H+ H+

N
N Ca2+ Ca2+

PERCEPTION TRANSDUCTION TRANSMISSION RESPONSE

23
Tropisms and Nastic Movements:
Orienting Plants in Space

The power of movement is not normally associated with pulvinus. Within each group, we can further distinguish
plants. Yet movement pervades the life of the green between nutation, tropism, and nastic movement.
plant. Movement in higher plants does not involve loco- The term nutation (or circumnutations) denotes a
motion as it does in animals, nor is it so obvious. Plant regular rotary or helical movement of plant organs, most
movement is mostly slow and deliberate, but it is a typically the stem apex, in space. Nutations are best de-
key factor in determining the orientation of plants in monstrated by time-lapse photography. Tropic respon-
space. Plants that have been inadvertently placed in the ses are directionally related to the stimulus such
horizontal position will reorient their root and shoot as light (phototropism), gravity (gravitropism), water
to the vertical. House plants will bend, appearing to (hydrotropism), or touch (thigmotropism). Nastic respon-
seek light coming through a window. Leaves may peri- ses are not obviously related to any vector in the stimu-
odically rise and fall throughout the day and night, lus. Directionality of nastic responses is inherent in the
while others track the sun as it moves across the sky. tissue and includes epinasty (bending down), hyponasty
Leaves of the Venus flytrap snap closed on a hapless (bending up), nyctinasty (the rhythmic sleep movements
insect. While most plant movements are relatively slow, of leaves), seismonasty (response to mechanical shock),
they nonetheless serve important functions by position- thermonasty (temperature), and thigmonasty (touch).
ing organs for the uptake of nutrients and water and This chapter will focus on the three plant move-
optimal interception of sunlight, or (in the case of the ments that have been explored most thoroughly. These
flytrap) obtaining nutrients such as nitrogen through are
the leaves.
There are two principal categories of movement in • phototropism, particularly the nature of the pho-
plants, based on the distinctiveness of their mechanisms. toreceptor and the role of auxin in the signal trans-
Growth movements are irreversible. They arise as duction chain,
the result of differential growth within an organ or • gravitropism, including a brief discussion of the
between two different organs. Turgor movements nature of the gravitational stimulus and the mecha-
are reversible, resulting from simple volume changes in nism of gravity perception, the particular character
certain cells—most often in a special organ called the of gravitropism in shoots and roots, and the role

391
392 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

of auxin and calcium in the differential growth res- angles intermediate to the light. Roots, on the other
ponse, and hand, are largely nonphototropic, although some may
• nastic movements, including the structure of motor exhibit a weakly negative response. The stems of ivy
organs and the role of potassium flux in nyctinastic (Hedera helix) are negatively phototropic during the
and seismonastic movements. shade-loving juvenile stage, but older branches become
positively phototropic. The stems of ivy-leafed toad
flax (Cymbalaria muralis) become negatively phototropic
following fertilization. This interesting behavior helps
23.1 PHOTOTROPISM: to place ripening seed pods into crevices in the walls on
REACHING FOR THE SUN which the plant is normally found.
Most people are familiar with the sight of house plants
bending toward the light from an open window, an 23.1.1 PHOTOTROPISM IS A RESPONSE
everyday example of the phenomenon called pho- TO A LIGHT GRADIENT
totropism (Figure 23.1). Phototropism is a classic plant
physiology problem that has attracted the interest of Phototropism is often defined as a response to unilateral
botanists since the middle of the nineteenth century. light, and so it is in the laboratory. Under normal growth
Darwin’s study of phototropism, published in his book conditions, however, the bending response will occur
The Power of Movement in Plants in 1881, is credited even in plants that are receiving light from all sides.
with overcoming the preoccupation of English-speaking All that is required is that the fluence rate be unequally
botanists with descriptive and taxonomic biology and distributed. In experiments with bilaterally illuminated
stimulating an interest in the more dynamic aspects of grass coleoptiles, for example, as little as 20 percent
plant function. Cell elongation in phototropically stim- difference in fluence rate on the two sides of the organ
ulated grass coleoptiles also led to Went’s discovery of will induce a bending response (Figure 23.2). Thus light
plant hormones (Chapter 18). can be presented unilaterally (as it is in most laboratory
Tropic responses may be either positive or negative. experiments), bilaterally, from all sides, and even from
If a plant responds in the direction of the stimulus (e.g., above, providing only that a gradient is created across
toward a light source) it is said to be positive. If it the organ. Phototropism is thus a growth response to a
grows away from the stimulus it is said to be negative. light gradient.
Whether the phototropic response is positive or negative The magnitude of a light gradient across an organ
depends largely on the nature of the organ or its age. such as a coleoptile is dependent on optical properties
For example, coleoptiles, hypocotyls, and the elongating of the tissue as well as differences in incident light.
portions of stems and other aerial organs are for the A light gradient across an organ, for example, can be
most part positively phototropic while the tendrils of
most climbing plants are negatively phototropic. Leaves
are normally plagiotropic, which means they orient at

FIGURE 23.2 A phototropic response will occur whenever

there is a light gradient established across the stem or
FIGURE 23.1 The phototropic response in oat (Avena coleoptile axis. The upper part of the figure represents
sativa) coleoptiles. Left: Dark-grown seedling placed unilateral illumination, which is normal in experimental
in unilateral blue light, from the right, for 90 minutes. situations. The lower part of the figure illustrates bilat-
Right: Unlighted control. Note that the overall length eral illumination, with the highest fluence rate from the
of the coleoptile is approximately the same in the two right. Phototropic curvature is the same in either case.
seedlings.
 23.1 Phototropism: Reaching for the Sun 393

intensified by screening within the organ. Pigments,

including but not limited to the photoreceptor itself, (A)
will attenuate the light as it passes through the organ.
Light can also be attenuated by scattering, reflection,
or diffraction within the cells or as it passes between

Relative absorption or response

cells. Thus gradients across individual cells, measured
by using microfiberoptic probes, may vary from 5:1
to 50:1. To further complicate matters, organs such (B)
as coleoptiles appear to function as light pipes. This
means that light applied to the tip, for example, will
be transmitted through the coleoptile to cells fur-
ther down the organ. Thus the phototropic stimulus
is far from being a simple matter. These complex
(C)
interactions between light and the optical properties
of tissue have led to significant difficulties in experimen-
tal design as well as in interpretation of the resulting
data.

350 400 450 500

Wavelength (nm)

23.1.2 PHOTOTROPISM IS A FIGURE 23.3 (A) The action spectrum for Avena coleop-
BLUE-LIGHT RESPONSE tile phototropism. The action spectrum shows peak
activity in the blue and UV-A regions of the spectrum.
Since the 1930s, action spectra for phototropism have For comparison, the absorption spectra for riboflavin, a
been repeatedly determined for a number of organisms, common flavonoid (B), and β-carotene (C) are shown.
but have been most thoroughly documented for coleop- Although β-carotene ‘‘fits’’ in the blue region (around
tiles of oats (Avena sativa) and maize (Zea mays) and for 450 nm), riboflavin has the required absorption in both
sporangiophores of the fungus Phycomyces. The action the blue and the UV-A regions (320 nm–400 nm) of the
spectra for oat coleoptiles and Phycomyces are virtually spectrum.
identical, indicating that they share a homologous, if not
common, photoreceptor. All other phototropic action
spectra are similar and consistently show two peaks in 23.1.3 PHOTOTROPISM ORIENTS
the blue region of the spectrum near 475 nm and 450 nm A PLANT FOR OPTIMAL
and a small peak or shoulder at 420 nm (Figure 23.3).
PHOTOSYNTHESIS
In addition there is a broad action peak in the UV-A
region near 370 nm. The action spectra for both oat and The phototropic blue-light response is distinct from
Phycomyces phototropism show an additional peak in the the blue-light responses mediated by phytochrome
region of 280 nm, indicating that the photoreceptor is and cryptochrome that were discussed in the previous
probably a chromoprotein. chapter. Phytochrome and cryptochrome responses
As early as the 1940s, it was suggested that the are morphogenetic responses—they alter the pattern
photoreceptor could be a flavin molecule such as ribo- of growth and development. The singular impact of
flavin. However, because of its action spectrum the pho- phototropism, on the other hand, is that it orients
toreceptor for phototropism was subject to the same growth and leaf angle toward incident light in order
flavin-carotenoid controversy described in the previous to maximize light interception for photosynthesis. The
chapter for other blue-light responses now known bending of coleoptiles and hypocotyls is only the most
to be regulated by the cryptochromes. On the other visible part of a larger blue-light syndrome that plants
hand, there were several physiological results that use to optimize photosynthesis. Plants also use blue light
ruled out carotenoids as the photoreceptor for pho- to control stomatal opening and facilitate gas exchange
totropism long before the responsible pigment, photo- as well as to relocate chloroplasts within the cell.
tropin, was finally discovered and shown to be a It has long been known that stomatal opening is
flavo-protein. Carotenoid biosynthesis, for example, under the control of light. On the one hand, light
can be blocked, either by mutation or by treatment absorbed by chlorophyll (i.e., red light) stimulates stom-
of seedlings with the herbicide norflurazon, which atal opening and obviously depends on photosynthetic
inhibits the enzyme phytoene desaturase. Yet reactions in the guard cell chloroplasts. However, there
carotenoid-deficient maize mutants, albino barley is a second, much more sensitive, system that is driven
seedlings, and norflurazon-treated seedlings all exhibit by low levels of blue light. Most of the evidence points
a normal phototropic response to blue light. to a dominant role of the blue-light response in the early
394 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

phases of stomatal opening, such as when the stomata pism is characterized by a rather curious fluence-
open at dawn, prior to the beginning of photosynthesis. response curve, quite unlike most photobiological
Plants also use blue light to control the high-light responses.
avoidance response of chloroplasts in the mesophyll Fluence response curves are generally obtained
cells. In low light, the chloroplasts always gather along by monitoring the response of the organ to differ-
the cell walls that are parallel to the surface, (i.e., peri- ent total amounts of light (fluence), usually by using a
clinal walls) that are perpendicular to the incident light single fluence rate but varying the presentation time.
(Figure 23.4). In high light, such as direct sunlight, Figure 23.5 shows a fluence-response curve determined
the chloroplasts avoid potential damage by lining up for Avena coleoptile phototropism that illustrates the
along the anticlinal walls (i.e., parallel to the incident classic response to increasing fluence. There is an initial
light). The redistribution of chloroplasts appears to be rise to a first peak, which is called first positive curva-
in response to a light gradient through the cytoplasm, ture. With increasing fluence, curvature declines, to the
so the responsible photoreceptor is probably located point that this may even result in a bending away from
in the cytoplasm, not the chloroplasts. The mecha- the light source. This decline and negative response is
nism of redistribution has yet to be discovered, but the called first negative curvature. Note that first negative
cytoskeleton is commonly involved in moving organelles curvature is not necessarily ‘‘negative’’ in the sense of
within the cell and may be involved in the movement of bending away from the light. It may be simply a reduced
chloroplasts as well. positive response. Following the region of first negative
curvature, the response curve again rises into what is
called second positive curvature. In some cases, a sec-
23.1.4 FLUENCE RESPONSE CURVES
ond negative and even a third positive curvature have
ILLUSTRATE THE COMPLEXITY
been reported. First positive curvature is also known
OF PHOTOTROPIC RESPONSES as tip curvature, because it is restricted to the apex of
Perhaps no aspect of phototropism has indicated the coleoptiles. Second positive curvature is also called basal
complexity of the process so much as attempts to define curvature because the curvature extends more toward
relationships between fluence and response. Phototro- the basal region of the coleoptile.

FIGURE 23.4 The high-light avoidance response of chloroplasts in a typical meso-

phyll cell. In low light conditions (left), the chloroplasts gather perpendicular to the
incident light along the upper and lower (periclinal) walls in order to maximize light
interception. In high-light conditions (right) the chloroplasts gather along the side
(anticlinal) walls, or parallel to the incident light, in order to avoid damage due to
excessive light. Mesophyll cells are shown in cross-section (A) and surface view (B).
 23.1 Phototropism: Reaching for the Sun 395

were drawn together in the late 1920s in an attempt to

2nd Positive explain phototropism. The Cholodny-Went hypoth-
36 1st Positive
esis states that unilateral illumination induces a lateral
redistribution of endogenous auxin near the apex of the
organ. This asymmetry in auxin distribution is main-
Degrees curvature

24 tained as the auxin is transported longitudinally toward

1st Negative the base of the organ. The higher concentration of auxin
on the shaded side of the organ stimulates those cells
12
to elongate more than those on the lighted side. It is
this differential growth that causes curvature toward the
0 light source.
The experimental basis for the Cholodny-Went
hypothesis is derived largely from agar-diffusion exper-
–13 –12 –11 –10 –9 –8 iments originally conducted by Went and described
Log fluence (mol photons cm ) –2 earlier in Chapter18. In Went’s experiments, oat coleop-
tiles were first stimulated with unilateral light. The
FIGURE 23.5 A phototropic fluence-response curve for
coleoptile apices were then excised, split longitudinally,
Avena coleoptiles. First positive, first negative, and sec-
ond positive curvatures are indicated. and the two halves placed on agar blocks in order to col-
lect the auxin that diffused out of the base. The amount
of auxin collected in the agar blocks was then assayed by
There is a fundamental law of photochemistry, the Avena curvature test (Chapter 18). Went reported
called the Bunsen-Roscoe reciprocity law, which says that a significantly higher quantity of auxin was collected
the product of a photochemical reaction is determined from the shaded half of the coleoptile apex than from the
by the total amount of energy presented, regardless of lighted half, indicating that unilateral lighting caused a
fluence rate or presentation time. In other words, the greater proportion of the auxin to be transported down
same result is obtained with either a brief exposure the shaded side of the coleoptile.
to a high fluence rate or a longer exposure to a low Doubts as to the validity of the Cholodny-Went
fluence rate. Numerous experiments have established hypothesis arose from numerous unsuccessful attempts
that the reciprocity law applies to first positive cur- to verify asymmetric auxin distribution by applying
14 C-labeled IAA to tropically stimulated coleoptiles.
vature but does not apply to first negative or second
positive curvatures. Second positive curvature is instead These problems, however, may be largely attributed to
very time-dependent. In other words, second positive poor experimental technique. It is now evident that a
curvature is more dependent on presentation time than large proportion of the radioactive auxin taken up by
on fluence rate. Failure of reciprocity for second pos- the tissue in those experiments did not enter the auxin
itive curvature suggests the possibility that more than transport stream. When care is taken to discount this
one photoreceptor might be involved. However, action nondiffusible auxin, a clear differential in auxin transport
spectra have been determined for both first and second can be detected. For example, when maize coleoptile tips
positive curvature and they are identical. Apparently were supplied with 14 C-IAA, approximately 65 percent
both first and second positive curvature are mediated by of the radioactivity was recovered from the shaded side.
the same photoreceptor and the complexities of second There was no significant asymmetry when subapical
positive curvature are due to subsequent events in the sections were used, further evidence that the lateral
signal transduction chain. redistribution of auxin occurs at the very apex of the
coleoptile.
23.1.5 THE PHOTOTROPIC RESPONSE In the 1960s, the Cholodny-Went hypothesis was
systematically reevaluated by W. R. Briggs and his col-
IS ATTRIBUTED TO A LATERAL
leagues. Briggs repeated Went’s original split-tip exper-
REDISTRIBUTION OF
iments but, unlike Went, he excised the tips and placed
DIFFUSIBLE AUXIN them on agar blocks before presenting the phototropic
At the same time F. W. Went and his contemporaries stimulus. The results (Figure 23.6) clearly demonstrate
had chosen to study the influence of the apex on coleop- that when the tip is partially split, leaving tissue conti-
tile elongation, parallel studies on the role of the root nuity only at the very apex of the coleoptile, exposure
apex were being conducted in Germany by N. Cholodny. to unilateral light causes an increase in the amount of
The result was independent proposals by Cholodny, in diffusible auxin on the shaded side and a decrease on
1924, and Went, in 1926, that the apex was able to the lighted side. The total amount of auxin recovered,
influence cell elongation in the more basipetal extension however, remains effectively constant. When lateral
region of the organ. These ideas of these 2 investigators diffusion of auxin is prevented throughout the entire
396 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

A. DARK CONTROL the differential in auxin-regulated gene expression could

Intact tip
be detected before there was any noticeable curvature of
25.8 the hypocotyls.

B. ILLUMINATED
Intact tip 23.1.6 PHOTOTROPISM AND RELATED
25.6 hν RESPONSES ARE REGULATED BY
A FAMILY OF BLUE-SENSITIVE
FLAVOPROTEINS
C. ILLUMINATED
Partially split tip
Two lines of study led to the discovery of the photore-
30.7 16.2 hν ceptor for phototropism, now called phototropin. In
the late 1980s, it was reported that blue light stimulated
D. ILLUMINATED
the phosphorylation of a 120 kDa plasma membrane
Totally split tip protein localized in the actively growing regions of etio-
22.3 23.0 lated pea seedlings. This is the same region that is most
hν
responsive to the phototropic stimulus. After extensive
FIGURE 23.6 Phototropic stimulation establishes an biochemical and physiological characterization, the pro-
asymmetric distribution of diffusible auxin in excised Zea
tein was found to be a kinase that autophosphorylates in
mays coleoptile apices. (A, B) Intact control apices. A was
maintained in darkness and B was provided light unilat-
blue light. There was also a strong suggestion that this
erally from the right. (C) Tips were partially split, leaving kinase was the photoreceptor for phototropism.
tissue continuity only at the very apex. A microscope A short time later, a mutant characterized by a
cover slip was inserted to provide a barrier to lateral failure to respond to the phototropic stimulus (non-
diffusion. The tips were then presented with unilateral phototropic hypocotyl 1, or nph1) was isolated from
light from the right. (D) Tips were totally split and the Arabidopsis. Plants carrying the nph1 mutant not only
diffusion barrier passed through the apex before being failed to exhibit phototropism, but coincidentally lacked
presented with unilateral light from the right. Numbers the 120 kDa membrane protein. When the NPH1 gene
indicate the amount of auxin collected in the agar blocks was cloned, it was found, as expected, to encode the
over a 3-hour period, based on degrees of curvature in 120 kDa protein. The NPH1 holoprotein was subse-
the Avena curvature bioassay. Values are for auxin col-
quently renamed phototropin 1 (phot1) because of its
lected from 3 tips (A, B) or 6 half-tips (C, D). (Data from
Briggs, W. R. 1963. Plant Physiology 38:237.)
functional role in phototropism.
Phototropin 1 is a flavoprotein with two flavin
mononucleotide (FMN) chromophores (Figure 23.7). It
has a carboxy-terminal domain with the characteristics
of a serine-threonine kinase. The photosensory domain
length of the tip, no such asymmetric auxin distribution at the N-terminus has two distinctive domains called
is observed. These results clearly support the princi- LOV domains, so named because they share charac-
pal tenet of the Cholodny-Went hypothesis, namely, teristics with microbial proteins that regulate responses
that unilateral light induces a preferential migration of to light, oxygen, or voltage. Not surprisingly, the two
auxin down the shaded side of the coleoptile. Their LOV domains are the two sites that bind FMN and make
experiments also confirmed that auxin production in phototropin responsive to light. A second phototropin,
coleoptiles of Zea mays is confined to the apical 1 to 2 mm phototropin 2 (phot2), has since been discovered. On
and that lateral redistribution during phototropic stim- the basis of amino acid sequence, the two phototropins
ulation probably occurs within the most apical one-half are about 60 % similar, but the two LOV domains are
mm. virtually identical and each phototropin binds two FMN
Compelling support for the Cholodny-Went the- chromophores.1
ory has been provided by a more recent study of auxin The two phototropins found in Arabidopsis, phot1
redistribution in Brassica oleraceae hypocotyls. The free and phot2, exhibit some overlapping functions. Each
IAA concentration found on the shaded side of the also appears to have unique physiological roles. First
hypocotyl was found to be at least 20 percent higher positive curvature appears to be mediated solely by
than on the lighted side following phototropic stimula-
tion. Moreover, the differential auxin concentration was
accompanied by a several-fold increase in the expres- 1
In 2001, the gene for photo2 was originally described as
sion of auxin-regulated genes on the shaded side of the NPL1 (NPH-like1), a homolog of the gene NPH1 (non-
hypocotyls, including two members of the α-expansin phototropic hypocotyl 1) or PHOT1. NPL1 has since been
family of genes that are necessary for cell wall extension renamed PHOT2 to bring the nomenclature in line with
(see Chapter 17). Finally, both the auxin differential and phototropin 1.
 23.1 Phototropism: Reaching for the Sun 397

FIGURE 23.7 The domain structures

PHOTOTROPIN
of phototropin and neochrome. Pho-
toropin contains two LOV domains
N LOV 1 LOV 2 Ser-Thr Kinase C that are characteristic of proteins
activated by light, oxygen, or volt-
age. Each LOV domain carries
NEOCHROME one flavin mononucleotide chro-
mophore that absorbs in the blue
region of the spectrum. At the
carboxy-terminal end of the pro-
N LOV 1 LOV 2 Ser-Thr Kinase C tein (–C) is a serine-threonine kinase
domain. Note that neochrome is
virtually identical to phototropin
except that it has a phytochrome pho-
tosensory domain at the N-termi-
nal end. Neochrome responds to both
blue and red/far-red light.

phot1, while second positive curvature is mediated by questions regarding the evolution of photoreceptors as
both phot1 and phot2. Phot1 and photo2 contribute well as their physiological action.
equally to stomatal opening, while the avoidance move-
ment of chloroplasts under high light intensities is 23.1.8 PHOTOTROPIN ACTIVITY
mediated only by phot2. AND SIGNAL CHAIN
Recent evidence has also indicated a role for
phototropins in the promotion of cotyledon and leaf Participants in the phototropin signal chain are only
expansion and the rhythmic sleep movements of kidney now just beginning to ‘‘come to light.’’ Some of the
bean leaves (see Chapter 24). more important factors can be summarized as follows:
1. Autophosphorylation of phototropin plays a significant
role in the phototropic response, probably by initiating
23.1.7 A HYBRID RED/BLUE LIGHT a phosphorylation cascade. Studies employing mutants
PHOTORECEPTOR HAS BEEN of the PHOT1 gene have shown that the protein is
ISOLATED FROM A FERN apparently folded in such a way that the phospho-
rylation site is blocked by the LOV2 domain in the
A particularly interesting photoreceptor has recently
dark. Absorption of blue light by the chromophore
been isolated from the fern Adiantum capillus-veneris.
induces a change in the conformation of the pro-
Designated neochrome (formerly known as phy3),
tein so that the phosphorylation site is available and
this photoreceptor has properties of both phytochrome
active. The role of the LOV1 domain is not clear.
and phototropin (Figure 23.7). The amino acid
Mutants lacking the LOV1 domain have shown that
sequence of the amino-terminal domain shows a
LOV1 is not necessary for phosphorylation but its
significant homology to the chromophore-binding
presence does increase kinase activity.
domain of phytochrome. Furthermore, when the gene
was expressed in yeast and the purified protein was 2. Phototropins may be involved in gene regulation. No
reconstituted with a phycocyanobilin chromophore, it substrates directly phosphorylated by phototropin
showed typical phytochrome photoreversible behavior. in planta have yet been identified, but there are
But neochrome also has the two LOV domains, which several proteins that interact with the photore-
bind FMN, and a serine/threonine kinase domain ceptor and are necessary for a proper response.
at the C-terminus that are virtually identical to For example, the proteins NONPHOTOTROPIC
phototropin. Neochrome is required for phototropism HYPOCOTYL 3 (NPH3) from Arabidopsis and a
in Adiantum, which is regulated by red as well as blue homologous protein (called an ortholog) from rice,
light. Neochrome is clearly a hybrid photoreceptor COLEOPTILE PHOTOTROPISM 1 (CPT1),
that mediates red, far-red, and blue-light responses. include domains that are characteristic of transcrip-
What is curious, however, is that Adiantum also has tional regulators or proteins that are involved in
two fully functional phototropins like their higher protein degradation. The mutants nph3 and cpt1,
plant counterparts and, again like their higher plant in which these proteins are missing, show no pho-
counterparts, phot2 is solely responsible for mediating totropic response.
high-light chloroplast avoidance movements. 3. Phototropin disrupts polar auxin transport. One of the
Several other ferns, mosses, and algae have both challenges presented by phototropism is to establish
phototropins and neochromes, which raises interesting whether or not a link exists between the absorption
398 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

of blue light by phototropin and the asymmetrical cotyledons (Figure 23.8), and the phototropic response
auxin distribution proposed by the Cholodny-Went of sunflower seedlings is markedly decreased if the
hypothesis. As described previously, asymmetric leaves are removed. The cucumber response, at least,
auxin distribution has been demonstrated experi- differs from the classical phototropic response in that
mentally. Recent experiments have focused on the it is induced by red light rather than blue light. This
relationship between phototropin and auxin efflux appears to be a phytochrome-mediated response and is
facilitator PIN1. PIN1 is normally localized at the related to inhibition of hypocotyl elongation below the
basal ends of xylem-associated cells where it irradiated cotyledon. Both the cucumber and sunflower
serves to facilitate the polar vertical flow of auxin responses may be attributed to the fact that the leaves
(Chapter 18). When the location of PIN1 in Arabi- are a prime source of auxin required for the growth
dopsis hypocotyls was monitored by immunofluore- response. Both cucumber and white mustard (Sinapis
scence microscopy following phototropic stimulus, alba) also exhibit a classical phototropic response
the basal location of PIN1 in wildtype plants induced by irradiating the hypocotyls directly with blue
was disrupted in the cortical cells on the shaded light. Clearly the control of stem growth in green plants
side of the hypocotyl. A similar disruption was is an area where there is still much to learn.
not observed in phot1 mutants. These results
suggest that phototropic bending is initiated by
a phototropin-mediated decrease in the vertical
transport of auxin. This would lead to a retention
or sequestering of auxin, and consequent increased
23.2 GRAVITROPISM
growth, in those cells that are directly involved in Gravitropism is probably one of the most unfailingly
phototropic bending. obvious and familiar plant phenomena to most people
(Figure 23.9). Everyone is aware that shoots always
grow ‘‘up’’ and roots always grow ‘‘down.’’ Or do they?
23.1.9 PHOTOTROPISM IN GREEN A casual walk through the woods or garden should
PLANTS IS NOT WELL reveal how overly simplified this view is. The lateral
UNDERSTOOD branches of most trees and shrubs do not grow up; they
grow outward in a more or less horizontal position.
A final area of concern is phototropism in light-grown
Stolons (or runners) of strawberry (Fragaria) plants and
plants, where relatively little is known about the
buttercups (Ranunculus) also grow horizontally along
phototropic process. As with phytochrome, discussed in
the soil surface. Dig into the soil and you will find
Chapter 22, most of what we know about phototropism
rhizomes (underground stems) and many roots growing
is derived from laboratory studies with etiolated seed-
horizontally. Many pendulous inflorescences show no
lings. However, in light-grown cucumber (Cucumis
directional preference for growth, but hang down simply
sativus) and sunflower (Helianthus annuus) seedlings
of their own weight.
subjected to uniform lighting, curvature of the
stem can be induced by simply shading one of the

FIGURE 23.8 Curvature in cucumber (Cucumis sativus)

seedlings induced by shading cotyledons. The left-hand FIGURE 23.9 Gravitropism in maize (Zea mays) seedlings.
cotyledon was covered with aluminum foil and the Four-day-old dark-grown seedlings were placed in the
seedling uniformly irradiated with white light for 8 horizontal position for 3 hours. Note the shoot exhibits
hours. (After Shuttleworth, J. E., M. Black. 1977. Planta negative gravitropism and the root exhibits positive grav-
135:51.) itropism.
 23.2 Gravitropism 399

Unlike most other environmental stimuli, the force Principal Shoot Axis
of gravity is omnipresent and nonvarying. It does not (negative orthogravitropic)
vary in magnitude as temperature does, for example.
Gravity cannot be turned on and off, such as light at
dawn and dusk. Moreover, gravity is not a unilateral
stimulus— there is no gradient component in gravity. Branches
(plagiogravitropic)
Cells on the lower side of a stem or root are subjected to (diagravitropic)
the same gravitational force as those on the upper side.
Consequently, it is likely that gravity can be detected
only by the movement of some structure or structures
within the cells—a movement that establishes an initial
asymmetry in the cell and is translated in terms of Soil level
pressure. The mass and movement of whatever structure
is involved must be consistent with the sensitivity and Rhizome
speed of the gravitational response and there must be (diagravitropic)
a mechanism for transducing the pressure signal into a Tertiary Roots
(plagiogravitropic,
biochemical signal that can lead to a differential growth or agravitropic)
response. Secondary Roots
(plagiogravitropic)

Primary Root
(positive orthogravitropic)
23.2.1 GRAVITROPISM IS MORE THAN
SIMPLY UP AND DOWN FIGURE 23.10 Diagram illustrating the range of gravit-
It is true that the root and shoot of the primary plant ropic responses in shoots and roots. Note that differences
axis do align themselves parallel with the direction in the gravitropic behavior among different levels of both
of gravitational pull. Such an alignment is said to shoot and root branches ensures the plant fills space.
be orthogravitropic. The primary root, which grows
toward the center of the earth, exhibits positive gravit-
ropism. The shoot, which grows away from the center
of the earth, exhibits negative gravitropism. Organs helps to reduce mutual shading and ensures a more
such as stolons, rhizomes, and some lateral branches, efficient capture of sunlight to drive photosynthesis.
which grow at right angles to the pull of gravity, are
said to be diagravitropic. Organs oriented at some
intermediate angle (between 0◦ and 90◦ to the vertical)
23.2.2 THE GRAVITATIONAL STIMULUS
are said to be plagiogravitropic. Lateral stems and lat- IS THE PRODUCT OF INTENSITY
eral roots are commonly plagiogravitropic. Organs that AND TIME
exhibit little or no sensitivity to gravity are said to be Gravitational stimulation (stimulus quantity or dose) is
agravitropic. the product of the intensity of the stimulus and the time
The advantages to the plant of positive and nega- over which the stimulus is applied:
tive gravitropic growth responses are fairly obvious.
Seeds may assume a random orientation in the soil, but d=t·a
in order to ensure survival, the shoot, with its photo- where a is the acceleration of mass due to gravity
synthetic structures, must be above ground in order (in g), t is the time (in seconds) over which the stim-
to take advantage of sunlight. The root system must ulus is applied, and d is the dose in g seconds (g z s)
remain in the soil in order to secure anchorage and a (see Box 23.1: Methods in the Study of Gravitropism).
reliable supply of nutrients and water. The primary root The minimum dose required to induce gravitropic cur-
most often exhibits a strongly positive orthogravitropic vature is called the threshold dose. Threshold dose will
response. Secondary roots (i.e., first-level branch vary depending on the organism or experimental con-
roots), however, tend to grow more horizontally ditions. Values of d in the range of 240 g · s (at 22.5◦ C)
while tertiary roots are generally agravitropic. This to 120 g z s (at 27.5◦ C) have been reported for Avena
hierarchy of gravitational responses ensures that the coleoptiles, but more careful mathematical analyses sug-
root system more effectively fills the available space gest that less than 30 g · s (i.e., an acceleration of 1 g for
and thus more efficiently mines the soil of water less than 30 seconds) is sufficient to induce gravitropic
and nutrients (Figure 23.10). In a similar fashion, a curvature in roots. Three other parameters are of inter-
hierarchy of negative orthogravitropic, diagravitropic, est when defining gravistimulation: presentation time,
and plagiogravitropic responses in the shoot system reaction time, and threshold intensity.
400 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

Qc Qc
BOX 23.1 the horizontal axis. This does not actually extinguish the
gravitational field, of course, but the summated effect is
Qc
Qc
CI
CI CI CI

S1

S2
S1 S1 S1 METHODS IN THE a nondirected constant stimulation. With the clinostat,
STUDY OF
S2
S2 S2

S3

S3 S3
S3
plants can first be subjected to a brief stimulus and then
GRAVITROPISM rotated to, in effect, remove any further stimulus. As
might be expected, continuous multilateral stimulation
has been found to influence a variety of physiological
parameters. Avena seedlings, for example, respond with
A fundamental requirement for any form of scientific increased growth rate and increased respiration. Some
experimentation is that of controlling the application of of these changes may be incidental, but others may
the stimulus in the form of intensity (or concentration) influence the gravitropic response. Results must always
and duration. Since the gravitational field of earth cannot be interpreted with caution.
be extinguished (except in the microgravity conditions
of space), experimentation on gravitational effects on
plants and other organisms has required some unique SPACE—THE FINAL FRONTIER
approaches.
Most experiments require a mass acceleration in the The advent of space flight in the 1950s has pro-
range of 1 g or less, which can easily be achieved by vided plant scientists with unique opportunities to study
simply orienting the organ (e.g., a coleoptile or primary responses to microgravity conditions. Since 1960, when
root) away from the vertical. The force (at least for the first wheat and maize seeds were carried aloft on
short-term stimulation) is generally proportional to the Sputnik 4, experiments with plants have been con-
sine of the angular deviation from the vertical. Thus ducted on manned and unmanned spacecraft from both
the force is greatest in the horizontal position since sine the United States and the Soviet Union (now Rus-
90◦ = 1 (the sine of angles less than 90◦ is less than 1). sia). Perhaps not unexpectedly, physiological effects
Seedling shoots generally must be oriented between 0.5◦ of microgravity are not limited to gravitropism but
to 10◦ from the vertical in order to induce curvature. embrace a variety of other cellular events. Many of
Forces greater than 1 g can be achieved by the use the effects are deleterious, including reduced growth,
of specially designed centrifuges. Similar centrifuges chromosomal aberrations, and other cytological abnor-
have been used earlier in the century for studying the malities. Death at the flowering stage was common
properties of animal (egg) membranes, and so forth. until, in 1982, Arabidopsis thaliana were successfully car-
Centrifugation has not been used extensively in the ried through a complete life cycle and produced viable
study of gravitropisn, but those experiments in which it seed. Many of the difficulties could be attributed simply
has been used have provided some useful insights. to the logistics of trying to maintain plants in space, but
The problem of extinguishing gravitational forces even with improved methods, difficulties are still being
has been approached in two ways: clinostats and space encountered. As yet the returns may be modest, but the
flight. A clinostat is a device that holds the plant axis in a use of microgravity as an experimental tool is ripe for
horizontal position while continuously rotating it about exploitation.

The minimum duration of stimulation required to sequence that leads to the asymmetric growth response.
induce a curvature that is just detectable is known as the Typically, 10 minutes is required before curvature can
presentation time. The intensity of stimulation should be visually detected, although reaction times may vary
also be defined, although a stimulus of 1 g at 90◦ is more from a few minutes to hours, depending on the species
or less standard. A force of 1 g is easily obtained by simply and conditions. In experiments employing sensitive elec-
placing the stem or root in a horizontal position. Presen- tronic position-sensing transducers, curvature of maize
tation times of 12 seconds for cress roots and 30 seconds coleoptiles could be detected within about 1.5 minutes
for Avena coleoptiles have been determined, but a brief of horizontal placement, while bending of the mesocotyl
1-second stimulus will induce curvature in Avena coleop- could not be detected before 3.5 minutes.
tiles if the stimulus is repeated every 5 seconds. This The minimum stimulus intensity required to induce
suggests that some cumulative receptive process begins a response is known as the threshold intensity. Thresh-
the instant the plant assumes a horizontal position. old intensities have been determined for a variety of
Presentation time should not be confused with reac- plant organs under different experimental conditions.
tion time, which is the interval between the presentation The results are remarkably consistent and indicate that
of the stimulus and the actual development of curvature. roots are perhaps an order of magnitude more sensi-
Reaction times involve the complete signal transduction tive than shoots. In land-based clinostat experiments
 23.2 Gravitropism 401

H+ H+

N
N Ca2+ Ca2+

PERCEPTION TRANSDUCTION TRANSMISSION RESPONSE

FIGURE 23.11 The four phases of root gravitropism. When the orientation of a root
changes in a gravitational field, the change is perceived in the root cap by the settling
of amyloplasts against intracellular membranes such as the endoplasmic reticulum.
The biophysical signal is then converted to a biochemical signal through second mes-
sengers such as hydrogen ions, calcium ions, and the relocation of auxin transport
facilitators (red circles). The signal is then transmitted to the elongation zone of the
root via an altered flow of auxin (arrows) which results in the curvature response. N
= nucleus.

(see Box 23.1), values for threshold intensity for Avena A third function, that of gravity perception, has
coleoptiles and roots were found to be 1.4 × 10−3 g and been established by experiments in which the root cap
1.4 × 10−4 g. Values calculated for lettuce seedling is wholly or partially surgically removed (Figure 23.12).
hypocotyl and roots in experiments aboard the Salyut 7 Complete removal of the root cap does not interfere with
spacecraft were 2.9 × 10−3 g and 1.5 × 10−4 g, respec- the elongation of the root but completely abolishes any
tively. It is apparent that many plants are very sensitive gravitropic response. Decapped roots will recover sen-
to gravitational stimulus. sitivity to gravity after about 24 hours, which correlates
with the regeneration of a new cap. Surgical experiments
23.2.3 ROOT GRAVITROPISM OCCURS have also indicated that removal of the central core, or
IN FOUR PHASES columella, cells caused the strongest inhibition of the
response to gravity. Individual cells or pairs of columella
Virtually all of the studies on root gravitropism have cells can be selectively removed or ablated (L. ablatus, to
focused on primary roots and have identified four suc- take away) with a nitrogen laser, in conjunction with an
cessive phases: perception, transduction, transmission, optical microscope. Ablation of the innermost columella
and growth response (Figure 23.11). Although the actual cells has the greatest impact on root curvature, without
timing may vary depending on the conditions of the affecting overall growth rate of the root (Figure 23.13).
experiment, the initial perception phase occurs within Laser ablation of the root cap peripheral cells, on the
perhaps one second of orienting a root off the vertical other hand, has no effect on the gravitropic response.
and involves biophysical mechanisms (e.g., pressure) for
sensing the direction of gravitational pull. The trans-
duction phase, occurring between 1 and 10 seconds
following reorientation, involves the conversion of the
biophysical single to a biochemical signal. The transmis-
sion phase occurs between 10 seconds and 10 minutes
of reorientation and involves a redistribution of auxin
within the root tip. The growth response, due to the
unequal distribution of auxin, causes curvature of the
root toward a more vertical orientation. A.

23.2.3.1 Gravity is perceived by the columella

cells in the root cap. Gravitropic perception in the
root is localized in the root cap, a thimble-like mass of
cells that covers the tip of the root. The root cap consists
of a central core of cells (the columella) arranged in B.
regular tiers and one or more outer layers of peripheral FIGURE 23.12 The role of the root cap in curvature of
cells. Traditionally, the function of the root cap was vertically oriented roots. (A) Control root. Growth is
thought to be twofold; it provides physical protection uniform when the root cap is left intact. (B) When the
for the root apical meristem and its peripheral cells root cap is surgically removed from one-half of the
secrete a mucilaginous polysaccharide that lubricates root, the root grows toward the side with the cap
the path of the growing root. remaining.
402 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

amyloplast (Figure 23.14). There may be 1 to several

individual grains within an amyloplast and as many as a
dozen amyloplasts in each statocyte. This compares with
the single large grains characteristic of starch storage
organs. Not all amyloplasts in all cells are readily mobile.
In fact, detection of putative statoliths, or readily mobile
Qc Qc Qc
CI
Qc amyloplasts, appears to be largely confined to regions of
CI CI CI high gravitropic sensitivity. These include the mass of
S1 columella cells in the central core of the root cap and, in
S1 S1 S1
hypocotyls, a zone of endodermal cells that sheath the
S2 S2
vascular tissues (also referred to as the starch sheath).
S2 S2 Mobile amyloplasts may also be found in the inner
S3 cortical cells of aerial organs and the pulvini, or motor
S3 S3
S3 organs in the nodes of grass stems that are responsive to
gravity.
Any gravity-sensing mechanism involving particle
FIGURE 23.13 Diagram of an Arabidopsis root cap show- sedimentation would have to operate with a speed and
ing the quiescent center (QC), columella initials (CI), sensitivity consistent with the known speed and sensitiv-
and three ranks of columella cells. Colored cells indicate ity of the response. In the 1960s, L. J. Audus undertook
the cells that are sensitive to gravistimulation, based on a careful examination of various subcellular particles.
laser ablation experiments. Relative sensitivity is indi- Audus concluded that, of all the cellular organelles, only
cated by the intensity of color. (Based on Perbal and starch grains have the mass and density to move through
Driss-Ecole, 2003). the viscous cytoplasm within known presentation times.
Ultrastructural examination has shown that other cel-
lular organelles, such as the endoplasmic reticulum,
23.2.3.2 Gravity perception involves displace- may become shifted in cells subjected to gravitational
ment of starch-filled amyloplasts. A response to
gravity must almost certainly involve sedimentation
of some physical structure within the cell. F. Noll
was the first to suggest, in 1892, that plants might
sense gravity in a manner similar to some animals.
Crustaceans, molluscs, and many other invertebrates
have gravity-sensing organs called statocysts, small
innervated cavities lined with sensory hairs. Within
the cavity are one or more statoliths, tiny granules of Nucleus
sand or calcium carbonate that are pulled downward
by gravity. When the statocyst changes position, the
statoliths also shift position, bending the sensory hairs
and sending an action potential to inform the central Mitochondria
nervous system of the change. Cell wall
In 1900, G. Haberlandt and E. Nemec indepen- Amyloplasts
dently adapted the statolith theory to account for plant
responses to gravity. Based on careful cytological stud-
ies, they proposed the starch-statolith hypothesis in
which starch grains found in specialized tissues func-
tion as statoliths. Statocytes are cells containing sedi-
mentable starch grains. Tissues that contain statocytes Endoplasmic
reticulum
are known as statenchyma. Support for the statolith
hypothesis was found in earlier reports by Darwin and
others that removal of the root tip, where most of the
starch grains are found, resulted in a loss of gravit- FIGURE 23.14 A statocyte (columella cell) containing
ropic response. Nonetheless, the hypothesis was not three statoliths (amyloplasts). (Based on an electron
universally accepted and over the decades a number of micrograph of Lepidium root, Volkmann and Sievers,
investigators have attempted to prove or disprove it. 1979. In W. Haupt, M. E. Feinleib (eds.), Encyclope-
A statolith is not a naked starch grain, but a group dia of Plant Physiology, NS, Vol. 7, pp. 573–600. Berlin:
of starch grains contained within a membrane, called an Springer-Verlag.)
 23.2 Gravitropism 403

stimulus, but these movements are thought to be a con- is important. The preferred view is that the statolith
sequence of starch grain sedimentation. Although there exerts pressure on one or more membranes or other cel-
is still no direct proof for the starch-statolith hypothesis, lular components. Although there is no direct evidence
there is a large body of evidence that is more consistent for pressure-sensitive membranes in plants, both the
with that idea than any other that has been put forward plasma membrane and the endoplasmic reticulum (ER)
to date. This evidence is summarized below: have been suggested as likely targets. Electron micro-
graphs of gravistimulated root statocytes, for example,
1. Gravitropism is generally absent in plant species that commonly show amyloplasts sedimented on the endo-
have no starch grains or amyloplasts. In lower plants plasmic reticulum against the lower side of the cell
such as algae and fungi, excess carbohydrate may (Figure 23.14).
not be stored as starch. In these cases, some other
substance may function as statoliths. In the alga 23.2.3.3 The transmission and response phases
Chara, for example, the role of starch grains is involve a lateral redistribution of auxin in the
replaced by granules of barium sulphate. elongation zone. Like phototropism, development
2. There is a strong correlation between the rate of starch of curvature in response to gravity ultimately involves a
sedimentation and presentation time. In sweet pea differential growth response. It is not surprising, then,
(Lathyrus odoratus), for example, there is a parallel that the Cholodny-Went hypothesis of asymmetric
increase in both sedimentation time and presenta- auxin distribution has dominated thinking and research
tion time as the temperature is lowered from 30◦ C into gravitropism for more than 60 years. Accordingly,
to 10◦ C. The decline in both is presumably related the hypothesis states that horizontal orientation of the
to an increase in protoplasmic viscosity. shoot or roots induces a lateral translocation of auxin
3. Loss of starch by hormone treatment or mutation is toward the lower side of the organ. Auxin redistribution
accompanied by a loss of graviresponse. For example, would bias the growth rate in favor of the lower side
roots of cress seedlings (Lepidium sativum) treated such that negatively gravitropic organs (e.g., coleoptiles
with cytokinin or gibberellin at 35◦ C become and shoots) would turn upward. In positively gravitropic
starch-free in 29 hours. The growth rate of treated organs such as roots, the higher concentration of auxin
roots is reduced only slightly (0.48 mm h−1 vs. is thought to inhibit elongation on the lower side relative
0.64 mm h−1 ) but any response to gravity is to the upper, causing the organ to grow downward.
completely eliminated. Transfer of the roots to Exogenous auxin, for example, very effectively inhibits
water in the light results in a parallel recovery of root growth when applied at concentrations of 10−6
both amyloplasts and gravitropic responsiveness M or greater, concentrations that normally stimulate
after 20 to 24 hours. In maize (Zea mays) the elongation of coleoptiles and shoots. In addition,
amylomaize mutant produces smaller amyloplasts gravitropic curvature is prevented by inhibitors of auxin
than the wildtype. In studies of the percentage transport (TIBA, NPA).
and speed of amyloplast sedimentation the degree Auxin flow in the root is described by the ‘‘auxin
of coleoptile curvature was strictly correlated fountain model’’ (Figure 23.15). Auxin synthesized in the
with the size of the amyloplast. Another mutant shoot is transported basipetally through the shoot and
of maize, hcf-3 (high chlorophyll fluorescence-3) is into the root. There it continues to move acropetally
unable to carry out photosynthesis and thus can toward the root tip through cells associated with the
form no starch in the leaf base statocytes when the central vascular tissues, or stele. In the columella region
endosperm reserves have been exhausted. Such of the root cap, the auxin flow is reversed and the auxin
seedlings do not respond to gravity unless fed moves basipetally into the cortical cells of the elongation
sucrose, in which case recovery of both amyloplasts zone (Figure 23.15A). In a vertical root the flow of
and sensitivity to gravity was noted. auxin into the cortical region is distributed uniformly
4. Amyloplasts can be displaced by a high-gradient magnetic around the root. When the root is displaced horizontally
field in place of gravity. An intracellular magnetic field (Figure 23.15B), the flow of auxin from the columella is
has been used to displace statoliths laterally (called redistributed laterally (i.e., downward). In other words,
magnetophoresis) in both roots and hypocotyls. The auxin flow in a horizontal root is biased toward the lower
magnetic field also induces a curvature similar to the side of the root. The implication is that the higher auxin
gravitropic response. content on the lower side of the root inhibits elongation
relative to the upper side and the root curves downward.
It is not known how the sedimentation of statoliths
creates physiological asymmetry in the cell or tissue, 23.2.3.4 Gravitropic induction in roots involves
although a number of models have been proposed. Most several second messengers and redistribu-
models agree that it is not the change in position of tion of auxin transporters. An early event in
the statolith or the process of movement per se that gravity-stimulated roots is a change in the membrane
404 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

FIGURE 23.15 The path of auxin flow in roots.

C S C
Auxin produced in the shoot flows into the
root through the central vascular tissue. In the
columella (yellow square), the auxin stream is
diverted into the epidermal and cortical cell files,
where it flows up toward the elongation zone.
When the root is displaced from the vertical, Elongation
events in the columella divert the main auxin flow
toward the lower side of the root. C

Auxin inhibits
elongation

A. B.

potential of the columella cells. Within seconds of prevented in horizontal organs treated with the auxin
reorienting Lepidium sativum roots to a horizontal transport inhibitor NPA. Histochemical techniques
position, the columella cells on the lower side of the have demonstrated calcium localization in cells of
root depolarize (the potential becomes less negative) the upper epidermis and underlying parenchyma
and those on the upper side hyperpolarize (the potential of Avena coleoptiles within 10 minutes of gravis-
becomes more negative). These changes in membrane timulation. In addition, both calcium redistribution
potential appear to be in some way related to the and gravitropism are prevented by prior treatment
cytoskeleton because they are inhibited by cytochalasin with EGTA (ethyleneglycol-bis-(β-aminoethyl ether)-
D, a drug that disrupts the cytoskeleton by binding N,N -tetraacetic acid), a chelator that ties up free
to rapidly elongating actin filaments. There is also calcium, and the graviresponse of coleoptiles is
evidence that amyloplasts are connected to the plasma prevented by treatment with chloropromazine, an
membrane by actin filaments. These observations inhibitor of the calcium-binding protein calmodulin.
have given rise to the hypothesis that displacement of This suggests that the response to gravity might at one
amyloplasts stimulates stretch-activated ion channels. stage involve a Ca2+ /calmodulin complex.
Stretch-activated channels are so named because they Experiments with exogenously applied calcium have
are activated in patch-clamp experiments when the provided equally convincing evidence of a role for cal-
membrane is stretched by applied suction. According to cium in root gravitropism. For example, asymmetrically
this hypothesis, stretch-activated ion channels would applied agar blocks containing 10 mM CaCl2 will induce
be responsible for the observed changes in membrane curvature of maize roots, but only if the block is applied
potential in the columella cells, which in turn would to the root tip (Figure 23.16). Migration of calcium in
lead to the asymmetric distribution of auxin. roots appears to be restricted to the root cap—migration
Changes in the pH of columella cells have also is prevented if the cap is removed—and is directed
been observed in gravity-stimulated roots. By using toward the lower side of the horizontal root. More-
pH-sensitive fluorescent proteins to monitor changes over, the calcium appears to move not through root
in pH during gravistimilation of Arabidopsis root, it has cap cells but through the thick mucilaginous layer that
been shown that pH of the root cap apoplast decreases coats the root cap. The importance of this mucilaginous
from pH 5.5 to 4.5 within 2 minutes of gravistimu- coating is reflected in the observation that its contin-
lation. Conversely, the cytoplasmic pH of columella ual removal by washing renders the root insensitive to
cells increases slightly, from pH 7.2 to pH 7.6. These gravity. Note that the direction of calcium asymmetry
pH changes in the root cap precede auxin-related pH relative to auxin is opposite in gravistimulated coleop-
changes in the elongation zone by about 10 minutes. tiles and roots. In both organs, calcium migrates toward
Several investigators have highlighted a role for the potentially concave side. Thus in a horizontally ori-
calcium in the gravity response of both coleoptiles ented root, calcium moves downward to accumulate on
and roots. Radio-labeled calcium (45 Ca) accumulated the lower side of the root cap but it moves toward the
in the upper half of sunflower hypocotyls and maize upper side of a coleoptile. The source of this calcium
coleoptiles within one hour of stimulation by gravity. is unknown, but it could be released from the ER as
Calcium redistribution also occurred following the result of an interaction between the amyloplasts and
asymmetric application of exogenous IAA and could be the ER.
 23.3 Nastic Movements 405

A B

A.

B.

FIGURE 23.17 The expression and distribution of the

auxin transport facilitator PIN2 in vertical (A) and grav-
istimulated (B) roots. In vertical roots PIN2 is located
more or less symmetrically throughout the peripheral
root cap, epidermis, and cortex, mediating the basipetal
C. flow of auxin toward the cell elongation zone uniformly
FIGURE 23.16 Calcium-induced curvature of the primary around the root. In gravistimulated roots, enhanced
root of maize (Zea mays). (A) An agar block containing degradation of PIN2 at the upper side of the root biases
calcium placed on the side of the root in the elongation PIN2 location to the lower side.
zone has no effect. (B) When the agar block contain-
ing calcium is applied to the root tip, the root grows
toward the source of calcium. (C) An agar block contain- proteasome-dependent degradation. Gravistimulation
ing EGTA, a calcium chelator, causes the root to grow in apparently leads to an increased rate of PIN2 degra-
the opposite direction. dation in the upper side of the root. At the same time,
higher auxin levels were found to promote increased
retention of PIN2 in the lower side of the root. This
Finally, and perhaps not unexpectedly, recent exper- unequal distribution of PIN2 would thus help to main-
iments in which the PIN proteins were linked to a green tain the auxin gradient originally established by PIN3
fluorescent protein and examined microscopically have in the columella cells.
demonstrated that the auxin fountain and root grav- But how does a root straighten out when it once
itropism depend on the coordinated distribution and again approaches a vertical orientation? It turns out that
activities of the auxin efflux facilitators PIN1, PIN2, auxin can also promote the degradation of PIN2. It has
and PIN3 (Figure 23.17). PIN1 is localized at the apical been proposed that as auxin levels continue to build
end of cells in the stele and is responsible for deliver- up in the lower side of the root, concentrations even-
ing the auxin stream to the root apex. PIN3 is located tually reach a threshold where auxin-mediated PIN2
along the lateral wall of the columella cells in a verti- degradation begins to reduce auxin transport toward the
cally oriented primary root, where it diverts the flow of elongation zone, thus reducing further curvature.
auxin laterally, or centrifugally, toward the peripheral The big unresolved question at this time, of course,
root tissues. PIN2 is located primarily on the basal walls is how the settling of amyloplasts in response to gravity
of the peripheral root cap, epidermal, and cortical cells induces changes in pH, calcium flux, and other second
where it mediates the basipetal stream of auxin toward messengers and how these changes are all linked to
the cell elongation zone. The importance of PIN2 in changes in the distribution and activity of the auxin
gravitropism is indicated by the observation that pin2 transport proteins.
mutants fail to establish the required lateral auxin dis-
tribution following gravistimulation and do not exhibit
a normal gravitropic response. 23.3 NASTIC MOVEMENTS
When a vertical root is rotated to the horizon-
tal position, two significant events occur. First, PIN3 In addition to the directed movements of tropisms,
becomes redistributed, accumulating along the lower many plants and plant parts, especially leaves, exhibit
sidewalls of the columella cells. This redistribution of nastic movements, in which the direction of movement
PIN3 presumably diverts the incoming auxin toward the is not related to any vectorial component of the stim-
lower side of the root. Second, PIN2 becomes asym- ulus. Nastic responses may involve differential growth,
metrically distributed between the upper and lower sides in which case the movement is permanent. Alterna-
of the root. The evidence suggests that the PIN2 pro- tively the movement may be reversible, caused by turgor
tein is rapidly turned over due to ubiquitination and changes in a specialized motor organ.
406 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

Epinasty and thermonasty are examples of nastic occurs at the base of the petiole (primary pulvinus),
responses involving differential growth. Epinasty is the the pinna (secondary pulvinus), or the pinnule (tertiary
downward bending of an organ, commonly petioles pulvinus). The pulvinus contains a number of large,
and leaves whose tips are inclined toward the ground. thin-walled motor cells, which alter the position of the
It is not a response to gravity, however, but appears leaf by undergoing reversible changes in turgor.
to depend on an unequal flow of auxin through the
upper and lower sides of the petiole. Epinasty is also a
common response to ethylene or excessive amounts of
auxin. The reverse response, called hyponasty, is less 23.3.1 NYCTINASTIC MOVEMENTS
common but can be induced by gibberellins. A typical ARE RHYTHMIC MOVEMENTS
example of thermonasty is the repeated opening and INVOLVING REVERSIBLE
closure of some flower petals, such as tulip and crocuses. TURGOR CHANGES
In spite of their repeated nature, however, thermonastic Nyctinastic movements (Gr. nyctos, night + nastos = clo-
movements are permanent and result from alternating sure) are most evident in leaves that take up a different
differential growth on the two surfaces of the petals. position in the night from that taken during the day.
The most dramatic nastic movements are all turgor Typically leaves or leaflets are in the horizontal, or open,
movements, which may be broadly separated into position during the day and assume a more vertical, or
three categories: (1) leisurely rhythmic leaf movements closed, orientation at night. The primary leaf of com-
in nyctinastic plants, (2) very rapid seismonastic mon bean plants exhibits particularly strong nyctinastic
movements in a limited number of species, and movements but this can also be seen in Coleus, prayer
(3) thigmonastic or thigmotropic curling of threadlike plants, and other common garden and house plants.
appendages in climbing plants and vines. Nyctinastic Observations of nyctinastic movements can be traced
and seismonastic responses depend on differential back as far as the writings of Pliny in ancient Greece.
turgor movements in specialized motor organs, called The Swedish botanist C. Linnaeus (in 1775) coined the
the pulvinus (pl. pulvini). The pulvinus is a bulbous term ‘‘plant sleep’’ to describe nyctinastic movements
structure most often encountered in plant families and they are commonly referred to as sleep movements
characterized by compound leaves, such as the Legumi- today. The sleep movements of bean were prominent in
noseae and Oxalidaceae (Figures 23.18 and 23.19). It the discovery of endogenous biological clocks and are
described further in Chapter 24.
Sleep movements have been studied by several
eighteenth- and nineteenth-century botanists, includ-
ing Darwin. The process, however, has been studied
Tertiary
most extensively by Ruth Satter and her colleagues in
pulvinus Samanea samanan, a member of the Leguminoseae with
Secondary doubly compound leaves (Figure 23.18). In Samanea the
pulvinus
paired pinnae and pinnules are normally separated and
spread apart, while in closing they fold toward each
Pinna other. In Samanea, the paired pinnules fold basipetally
Pinnule
(i.e., downward), but in other species, such as Mimosa
Rachilla pudica and Albizzia julibrissin, closure of paired pinnules
Rachis
is upward, or acropetal. The doubly compound leaves
of Mimosa, Albizzia, and Samanea all have three pulvini,
but the simple leaf of Phaseolus (bean) has only two. It is
the secondary pulvinus that generally exhibits the more
rapid or dramatic change and has consequently been
studied most extensively (Figure 23.19). They are also
Primary
pulvinus relatively large (2 to 3 mm diameter, 4 to 7 mm long
in Samanea) and the changes in curvature are readily
Open Closed
visible to the naked eye.
FIGURE 23.18 A leaf of Samanea samanan, illustrating
All nyctinastic responses depend on reversible tur-
the location of primary and secondary pulvini. Activation
gor changes in the pulvinus. The pulvinus is typically
of the primary pulvinus causes leaflets to fold upward,
parallel to the rachis. Activation of the secondary pulv- cylindrical in shape, with prominent transverse furrows
inus causes the rachilla to fold downward. (Reproduced which facilitate bending, on the adaxial and abaxial sides
from the Journal of General Physiology 40:413–430, 1974, (Figure 23.19). It contains a central vascular core with
by copyright permission of the Rockefeller University both xylem and phloem surrounded by sclerenchyma
Press.) tissue. The vascular tissue assumes a linear arrangement
 23.3 Nastic Movements 407

Adaxial surface

Extensor cells Epidermis

Cortical
parenchyma
Vascular bundle

Flexor cells

A. B. Abaxial surface

FIGURE 23.19 The pulvinus. (A) Secondary pulvini of bean (Phaseolus vulgaris). The
secondary pulvinus is the swollen area (arrows) at the juncture of the petiole with
the stem, just below the axillary bud. In bean, the primary pulvinus is located at the
distal end of the petiole, where it attaches to the leaf. During closure in bean, the
petioles fold toward the stem axis while the leaf blade drops from the horizontal
to the vertical position. (B) Schematic diagram of the bean secondary pulvinus in
cross-section, showing the enlarged cortical parenchyma region. During closure, the
motor cells of the extensor region lose turgor, while the motor cells of the flexor
region gain turgor and the petiole moves toward the stem axis. During opening, the
extensor cells gain turgor and the flexor cells loose turgor, thus driving the petiole
away from the stem axis.

as it passes through the pulvinus, apparently enhanc- genous rhythms. Although the mechanism of signal
ing the flexibility of the pulvinar region. Outside the perception and how these three stimuli interact is not
vascular core is a cortex comprised of 10 to 20 layers known, it is clear that both the receptors and the
of parenchyma cells. The cells of the outer cortex have responding system (the motor cells) are located in the
thin, elastic walls and exhibit large changes in size and pulvinus—at most a few cells apart. It is known that
shape during movement. These are called motor cells. phytochrome can ‘‘reset’’ the endogenous clock that
Changes in the size and shape of the motor cells are regulates nyctinastic leaf oscillations. The relationship
responsible for leaf movement. between phytochrome and endogenous rhythms will be
The opposite sides of the pulvinus are known as discussed in the next chapter.
the extensor and flexor regions (Figure 23.19B). The
extensor region is formed by motor cells that lose turgor
during the bending movement, or ‘‘closure.’’ Motor 23.3.2 NYCTINASTIC MOVEMENTS
cells in the flexor region gain turgor during closure ARE DUE TO ION FLUXES
and lose turgor during opening. Thus, the swelling AND RESULTING OSMOTIC
of extensor motor cells and shrinkage of flexor motor
RESPONSES IN SPECIALIZED
cells straightens the pulvinus and opens or spreads apart
leaves or leaflets. The relative positions of extensor
MOTOR CELLS
and flexor regions in the pulvinus (whether adaxial or Regardless of the nature of the stimulus, motor cell
abaxial, for example) will be reversed, depending on volume changes are due to osmotic water uptake (or
whether closure is basipetal or acropetal. loss) as a result of ion accumulation (or loss) across
Nyctinastic movements are sensitive to blue light, the cell membrane. What ions are exchanged, how are
the physiological status of phytochrome, and endo- they transported, and what is the driving force for ion
408 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

movement? These questions have been approached 80

with a variety of techniques, including histochemi-
cal and radiochemical methods, and scanning electron 70
microscopy coupled with X-ray analysis. The results
show that leaf movement in all nyctinastic plants stud-
ied thus far is associated with a massive redistribution of 60
potassium ion (K+ ) between the symplast and apoplast
in both the extensor and flexor regions of the pulvinus 50
(Figure 23.20). Swollen extensor cells are characterized
by high protoplasmic K+ and low apoplastic K+ . In
Phaseolus vulgaris, fully 30 percent of the osmotic poten- 40
tial change can be accounted for by K+ movement. The
charge carried by K+ is compensated primarily by chlo-

K+ Activity (mM)
30
ride and possibly small organic anions such as malate
and citrate.
Beyond the central role of K+ flux in nastic move- 20
ments, it is difficult to pin down the specific sequence
of molecular and biophysical events in the signal chain.
10
Patch-clamp experiments with isolated Samanea motor
cell protoplasts have established that K+ exchange across
the plasma membrane occurs through K+ channels and 0
that these channels can be regulated by changing the
membrane polarity. Depolarization of the membrane 30
opens the channels and allows K+ to move out of the
cell down its electrochemical gradient. It has also been 20
established that there are pH gradients across the plasma
membranes of motor cells. In the case of open Samanea 10
pulvina, the pH of the apoplast is about 5.5 in the
flexor region and 6.2 in the extensor region. The cyto- 0
0 20 40 60 80 100
plasmic pH is approximately neutral in both regions.
Time (min)
Upon a light/dark transition (leading to closure), the
pH gradient in the extensor region dissipates while FIGURE 23.20 Changes in K+ activity in the apoplast of
extensor (upper curve) and flexor (lower curve) cells
in the flexor region the gradient increases. Although
during closure of Samanea leaflets. Loss of K+ from the
quantitative relationships between H+ flux and K+ flux
protoplasts is followed by loss of water and turgor. Clo-
have yet to be tested, H+ extrusion could contribute sure and opening were stimulated by dark and white
to the electrochemical gradient necessary to drive K+ light periods as indicated by the bar between the two
uptake. Any observed changes in membrane potential graphs. (Adapted from Lowen, C. Z., R. L. Satter. 1989.
are undoubtedly the consequence, not the cause, of the Light promoted changes in the apoplastic K+ activity
cross-membrane traffic in osmotically active ions. in the Samanea samanan pulvinus. Planta 179:412–427,
The prominent roles of K+ channels and H+ Figure 1. Copyright Springer-Verlag.)
pumps have been incorporated into the current model
for motor cell movement. A simplified version of the
model is shown in Figure 23.21. In this model, the the motor cells. The changes could be appropriately
light signal activates phytochrome (or cryptochrome), greater if restricted to the smaller population of motor
which accelerates inositol phospholipid turnover. cells. If inositol phospholipid metabolism functions in
Recent experiments have shown that light that plants as it does in animals, DAG would be expected
stimulates opening of Samanea pulvini also decreases to activate a protein-kinase C (or its plant equivalent)
the level of phosphotidylinositol 4,5-bisphosphate to phosphorylate certain proteins. IP3 would be
(PIP2 ) and increases the level of the second messenger expected to release free calcium—exogenous IP3 does
inositol 1,4,5-triphosphate (IP3 ). There is a transient liberate calcium—although from which compartment
stimulation of diacylglycerol (DAG). These changes is not known. Both the phosphorylated protein and/or
are qualitatively similar but quantitatively smaller transient increases in free calcium stimulate proton
than those normally detected in animal systems. The extrusion by activating the proton pump. The resulting
assays, however, involved whole pulvini, which contain electrochemical gradient energizes the uptake of K+
vascular, collenchyma, and epidermal tissues as well as and other ions, which in turn stimulates the osmotic
 23.3 Nastic Movements 409

+
H+ Ca2

hν
+

Pr Pfr PIP2

?
Plasma
membrane

[DAG]

− K+ C1–
2+
Cytosol [IP3] [Ca ]

Protein + ATP Protein ~ P

FIGURE 23.21 A proposed model for the interaction of phytochrome, biological
clocks, and the inositol triphosphate system in leaf movements of nyctinastic plants.
Light, mediated by phytochrome and modulated by the endogenous clock, acceler-
ates inositol phospholipid turnover and increases the level of the second messengers
inositol-1,4,5-triphosphate (IP3 ) and diacylglycerol (DAG). The second messengers
stimulate a release of Ca2+ into the cytosol and phosphorylation of various proteins
which in turn stimulate the extrusion of protons from the cell. K+ diffuses into the
cell in response to the proton motive force. An active transport pump extrudes Ca2+
as an aid to restoring Ca2+ homeostasis.

uptake of water and motor cell swelling. The presence a wider variety of stimuli including shaking or wind,
of a calcium pump that extrudes Ca2+ would help to falling raindrops, wounding by cutting, and intense heat
ensure the restoration of Ca2+ homeostasis. or burning.
Many details of this model remain to be described, The best known example of seismonastic plants is
especially the function of the inositol phospholipid cycle the tropical shrub Mimosa pudica (Figure 23.22). The
in plants. Still, plant cells are known to contain virtually survival advantage of such a response is not certain.
all the required components and the model is consistent Some have suggested that since these plants grow in
with what has been observed in pulvini thus far. Signifi- arid, exposed areas where they are exposed to drying
cant advances are to be expected in the future, especially winds, folding of the leaves may be a means of reducing
now that patch-clamp techniques—long a mainstay of water loss. Others suggest that it is a means of protection
electrophysiology research for animal cells—can be from large herbivores or insects. However, one thing is
applied to plant cell protoplasts. This state-of-the-art clear—the response is very rapid. When the pulvinus
technique has been in use for plant cells only since is stimulated directly, bending begins in less than one
about 1984, but has proven invaluable for the study of second!
ion channels. The ultimate response, leaf movement, of course
involves movement of pulvini motor cells just as in nycti-
nastic movements. However, there are three essential
23.3.3 SEISMONASTY IS A RESPONSE TO characteristics of the seismonastic response that have
MECHANICAL STIMULATION served to focus attention on the early steps of signal
transduction. The first of these is the rapidity of the
A limited number of leguminous plants that possess response. Second, seismonasty follows the ‘‘all-or-none
pulvini and exhibit nyctinastic movements also exhibit a principle,’’ which means that there is no obvious rela-
response to mechanical stimulation. This phenomenon tionship between the intensity of the stimulus and the
is known as seismonasty. Since seismonastic plants extent of the response. Third, excitation is propagated
respond to touch, they are sometimes considered from the place of stimulation. The similarity of these
thigmonastic. However, seismonastic plants respond to characteristics to animal nerve transmission has given
410 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space

A. B.
FIGURE 23.22 Seismonasty in the sensitive plant Mimosa pudica. The plant is shown
in the open (A) and closed (B) positions. The plant on the right (B) was photographed
about 10 seconds after closure was stimulated by a sharp tap to the stem with a pencil.

rise to the expectation that plants may also be capable substance has been isolated from 14 higher plants that
of transmitting stimuli in the form of potential changes. exhibit nyctinastic movements. It has been suggested
Indeed it has now been well established that virtually that turgorin may give rise to action potentials in a
any part of the Mimosa plant can perceive stimuli and manner similar to the animal neurotransmitter, acetyl-
transmit them as electric pulses to the pulvini. Although choline.
plants do not have discrete nerve tissue, it appears that
phloem sieve tubes can and do function as conduits for
signal transmission. Stimulation of the petiole results in a
rapid depolarization that is propagated basipetally along SUMMARY
the sieve tube at a rate of about 2 cm s−1 . The unique
structure of the sieve tube with its protoplasmic conti- Plant movements serve to orient the plant body in
nuity through the sieve plates appears to be well suited space. Thus roots exhibit positive gravitropism, grow-
for transmission of electrical signals. The appearance of ing down in order to mine the soil for mineral nutrients
the action potential is correlated with a rapid uptake of and water. Shoots exhibit negative gravitropism and
protons, suggesting that proton flux is responsible for positive phototropism in order to optimize the inter-
the depolarization. When the action potential reaches ception of sunlight for photosynthesis.
the pulvinus, it appears to stimulate a rapid unloading of There are several categories of plant movements.
both K+ and sugars into the apoplast. Water would fol- Growth movements involve cell division and elonga-
low and the resulting loss of turgor would cause collapse tion and are consequently irreversible. Turgor move-
of the motor cells. ments involve changes in turgor pressure and cell
Other investigators have found that substances iso- volume, and are reversible. Tropisms are direction-
lated from phloem sap of Mimosa and other species will ally related to the stimulus whereas the directionality
stimulate closure of Mimosa pulvini when applied to the of nastic movements is inherent in the tissue and are
cut end of the stem. The active substance has been iden- not related to any vector in the stimulus. Nutations are
tified as a glycosylated derivative of gallic acid (4-0-β-d- rotary or helical movements that are best observed with
gluco-pyranosyl-6 -sulphate)). Called ‘‘turgorin,’’ this time-lapse photography.
 Further Reading 411

Under natural conditions, phototropism is a response is illustrated by seismonasty in the sensi-

growth response to a light gradient, although in the tive plant Mimosa. Seismonasty involves similar turgor
laboratory it is usually studied by subjecting organs changes in response to physical disturbance.
to unilateral light. Organs may either grow toward
(positive phototropism) or away from (negative
phototropism) the higher irradiance. Phototropism CHAPTER REVIEW
is a response to blue and UV-A light; mediated by a
flavoprotein called phototropin, located in the plasma 1. Define phototropism. Is phototropism restri-
membrane. cted to unilateral lighting? In what way(s) can a
The phototropic response is characterized by dif- light gradient be established across a plant organ
ferential growth on the lighted and shaded sides of the such as a stem?
responding organ. The most generally accepted the- 2. What pigment(s) function as the photoreceptor
ory to account for differential growth in coleoptiles for phototropism? List the evidence that supports
and stems is the Cholodeny-Went theory. This the- your conclusion.
ory proposes a lateral redistribution of auxin as it flows 3. Review the experimental basis for the Cholodny-
basipetally from the apex where it is synthesized. In the Went hypothesis.
case of positive phototropism, the higher concentration 4. Shoots and roots express various levels of gravit-
of auxin flows down the shaded side of the organ, caus- ropic response. What are the physiological advan-
ing cells on the shaded side to elongate more rapidly tages to be gained by such variation in response?
than those on the lighted side.
5. Review the statolith theory for gravitropism
Unlike most stimuli to which plants are exposed, as it applies to roots. How is the gravita-
gravity is omnipresent and nonvarying. There is no tional stimulus perceived by a root and how
gravitational gradient. Gravity can be sensed only by does it respond? What is the evidence that
movement of cellular structures (statoliths), which calcium is involved in root gravitropism?
then establishes an asymmetry that is translated in
6. Describe nyctinasty. What might be the physio-
terms of pressure. Although there is no direct proof,
logical significance or survival value of nyctinasty?
the weight of evidence indicates that statoliths are the In what ways is the seismonastic response similar
starch-containing plastids, amyloplasts. to nyctinasty? In what ways is it different?
Sensitivity to gravity in the root is localized in
the columella, a group of cells in the central core
of the root cap. The primary transducer that senses
the pressure of the statoliths and initiates the sig- FURTHER READING
nal transduction chain remains unknown. Some evi-
Abas, L. et al. 2006. Intracellular trafficking and proteolysis
dence suggests it might be the endoplasmic reticulum.
of the Arabidopsis auxin-efflux facilitator PIN2 are
Another theory proposes that the sedimenting amy- involved in root gravitropis. Nature Cell Biology
loplasts activate stretch-activated ion channels in the 8:249–256.
plasma membrane. As in phototropism, the gravit- Blancaflor, E. B., J. M. Fasano, S. Gilroy 1998. Mapping
ropic response involves differential growth that can the functional roles of cap cells in the response of
be explained by redistribution of auxin transport. The Arabidopsis primary roots to gravity. Plant Physiology
steps between pressure sensing and auxin redistribu- 116:213–222.
tion are unknown, but experiments indicate that pH Brown, A. H. 1993. Circumnutations: From Darwin to space
changes, calcium ions, and inositol triphosphate may flights. Plant Physiology 101:345–348.
all be involved. Ultimately, the signal chain results in Celaya, R. B., E. Liscum 2005. Phototropins and associated
the relocation of auxin transport facilitators of the PIN signaling: Providing the power of movement in higher
plants. Photochemistry and Photobiology 81:73–80.
family.
Christie, J. M. 2007. Phototropin blue-light receptors.
Plants exhibit a variety of nastic responses. One
Annual Review of Plant Biology 58:21–45.
of the most prominent is the periodic movement of
Darwin, C. 1881. The Power of Movement in Plants. New York:
leaves known as sleep movements, or nyctinasty. Leaf
Appleton-Century-Crofts.
movement is mediated by turgor changes in special-
Esmon, C. A. et al. 2006. A gradient of auxin and auxin-
ized motor cells located in structures called pulvini, dependent transcription precedes tropic growth
found at the distal end of the petiole. Turgor changes responses. Proceedings of the National Academy of Sciences,
are mediated by a flux of potassium ion induced by an USA. 103:236–241.
interaction between phytochrome, biological clocks, Fasano, J. M., S. J. Swanson, E. B. Blancaflor, P. E. Dowd,
and the inositol triphosphate system. Another nastic T. Kao, S. Gilroy 2001. Changes in root cap pH are