesis usually ceases. Thus the embryos of orchids do not
ing hilum and raphe. C. Seed cut in median longisection showing seed coat, undergo the usual organogenesis exhibited by most other spe-
endosperm, and surface view of one of the two cotyledons of the embryo.
D. Seed cut in the transverse longitudinal section showing thin cotyledons
cies but become arrested at the globular stage of development.
and hypocotyl surrounded by endosperm in this albuminous seed. E. Mature At this phase the seeds usually are dispersed and consist sim-
embryo dissected from seed. C, caruncle; Co, cotyledon; En, endosperm; ply of the transparent seed coat and the rudimentary embryo
Hy, hypocotyl; Ra, radicle; sc, seed coat. (From Troll,1957.) (Figure 5.8A,G).
Early Plant Development 111

1 mm

A. B. C.

SC

D.

SU 1 mm
50µ

G.

F. E.

p SC

100µ
SU H.

FIGURE 5.8 Orchid embryogenesis. A–F. Stages in germination and early seedling development in Odontoglossum. A, B. Seeds containing embryos. C,
D. Germination and early swelling or embryo to form a parenchymatous protocorm. E. Shoot initiation from distal pole of protocorm. F. Positively geotro-
pic root initiated from ventral side of protocorm. G. Median longisection through seed of Cattleya mendelii, showing mature spherical stage embryo with
multicellular suspensor and complete absence or endosperm. H. Young protocorm enlarging out of seed coat. P, papilla; SC, seed coat; SU, suspensor. (A–F
from Burgeff as reproduced in Goebel, 1933; G, H from Shushan, 1959.)

In nature, subsequent orchid embryo enlargement and ger- protocorm (Figure 5.8B–D,H). The thin seed coat is shed
mination is dependent upon its infection by a mycorrhizal during this dilation growth (Figure 5.8C,D,H). The distal pole
fungus. The fungus supplies carbon and other nutrients until of the protocorm is the site of origin of the shoot apex; the
the orchid develops its own shoot and becomes photosyn- first roots are initiated from the proximal face of the proto-
thetic (Hadley, 1982). Mycorrhizal infection occurs while corm (Figure 5.8E,F). By culturing orchid embryos on sterile
the embryo is still within the seed coat. The embryo then media in the laboratory, it is possible to artificially bypass the
undergoes considerable growth in volume to form an organo- fungal symbiont and determine the nutritional contribution of
graphically undifferentiated parenchymatous mass called a the fungus (Hadley, 1982).
112 Kaplan’s Principles of Plant Morphology

At first glance, the inhibited development of the orchid embryo water uptake. Using eosin dye uptake experiments combined
could be interpreted to result from the lack of endosperm and that with selective plugging of certain ovule positions with lacquer,
the mycorrhizal fungus supplies these nutritional requirements. Berggren demonstrated that in anatropous ovules, water uptake
However, Wirth and Withner (1959) have argued that since mem- occurs principally through the chalaza of the ovule and then
bers of some other flowering plant families—Podostemaceae, for spreads along the raphe to the hilum and then toward the root
example—also have ovules that lack endosperm, and yet have apex (Figure 5.10D–F). In the campylotropous ovules found in
embryos that become more elaborated than those of orchids, that leguminous seeds, uptake is principally through the hilum or
the rudimentary form of the orchid embryo cannot be attributed scar of the funicle and then spreads from the root apex toward
to the lack of endosperm. While raising an important point, the cotyledons (Figure 5.10A–C). Absorption in orthotropous
Wirth and Withner’s argument cannot be evaluated critically ovules takes place entirely through the micropyle to the radicle
without more detailed comparative study of seed development in tip and then along the radicle down to the cotyledons that are
both Orchidaceae and Podostemaceae. In a study of a member of directed toward the hilum (Figure 5.10 G–I). Thus not only is
Podostemaceae (Dicraea stylosa) Mukkada (1962) has suggested ovule morphology significant for the shape and developmental
that a densely cytoplasmic, free-nuclear cavity in the ovule of pattern of the embryo contained, it also can be significant for the
this species may serve the function of embryo nutrition. Hence mode of water uptake in the process of germination.
alternative nutritional modes may exist in developing seeds of Once embryo growth has been activated by the imbibed water,
Podostemaceae that account for the more extensive develop- the hypocotyl-root axis undergoes the most significant early
ment of their embryos. Given the significance of determining the elongation and is responsible for the emergence of the embryo
actual role of endosperm in embryogenesis in vivo, more detailed from the seed. In fact, physiologists typically use the emergence
study of such endospermless angiosperms is an important area of the primary root pole or radicle as the indicator that germina-
for future investigation. tion has occurred.
Since the root pole lies adjacent to the micropyle, one usu-
ally assumes that root emergence occurs through that opening of
the ovule. However, the actual diameter of the micropyle in the
Seed Germination mature seed of a legume such as a bean (Figure 5.2B) is tiny,
Nature of the Process and it is doubtful that any primary root could squeeze through
such a constricted opening. In fact, most embryos emerge from
If water is available where a seed has landed in a new location, the their seeds through much larger openings of the ovule which
seed will imbibe it. This imbibition, in turn, initiates a set of com- result from 1) the formation of slits or valves in the seed coat
plex physiological processes that mark the end of dormancy and which break open as the root grows through the micropyle, 2) the
the resumption of growth of the embryo, resulting ultimately in the embryo simply bursting through the seed coat, or 3) the embryo
emergence of the young sporophyte from the confines of the seed lifting off a kind of seed lid or operculum (Boesewinkel and
coat and its establishment in this new space as an independent, pho- Bouman, 1984). Such opercula are formed at the micropylar and
tosynthesizing plant. This entire process of germination is a mor- hilar region of the seed and are zones of weakness that result in
phologically complex process and has many variations, some of the separation of a lid from the ovule providing a larger exit for
which may represent adaptations to differing local environments. radicle emergence (Figure 5.11A–D).

Morphology of Germination
Basic Patterns of Growth During Germination
Initial Stages in Relation to Ovule Structure
Once the root pole has emerged from the seed coat, the embryo
One usually thinks of the seed coat, or testa, as a protective usually exhibits either epigeal germination or hypogeal germi-
structure of the seed, preventing desiccation beyond a certain nation. In epigeal germination (Figure 5.12A,B), the cotyledons
point, and, in different species, having various specializations are pulled above the soil level (from the Greek epi meaning upon
and elaborations of its surface to aid in seed dispersal, either by and geus meaning the earth) whereas in hypogeal germination
wind or animal vectors (Boesewinkel and Bouman, 1984). But (Figure 5.12C), the cotyledons remain below the soil (from the
as Klebs (1885) demonstrated, the epidermis of fruits and seeds Greek hypo meaning below and geus meaning earth).
also can be significant in attachment of the seed to soil particles, The fundamental difference between these two germination
not only for the purpose of water conduction, but also to bind patterns depends on the distribution of growth in the embryonic
the seed to the soil as a counterforce to the pull of the seedling axis. In epigeal germination, elongation occurs principally in the
emerging from the seed coat. Not only do some seeds, such as hypocotyl and is responsible for the extension of the seedling,
those of various Boraginaceae, have a tangle of hairs that serve including the cotyledons, above the soil level (Figure 5.12A,B).
to attach them to the soil particles, but many plants that grow in By contrast, in hypogeal germination, the hypocotyl remains
arid locations extrude sticky mucilages from their seed coats that short and shoot elongation occurs principally in the epicotyl,
glue the seed to the soil particles when it is wetted (Klebs, 1885). i.e. in that portion of the shoot above the point of insertion of
It had been assumed that water uptake in the ovule is gener- the cotyledons (Figure 5.12C). Because of this growth distri-
ally through the entire surface of the seed. However, Berggren bution, the cotyledons are neither pulled out of the confines of
(1963) has not only demonstrated convincingly that initial water the seed coat nor above the soil level. Whatever extension of the
uptake occurs preferentially in specific positions in the ovule shoot occurs above the soil is due to elongation of the epicotyl
but that different types of ovules can show distinctive paths of (Figure 5.12C).
Early Plant Development 113

86 hr 116 hr
76 hr
140 hr

57 hr

166 hr

n cot
em
45 hr
rad cot
te 120 hr ep
par
24 hr
72 hr par
ch 48 hr

pa
24 hr
rad

r
cot
hi
m m
m ch 96 hr
f
14 hr
hi

A. B. C.

48 hr

42 hr

par

ch

n 36 hr
raf plu ep
cot
rad
em cot
raf

24 hr par

ep
m rad

m
f
hi
m
hi
15 hr 12 hr

car
raf
ch

D. E. F.

m
par ch
24 hr

30 hr
raf
em
d
ra

car
p.carp
hi
m
te
n
42 hr per

ch
rad

cot

54 hr
66 hr hi

72 hr

G. H. I.

FIGURE 5.10 Diagrams of sections of ovules with differing morphologies, illustrating the paths of water movement and timing into each ovule. A.
Campylotropous ovule. B. Longitudinal section of seed of Brassica napus showing path of eosin-colored water absorption. C. Longitudinal section of
seed of Melandrium noctiflorum showing path of eosin-colored water absorption. D. Anatropous ovule. E. Longitudinal section of seed of Vicia 1utea. F.
Longitudinal section of seed of Trifolium pratense, showing the path of eosin-colored water absorption. G. Orthotropous ovule. H. Longitudinal section of
seed of Polygonum lapathifolium, showing the path of eosin-colored water absorption. I. Seed of T. pratense mounted to show the micropyle, hilum, raphe,
and chalaza. ca, caruncula; ch, chalaza; cot, cotyledons; em, embryo sac (in seeds, embryo); f, funiculus; hi, hilum; m, micropyle; n, nucellus; rad, radical;
raf, raphe; t, testa. Arrows indicate the primary place of absorption in the seed. (From Berggren, 1963.)
114 Kaplan’s Principles of Plant Morphology

FIGURE 5.11 Scanning electron micrographs of germinating seeds showing the mode of emergence of the root pole of the embryo from the seed coat
through opercula in: A. Begonia leptotrichia. B. Stanfieldiella imperforate. C. Phylidrium lanuginosum. D. Cereus aethiops. (From Boesewinkel and
Bouman, 1984.)

PL PL

Ep
Cot
Cot

PL PL

Hy Hy Ep

Cot

A. B.

C.

FIGURE 5.12 Diagram illustrating differences in growth distribution in early seedling development or a dicotyledonous flowering plant that produce an
epigeal germination pattern (A and B) and a hypogeal pattern (C). Cotyledons and hypocotyl-root are black, whereas epicotyl is clear. Cot, cotyledon; Ep,
epicotyl; Hy, hypocotyl; PL, primary leaf. (From Troll, 1959.)
Early Plant Development 115

Duke (1965) has proposed the use of two additional terms in the organ which shows the earliest and greatest development. Not
germination characterization. These are phanerocotylar (from only does it extend significantly in length, but it also produces a
the Greek phaneros meaning manifest or evident and cotyledon profusion of branch roots that extend laterally in contrast to the
meaning a hollow vessel) characterized by cotyledons that escape marked positive geotropism of the primary root (Figure 5.13A).
the seed coat during germination and cryptocotylar (from the Soon thereafter, the hypocotyl shows the greatest amount of elon-
Greek cryptos meaning hidden and cotyledon meaning a hollow gation. Because the cotyledons initially are inside the seed coat and
vessel) characterized by cotyledons that remain inside the testa represent a point of anchorage, in the early stages the hypocotyl
during germination. The usefulness of these terms is they add takes the form of a hook and pulls against the force exerted by the
another dimension to the characterization of germination morphol- fixed locus of the cotyledons (Figure 5.13A). Once the cotyledons
ogy. Plants that have hypogeal germination and hence cotyledons have emerged from the seed coat, the hypocotyl straightens up
that remain below the soil level will also usually be cryptocoty- and carries the cotyledonary pair at its summit (Figure 5.13B,C).
lar because the growth distribution in the epicotyl will not result Following cotyledon emergence, the first internode of the epi-
in cotyledon withdrawal from the seed coat (Figure 5.12E). cotyl elongates. It likewise assumes an initial hook configuration
However, in epigeal germination, the cotyledons may or may not because, like the hypocotyl, it is pulling against the forces of its
be withdrawn from the confines of the seed coat. Hence epigeal enclosed, enlarging first pair of primary leaves (Figure 5.13B).
germination may be either phanerocotylar or cryptocotylar. During germination, the two primary leaves expand markedly
Two members of the bean family Leguminosae—the common in comparison with the primordial form we initially saw them
garden bean Phaseolus vulgaris and the garden pea plant, Pisum in the ungerminated embryo (compare Figure 5.13B,C with
sativum—illustrate the contrast between epigeal and hypogeal Figure 5.2C). Once the pair of primary leaves is free of the seed
germination. Since the seeds of both species are exalbuminous coat, the epicotylar internode also straightens and grows erectly,
with reserves being deposited in the cotyledons, differences in separating markedly the point of primary leaf insertion from that
germination are due simply to differences in growth distribution. of the cotyledonary node below (Figure 5.13C,D). During subse-
Phaseolus exhibits both epigeal and phanerocotylar germina- quent epicotylar growth, new leaves are initiated from the shoot
tion and its first expression is protrusion of the root apex from the apical meristem and internodes elongate between them. Since
micropylar pole of its campylotropous ovule. The primary root is Phaseolus is a vine, its shoot emphasizes internodal elongation

foliage leaf
epicotyl
seed coat hook

cotyledons
epicotyl

seed coat
cotyledons withered
cotyledon
hypocotyl
hypocotyl

A. B. C. D.

FIGURE 5.13 Stages in the epigeal germination of the common garden bean, Phaseolus vulgaris. A. Emergence from seed coat showing elongated hypo-
cotylar hook. B. Hypocotyl straightens as cotyledons are pulled from seed coat. C. Cotyledons and epicotylar shoot unfold. D. Storage cotyledons wither as
shoot continues to grow. (From Weier et al., 1982.)
116 Kaplan’s Principles of Plant Morphology

and the resulting emphasis on stem extension is evident, even in The initial stages of hypogeal germination in the pea, Pisum,
the earliest phases of its seedling development. are similar to those of Phaseolus with the early emergence of
In describing the organ proportions in the ungerminated embryo the radicle (Figure 5.14A). But in contrast to bean, it is the epi-
of Phaseolus (Figure 5.2C), we noted the dominance in size of cotyl rather than the hypocotyl which undergoes the significant
the cotyledons relative to the rest of the embryonic body. From the early growth (Figure 5.14B,C). Like the hypocotyl in bean,
germination stages of this plant it is clear that the cotyledons reach early extension of the epicotyl is hooked as it pulls the shoot tip
their full size prior to dormancy and then cease to grow, whereas free of the confines of the testa (Figure 5.14B). However, subse-
the embryonic axis (including the primary root) elongates signifi- quent growth is strictly erect (Figure 5.14C). In contrast to the
cantly and ultimately becomes larger than the cotyledons. This is enlarged primary leaves with expanded blade surfaces of epicot-
because the cotyledons in bean are largely storage organs and will ylar leaves of Phaseolus, Pisum bears reduced, scale-type leaves
wither and die after the nutrients have been extracted from them for the first few nodes of the epicotyl until it emerges into the
(Figure 5.13C,D). As we shall see subsequently, not all species air (Figure 5.14D). Thereafter the leaves are larger, more con-
have cotyledons which are so limited in their development; many ventionally laminate organs. Like the cotyledons in Phaseolus,
have seed leaves that actually enlarge beyond their size in the seed those in Pisum function strictly in reserve storage. Because of
and serve as photosynthetic organs as well. the hypogeal germination pattern, not only are they not pulled

young shoot

epicotyl
seed coat

cotyledon

hypocotyl hypocotyl

radicle

A.

secondary roots

primary root

B.

C.

D.

FIGURE 5.14 Stages in the hypogeal germination of the garden pea, Pisum sativum. A. Emergence and positively geotropic growth of the root pole. B.
Emergence of the epicotyl while cotyledons stay in seed coat. C. Continued downward growth of root and upward growth of shoot. D. Epicotylar shoot comes
aboveground while first root produces lateral branches. (From Weier et al., 1982.)
Early Plant Development 117

above the soil, but they remain enclosed by the seed coat and the collet will stay inside of the seed coat and serve as a point of
have their nutrients withdrawn and translocated to the growing absorption and attachment while the shoot and root poles grow
regions of the shoot and root (Figure 5.14D). Hence Pisum is up and down from it (Klebs, 1885). In other species, especially
cryptocotylar. in aquatic plants where the primary root is retarded in its out-
growth, an abundance of hairs is produced from the margins
of the collet which then serves as the point of anchorage of the
Morphological Delineation between
seedling to the substratum (Figure 5.15). Thus not only is the
Hypocotyl and Root collet useful as a developmental marker, but it also can have an
In distinguishing the locus of growth in the embryonic axis dur- important function in seedling establishment.
ing germination, one problem is determining how much growth Where such a collet is well developed, it frequently already
occurs in the hypocotyl versus the primary root which, exter- appears in the embryo as a collar surrounding the root apex;
nally, can look simply like a continuation of the hypocotyl. compare this to the way an integument surrounds the nucel-
While the upper boundary of the hypocotyl is clearly demarcated lus of an ovule (compare Figure 4.6 with Figure 5.16C,D).
by the cotyledonary node, its lower boundary with the primary In such species there is no difficulty in delimiting the bound-
root is more difficult to define. It was just the absence of such a ary between hypocotyl and root, for the latter is only repre-
hypocotyl-root delineator in the embryos of many seed plants sented by the root apical meristem. For example, the embryo
that led us to refer to their embryonic axes as the “hypocotyl- of Eucalyptus globulus (Myrtaceae) has a well-defined collet
root” in Chapter 4. encasing its radicle (Figure 5.16A,B). During germination
In Chapter 1 we noted that the root and stem have distinc- most of the extension occurs in the hypocotyl and the root
tive tissue arrangements, especially in their vascular tissues apex appears only as a small nubbin, surrounded by the collar
(Figure. 1.7). The anatomical transition between root and stem (Figure 5.16A,B). The collet in Eucalyptus also produces a
typically occurs in the hypocotyl (Esau, 1977), but there may
be no external sign of that change. Fortunately, during the ger-
mination of some species, a marker often develops between the
hypocotyl and root that helps to determine the relative rates of
elongation of these two organs during early seedling growth.
This is the so-called collet, or collar.
The collet usually is a swelling around the base of the hypo- C
C
cotyl and is delimited proximally by the much narrower diameter C. Ra Ra D. S

of the primary root (Figure 5.15). In some species, one edge of

Co Co
Hy
Hy
C

C
Hy
Ra
C Ra Ra
A. B.
S

A. Hy
C

C
Rh
C. D.
R
C
C

E. F.

F.
FIGURE 5.16 Collet development in the embryo and seedling or
Eucalyptus globulus. A. Embryo dissected from mature seed showing
enlarged, lobed cotyledons. B. Germinating seed with two embryos. C.
B. E. Detail of root pole of embryo showing collet surrounding the radicle apex.
D. Median longisection of root pole of ungerminated embryo showing collar
FIGURE 5.15 Germination stages of dicotyledons exhibiting a collet with surrounding the root apex. E. Germinated seedling showing the develop-
a wreath of root hairs demarcating the hypocotyl from the primary root in: ment of a rhizoidal wreath from the margins of the collet at the base of the
A, B. Clintonia pulchella; C. Elatine hexandra; D. Sempervivum patens; E. hypocotyl. F. Longisection through the hair-bearing collet shown in E. C,
Phyllodoce taxifolia; and F. Anemopsis californica. c, collet. (From Klebs, collet; Co, cotyledon; Hy, hypocotyl; R, primary root; Ra, radicle; Rh, rhi-
1885.) zoids. (From Briosi, 1882 as reproduced in Troll, 1943.)
118 Kaplan’s Principles of Plant Morphology

profusion of hairs such that the young seedling looks like a lit- like that of Phaseolus (Figure 5.17), but instead of withering
tle ballerina (Figure 5.16E,F). It is only after these hairs have after nutrients have been withdrawn, as in storage cotyledons,
grown out and anchored the seedling that the radicle grows out those in Ricinus are initially absorptive while still in the seed
and down (Figure 5.16E). coat. They then expand and photosynthesize before they die
(Figure 5.17).
Some phanerocotylar species have photosynthetic cotyledons
Variations in Germination Pattern that expand their surfaces significantly following their emer-
gence from the seed coat. For example, in Oenothera bistorta
Eudicots
(Onagraceae), a recently germinated seedling bears only small,
The castor bean Ricinus communis (Euphorbiaceae) exhibits a ovate cotyledons (Figure 5.18A). During subsequent growth
typical epigeal germination pattern nearly identical to what we not only do the two cotyledons develop flattened stalk regions
have described earlier in Phaseolus (Figure 5.17), but with a sig- resembling a petiole (Figure 5.18A), but these stalks undergo
nificant difference in the development and fate of its cotyledons. a significant intercalary growth in length so that they not only
As we noted earlier, the seeds of Ricinus are albuminous with come to comprise the greatest proportion of total cotyledon
very thin cotyledons. Germination is epigeal and phanerocotylar length, but they also grow in breadth so that they become nearly

hypocotyl
seed coat endosperm

endosperm radicle

foliage leaf
B. epicotyl
A.

seed coat

cotyledons

withered cotyledons

hypocotyl

hypocotyl
endosperm

C. D. E.

FIGURE 5.17 Germination and early seedling development in the epigeal castor bean, Ricinus communis, showing non-storage cotyledons that initially
are haustorial (A–C) and then open up and photosynthesize (D) and finally wither (E). (From Weier et al., 1982.)
Early Plant Development 119

l l

C1

C1

C1

C1 l
l

A.
B.

FIGURE 5.18 Germination stages in Oenothera bistorta, showing the post-germination expansion of the cotyledon photosynthetic surface by the intercala-
tion of a basal blade segment (A) which subsequently expands in surface and develops a rib so that the cotyledons come to resemble the foliage leaves that
follow (B). C1 the original cotyledon blade surface; 1, the intercalated blade segment. (From Lubbock, 1892 as reproduced in Goebel, 1933.)

as wide as the “original” cotyledonary blades (Figure 5.18B). L

pet
In addition, the intercalated blade regions develop a thickened
midrib that makes them resemble the foliage leaves that follow
(Figure 5.18B). The only features that distinguish O. bistorta
cotyledons from subsequent appendages is the presence of the L
original ovate blade at their tips (C1 in Figure 5.18B). V
In addition to various nutritional roles, cotyledons also may be
the first and only part of the embryo to emerge above the soil in V CoT
germination. In Smyrnium oluastrum (Umbelliferae), for exam-
ple, germination is epigeal and phanerocotylar but differs from V
what we have described in Phaseolus and Ricinus; its hypocotyl
remains short and it is the petioles of the cotyledons that elon-
gate significantly to carry the cotyledonary blades above the soil
surface for photosynthesis (Figure 5.19A–C). The cotyledons of
S. oleastrum are united into a tube at their base and some elon-
gation occurs in the basal tube. The majority of cotyledonary C.
extension, however, occurs in the petioles between the proximal
tubular base and distal blades (Figure 5.19B). The first leaves
of the epicotyl will then grow upward between the cotyledons
(Figure 5.19C) (Klebs, 1885).
While the cotyledons in Smyrnium oleastrum are united A.
only at the base, some geophytic genera such as Podophyllum B.
(Berberidaceae) and Eranthis (Ranunculaceae) have cotyledon
petioles that are entirely united into an elongated tube which FIGURE 5.19 Germination stages of Smyrnium olusatrum where it is
play a significant role in the regulation of epicotylar depth in the cotyledonary petioles that exhibit the most significant elongation in
the soil. What looks like a hypocotyl in the seedlings of spe- carrying the blades above ground (A–C) rather than elongation in the
cies in these two genera is actually the common cotyledonary hypocotyl which remains short here. Cotyledons are fused into a coty-
ledonary tube at their base. CoT, cotyledonary tube; L, lamina of coty-
tube with two cotyledonary blades borne at the top of that tube
ledons; Pet, free petiole of cotyledon; V, vegetative apex. (From Klebs,
showing some degree of union as well (Figure 5.20B,C). The 1885.)