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Sink strength as a determinant of dry matter partitioning in the whole plant

Article in Journal of Experimental Botany · January 1996

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 Journal of
Journal of Experimental Botany, Vol. 47, Special Issue, pp. 1281-1291, August 1996 Experimental
Botany

Sink strength as a determinant of dry matter partitioning

in the whole plant
L.F.M. Marcelis 1
OLD-Research Institute for Agrobiology and Soil Fertility (AB-OLD), PD Box 14, NL-6700 AA Wageningen,
The Netherlands

Received 14 August 1995; Accepted 21 December 1995

Abstract several crops it has been shown that the dry matter
partitioning into an organ can be quantitatively
Dry matter partitioning is the end result of the flow of
described as a function of its potential growth rate
assimilates from source organs via a transport path to
relative to that of the other plant organs.
the sink organs. The dry matter partitioning among
the sinks of a plant is primarily regulated by the sinks
Key words: Dry matter distribution, potential growth rate,

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themselves. The effect of source strength on dry
matter partitioning is often not a direct one, but indir- sink, source, translocation.
ect via the formation of sink organs. Although the
translocation rate of assimilates may depend on the
Introduction
transport path, the transport path is only of minor
importance for the regulation of dry matter parti- The term dry matter partitioning is used in various
tioning at the whole plant level. meanings. It may be defined as, for instance, the distribu-
To understand the regulation of dry matter parti- tion of dry matter between the organs of a plant, or as
tioning by the sinks, a parameter like sink strength is the distribution between different processes (e.g. synthesis
needed that describes a sink's ability to influence and hydrolysis of sugars, export, respiration, etc.) or as
assimilate import and is independent of the rest of the all the processes acting on dry matter in the plant. In this
plant. The term sink strength can be defined as the paper, the first definition will be used, where partitioning
competitive ability of an organ to attract assimilates. is, in fact, the end result of the processes acting on dry
However, there is much debate and confusion about matter. Moreover, in this paper the term partitioning will
the term sink strength because this term is often not be used in a relative sense, i.e. it refers to fractions of the
clearly defined. Sink strength has been proposed to dry matter of the whole plant: Hence, the flux of dry
be the product of sink size and sink activity. Although matter into an organ may increase while dry matter
cell number is often considered as a suitable measure partitioning into that organ does not necessarily increase.
of sink size, it appears not always to be an important Although there is considerable information on the
determinant of sink size. Moreover, sink strength may operation of individual processes in plants such as photo-
depend on sink age rather than sink size. synthesis, sugar metabolism, translocation, and cell
A model for dry matter partitioning into generative expansion, the controls which actually regulate the parti-
plant parts, which is based on sink strengths of the tioning of dry matter at the whole plant level are still
organs, is described. The potential growth rate (poten- only poorly understood (Wardlaw, 1990). Several theories
tial capacity to accumulate assimilates) has been have been put forward to explain the mechanism by
shown to be an important parameter that quantitatively which dry matter is distributed among plant organs, but
reflects the sink strength of an organ. The potential no unequivocal theory is available at present (Gifford
growth rates of the plant's organs are not static but and Evans, 1981; Wolswinkel, 1985; Farrar, 1988, 1992;
change dynamically. The potential growth rate of a Patrick, 1988; Wardlaw, 1990). Moreover, quantitative
fruit is a function of both its age and temperature. For data on dry matter partitioning within whole plants-in

1 Fax: + 31 317 423110. E-mail: [email protected].

© Oxford University Press 1996

1282 Marce/is

particular, during the generative stage of crops-are level is discussed and the concept of sink strength is
scarce (Wareing and Patrick, 1975; Marcelis, 1993a). evaluated-what is sink strength? what is its importance
In crop growth models, the dry matter partitioning and how can it be measured? Finally, a model for dry
among plant organs is often described as only a function matter partitioning based on sink strengths of the organs
of the developmental stage of the crop (Penning de Vries is described.
and van Laar, 1982). However, this description is entirely
empirical and usually only valid under a limited range of
Effect of source on dry matter partitioning
growing conditions (Fick et al., 1975; Loomis et al., 1979;
Wilson, 1988). A source can be crudely defined as an organ that is a net
The dry matter partitioning between root and shoot exporter of carbon assimilates. Source strength refers to
has been described as a functional equilibrium between the rate at which carbon assimilates are produced. A high
root activity (water or nutrient uptake) and shoot activity source strength due, for example, to high irradiance
(photosynthesis); i.e. the ratio of root-to-shoot weight is strongly enhances the total plant growth, but information
proportional to the ratio of shoot-to-root specific activity on the effect of source strength on the partitioning of the
(Brouwer, 1963). Although in this way the ratio between assimilates among the plant organs is limited.
shoot and 'root dry weight can often be estimated fairly Ho ( 1988, 1992) concluded that assimilate supply
well in vegetative plants, the mechanism underlying this affects only the degree of competition among sinks, but
equilibrium is quite complicated and not well under- not the partitioning among sinks. Daie (1985) also con-
stood (Brouwer, 1983; Lambers, 1983; Farrar, 1992). cluded that the source seems not to control partitioning.
Furthermore, this equilibrium can only be applied to However, Wardlaw (1990) discussed that there is often
shoot:root ratios and not easily to ratios between other an hierarchy among sinks. That is, some organs (e.g.

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plant organs, because of the absence of functional fruits, seeds or underground storage organs) have priority
interdependence. and suffer less from a reduction in assimilate supply than
Dry matter partitioning is the end result of a other organs (e.g. flowers). Minchin et al. (1993) showed
co-ordinated set of transport and metabolic processes that this behaviour could be predicted by a simple model
governing the flow of assimilates from source organs via based on mass flow according to the Munch hypothesis
a transport path to the sink organs. The activities of these through the phloem and Michaelis-Menten kinetics of
processes are not static, but may change both diurnally unloading in the sinks and they (Minchin et al., 1994)
and during plant development (Patrick, 1988). applied this model to root:shoot partitioning in barley
Assimilates are produced by photosynthesis in the source seedlings. However, the reported hierarchy among organs
organs (mainly leaves). The assimilates can be stored or for assimilates is often an apparent one. A change in
transported from the source to the different sink organs weight ratio between organs with changing source
via vascular connections (phloem). The translocation rate strength does not always indicate a true change in dry
of assimilates in the phloem is often considered to be matter partitioning, for instance, the allometric relation-
driven by gradients in solute concentration or in water ship of the organs (a constant relation between the relative
or turgor potential between the source and the sink ends growth rates) might still be unchanged as discussed by
of the phloem (Ho, 1979; Wolswinkel, 1985; Lang and Farrar and Williams (1991). Equally, the effects of source
Thorpe, 1986; Patrick, 1988; Lang and During, 1991). strength might primarily be on ontogeny which may
Utilization and compartmentation of the assimilates in indirectly lead to a change in weight ratios (Terry, 1968).
the sink are important to maintain these gradients. The Organ initiation often decreases and organ abortion
control of dry matter partitioning may be at the source, increases with decreasing source strength (Wardlaw,
at the sink and/or at the transport path. However, several 1990). As a consequence in the long term the number of
authors have found indications that dry matter parti- sink organs may change considerably and hence the dry
tioning among sink organs is primarily regulated by the matter partitioning.
sinks themselves (Evans, 1975; Gifford and Evans, 1981; In cucumber no noticeable relationship between the
Farrar, 1988; Ho, 1988; Verkleij and Challa, 1988), partitioning of dry matter into the fruits and solar radi-
In this paper, partitioning is studied at the whole plant ation of the same day or week was observed during a
level because regulation that may occur in one region of growing season (Liebig, 1978; Marcelis, 1992a). However,
the plant is not isolated from the other parts of the plant a large change in solar radiation seemed to induce a
(Daie, 1985). Furthermore, it is more likely that a series change in dry matter partitioning to the fruits, but the
of events rather than a single limiting event controls time lag between the change in radiation and the change
partitioning (Wardlaw, 1990). Emphasis is put on the in partitioning was variable (Marcelis, 1992a). That the
partitioning into generative plant parts. The importance direct effect of irradiance on dry matter partitioning is
of the source, the transport path and the sinks in the limited, is substantiated by an experiment where cucumber
regulation of dry matter partitioning at the whole plant plants of identical size and with a fixed number of fruits
 Sink strength and dry matter partitioning 1283
were shaded for 4 d (Marcelis, 1993d). Total plant growth taxis is not an important factor regulating dry matter
rate decreased by 60%, but the partitioning between partitioning.
generative and vegetative growth was not significantly Generally, the phloem does not limit translocatory flux,
affected. Heuvelink (1995b) also concluded for tomato as it appears to have considerable spare transport capacity
that source strength had no direct effect on dry matter (Milthorpe and Moorby, 1969; Kallarackal and Milburn,
partitioning between generative and vegetative parts. 1984; Wardlaw, 1990; Passioura and Ashford, 1974).
However, Yoshioka and Takahashi (1979, 1981) found However, in apical meristems and young primordia the
that the distribution of 14C and dry matter to the fruits phloem may not yet be differentiated to ensure enough
decreased at increasing irradiance in tomato plants with transport capacity (Williams, 1960; Milthorpe and
a fixed number of fruits per plant. Moorby, 1969; Patrick, 1972). Despite the fact that, in
Although effects of source strength in the short term some cases, partitioning is related to the relative distance
may be limited, in the long term increased source strength between sinks and sources (Cook and Evans, 1983),
may increase dry matter partitioning into the fruits, as distance is generally not an important factor in dry matter
shown for cucumber (Marcelis, 1993d). This effect of partitioning. It has been shown that increasing the dis-
source strength on dry matter partitioning was an indirect tance between source leaves and fruits had no effect on
effect via an increase in number of fruits on the plant fruit growth in apple (Hansen, 1977) and cucumber
rather than a direct effect on dry matter partitioning (Schapendonk and Brouwer, 1984). Further evidence that
(Marcelis, 1993d). Accordingly, an enhancement of transport distance is not important in regulating dry
source strength by CO 2 enrichment during an extended matter partitioning in the whole plant was found by Gent
period increased dry matter partitioning into the fruits (1982) for soybean plants with two branches. Pod growth
for cucumber and sweet pepper (Nederhoff, 1994) and was similar for all branches whether 2 leaflets and 2 pods

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tomato (Tripp et al., 1991). However, in some experi- per node were retained on each branch or whether on
ments no effects of source strength on the dry matter one branch 1 leaflet and 3 pods and on the other branch
partitioning between fruits and vegetative parts were 3 leaflets and 1 pod per node were retained (Gent, 1982).
observed in tomato and soybean (Eg1i, 1988; Cockshull Similarly, Heuvelink (1995a) showed that in tomato
et al., 1992; Nederhoff, 1994). plants with two shoots and a shoot length of more than
In conclusion, source strength per se seems to have no 2 m dry matter partitioning between vegetative and
direct effect on dry matter partitioning. However, in the generative parts was not affected whether the fruits were
long term (weeks) dry matter partitioning may change located on only one shoot or whether the same number
because of a change in number of sinks and thus in of fruits were divided over the two shoots. Part of these
amount of machinery. According to Farrar (1992) this results can be explained by the fact that sometimes sinks
can be interpreted as source strength exerting coarse were functioning close to assimilate saturation (sink lim-
control but not fine control over dry matter partitioning. itation). The model on phloem transport proposed by
Minchin et al. (1993) showed that the transport resistance
does not affect partitioning when sinks are functioning at
saturation. In many situations plant organs may function
Effect of transport path on dry matter partitioning
close to saturation (Lambers, 1983; Hocking and Steer,
As the assimilates move from source to sink organs via 1994), which further substantiates that the transport path
the phloem, this transport system may control dry matter is normally not a dominating factor in dry matter
partitioning. According to the Hagen-Poisseuille relation- partitioning.
ship the cross-sectional area of the phloem and the length
of the phloem pathway from source to sink are important
Effect of sink on dry matter partitioning
determinants of the resistance of the transport path
(Farrar, 1992). Hence, proximity of sink and source could The partitioning of assimilates among sinks has often
be important in regulating dry matter partitioning. been suggested to be regulated primarily by the sinks
Moreover, differentiation of the phloem determining the themselves (Evans, 1975; Gifford and Evans, 1981;
vascular link and phyllotaxis may affect dry matter parti- Farrar, 1988;Ho, 1988;Verkleij and Challa, 1988). Effects
tioning. Experiments with labelled carbon have shown of sinks on dry matter partitioning have been clearly
that assimilates may be transported according to the demonstrated by experiments on several fruit crops (Heim
phyllotaxic link between sources and sinks (Wardlaw, et al., 1979; Lenz, 1979; Nielsen and Veierskov, 1988;
1968; Russell and Morris, 1983). However, when the Richardson and McAneny, 1990; Marcelis, 1993c;
source:sink balance is modified these apparent phyllotaxic Heuvelink and Buiskool, 1995): An increase in number
limitations on assimilate partitioning are readily overcome of generative sinks increased the generative:vegetative
(Wardlaw, 1968; Oparka and Davies, 1985). Hocking ratio, but decreased the partitioning into the individual
and Steer (1994) also concluded that, in general, phyllo- generative sinks. In cucumber the daily dry matter parti-
1284 Marcelis

tioning to the fruits showed a closer relationship to the 85-87% of all the carbon is considered, because 13-15%
total weight than to the total number of fruits growing is respired (Marcelis and Baan Hofman-Eijer, 1995). For
at the same time on a cucumber plant (Fig. 1). Hence fruits of other species 8-22% is respired (Blanke and
the sink strength (competitive ability to attract assimil- Lenz, 1989; Walton and Dejong, 1990; Pavel and Dejong,
ates) is not only correlated with the number of sinks, but 1993; Dejong and Walton, 1989). However, over the
also with the weight of the individual sink organs. As course of a growing season up to one-half of the gross
will be discussed later the correlation with weight of carbon produced by photosynthesis may be lost by res-
individual sink organs seems not to be a causal one. piration (Amthor, 1984). Respiration can be separated
To understand the regulation of dry matter partitioning conceptually into two functional components: mainten-
by the sinks, there has been substantial interest in a ance respiration and growth respiration (Thornley, 1970).
property of a sink, called sink strength, that determines Maintenance respiration is primarily a function of organ
this regulation. The term sink strength can be defined as weight, organ composition, temperature, and metabolic
the competitive ability of an organ to receive or attract activity (Amthor, 1984; Lambers, 1985). Growth respira-
assimilates (Wareing and Patrick, 1975;Wolswinkel, 1985; tion is, in general, linearly related to the growth rate
Farrar, 1993b). At present many discussions focus on the (Penning de Vries et al., 1974; Marcelis and Baan
question whether the concept of sink strength is a useful Hofman-Eijer, 1995). This relationship may depend on
one, or a vague and confusing concept (Farrar, 1993a). the type of organ due to differences in chemical composi-
Much confusion is due to lack of a clear definition of tion (Penning de Vries et al., 1974; Vertregt and Penning
sink strength. The actual rate of assimilate import or of de Vries, 1987). Due to linearity between dry weight
growth has often been used as a measure of sink strength increase and growth respiration, net sink strength can be
(Warren Wilson, 1972). When defined in this way, sink a good indicator for the total flux for dry weight growth

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strength in fact represents the net result of assimilate flow plus growth respiration. In those cases where the frac-
which may depend on the competitive ability of all sinks tional loss by maintenance respiration is low, for example,
on a plant and the assimilate supply (source strength). when the relative growth rate is high, net sink strength
This is not a useful measure of sink strength and it is the can also be an indicator for gross sink strength.
prime cause why some authors reject the use of the
concept of sink strength. Minchin and Thorpe (1993), Potential growth rate as a measure of sink strength
dismissing sink strength (as measured by the actual import
rate) as a misnomer, and other authors (e.g. Patrick, Wareing and Patrick (1975) and Wolswinkel (1985) sug-
1993) stated that it should be possible to identify a set of gested the potential capacity of a sink to accumulate
parameters to describe a sink's ability to influence assimil- assimilates as a measure of sink strength. This potential
ate import which are independent of the rest of the plant. capacity reflects the intrinsic ability of the sink to receive
or attract assimilates, which has also been stressed by Ho
(1988) as a critical determinant of organ growth. More
Gross versus net sink strength
precisely, the sink strength can be measured as the poten-
The carbon assimilates an organ receives are used for dry tial capacity to import assimilates into the phloem of the
weight accretion and respiration. To estimate the net gain sink region and to transport the imported substances
of carbon from the dry weight, the carbon concentration from the phloem into the cells of the sink organ
of the dry matter should be taken into account. This (Wolswinkel, 1985). The potential capacity for assimilate
concentration differs between types of plant organs accumulation of a sink can be quantified by the potential
(Vertregt and Penning de Vries, 1987), but it may be growth rate of a sink, i.e. the growth rate under conditions
fairly constant for one type of organ, as observed for of non-limiting assimilate supply. Conditions for potential
cucumber fruits (Marcelis and Baan Hofman-Eijer, 1995). growth can be created by growing plants at a high
However, Ho (1976) observed a distinct change in carbon irradiance and/or reducing the number of sinks on a
concentration of tomato leaves during ontogeny. Due to plant. Sometimes problems may arise in measuring the
respiratory losses of assimilates in the sink organ, the potential growth rate, as reported by Lieth and Pasian
absolute growth rate or the net accumulation rate of dry ( 1991) for rose leaves and Marcelis (1994) for vegetative
matter in a sink organ underestimates the total amount growth in cucumber, while in sweet pepper potential
of assimilates a sink receives. According to Ho et at. growth rate of the fruits is hardly measurable as in many
(1989) the net accumulation rate of dry matter is a fruits blossom-end rot occurs when assimilate supply is
measure of 'net sink strength', while the net gain of dry high {Marcelis, unpublished data). Potential growth rate
matter plus respiratory loss of dry matter is a measure of is not a static parameter, but may change with, for
'gross sink strength'. example, developmental stage or temperature, but not
When carbon partitioning among fruits in cucumber is with factors such as light intensity or CO 2 concentration
measured in terms of dry weight distribution on average which are assumed to affect only the availability of
 Sink strength and dry matter partitioning 1285

assimilates. During development of an organ the potential tial growth rate of the cucumber fruit when source
growth often shows a sigmoid growth pattern (Bollard, capacity is not affected (Marcelis and Baan Hofman-
1970; Dennett et al., 1978; Marcelis, 1992b). Effects of Eijer, 1993).
temperature on growth rate are often confounded with
effects of the developmental stage. Marcelis and Baan Sink strength = sink size x sink activity?
Hofman-Eijer (1993) showed that the development of a
cucumber fruit was closely related to the temperature Warren Wilson (1972) proposed that sink strength is the
sum and that the effect of temperature on the growth rate product of sink size and sink activity, which can also be
of a fruit could be separated from developmental effects stated as the product of sink weight and relative growth
by considering growth as a function of the temperature rate (RGR). Ho (1988, 1992) suggested that sink size
sum. As development is related to temperature sum, the reflects the physical constraint while sink activity reflects
growing period (in days) decreases with increasing tem- the physiological constraint upon a sink organ's assimilate
perature. The growth rate of organs usually increases import. Ho (1988, 1992) considered cell number as a
with increasing temperature (Wardlaw, 1970; Auld et al., suitable measure of sink size, and the physiological pro-
1978; Egli and Wardlaw, 1980; Dekhuijzen and Verkerke, cesses for the uptake and accumulation of imported
1986; Marcelis and Baan Hofman-Eijer, 1993), although assimilate in the sink cells as a meaningful measure of
Heuvelink and Marcelis (1989) and De Koning (1994) sink activity. However, in cucumber fruits grown at non-
did not observe a significant effect of temperature on limiting assimilate supply, a small number of cells, due
potential growth rate of tomato fruits. For cucumber to a low assimilate supply during early fruit development,
fruits it was concluded that the potential growth rate is was to a great extent compensated by an increased
a function of both its temperature sum after anthesis and expansion rate of individual cells (Marcelis, 1993b).

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the actual temperature (Marcelis and Baan Hofman- Therefore, cell number seems not to be an important
Eiier, 1993). determinant of fruit size, although fruit size often correl-
When organ growth was not limited by assimilate ates positively with cell number (Marcelis, 1993b). In
supply, the increase in growth rate with increasing temper- potato, Sattelmacher and Laidig (1991) also observed a
ature was much higher than at a lower level of assimilate positive correlation between tuber size and cell number,
supply (Wardlaw, 1970;Egli and Wardlaw, 1980; Marcelis but the growth rate seemed not to be causally related to
and Baan Hofman-Eijer, 1993); a non-limiting assimilate cell number. In addition, Bunger-Kibler and Bangerth
supply was achieved in cucumber by removing competing (1982) and Bohner and Bangerth (1988) observed an
fruits (Marcelis and Baan Hofman-Eijer, 1993), in wheat inverse relationship between cell number and cell size in
by growing grains at high irradiance (Wardlaw, 1970) or tomato fruits when parthenocarpy was induced by exo-
in soybean by growing cotyledons in vitro (Egli and genously applied hormones or when distal and proximal
Wardlaw, 1980). As the level of assimilate supply hardly fruits were pollinated simultaneously. These results indi-
affects the growing period of an organ (Dennett et al., cate that cell number is not a suitable measure of sink size.
1979; Cockshull et al., 1992; De Koning, 1994; Marcelis, According to Wardlaw (1990) sink strength may
1993b), while it affects the magnitude of the response of increase with increasing sink size, because of an associated
the growth rate to temperature, at a non-limiting assimil- increase in the size of the surface (membrane) area across
ate supply the final organ size (potential size) may increase which metabolites are transferred from the vascular
whereas at a low assimilate supply the final size may system to the zone of utilization (unloading area). As
decrease with increasing temperature. shown in Fig. lA, dry matter partitioning into cucumber
Several authors (Coombe, 1976; Ho, 1984; Jenner, fruits correlates with the total fruit weight (sink size),
1985; Patten et al., 1986) have argued that growth poten- which might indicate a correlation between sink size and
tial of sink organs is largely determined during the early sink strength. However, the size often correlates with the
development of the sink organ. However, these conclu- age of an organ, which might have led to an apparent
sions may partly be the result of effects of environmental relationship between sink size and sink strength. The
factors during early sink development on the future source actual growth rate of a cucumber fruit depended on its
capacity of the plant rather than on the future sink age rather than its size (Marcelis, 1993b). Different
strength. Marcelis (1993b) showed that assimilate supply weights of cucumber fruits were achieved by retaining 6
during ovary development in cucumber had no sub- or no competing fruits during 6, 12 or 18 d (Table 1).
sequent effects on fruit growth, except for effectsmediated Despite strong differences (> 300%) in fruit weight, a few
through the source capacity of the plants. However, days after removal of the competing fruits the small fruits
Increasing the temperature of the ovary (from 17.5 to grew almost at the potential rate, i.e. the growth rate of
27.5°C), while plant temperature was kept constant fruits which were grown without competing fruits
(17.5 °C), showed that environmental factors during early throughout. A small size was fully compensated by an
development can also have a positive effect on the poten- increased sink activity (RGR). Comparable results were
1286 Marcelis
Starck and Ubysz (1974) concluded that dry matter
0> 1.00 A partitioning into an organ was determined by its growth
c:
'c
o rate rather than its size. When the sink strength of an
~ 0.75 organ is high, its growth rate will be high and, con-
a:s
Co sequently, its size will increase. Therefore, sink strength
~ 0.50 and sink size are often intercorrelated, but sink strength
a:s
E is probably not causally related to sink size.
e 0.25
Q

0.00 ._--'-----'-----'-----'-----'-_-'-------l Model for dry matter partitioning based on sink

o 20 40 60 strengths
Dry weight of fruits on the plant (g) As discussed before, dry matter partitioning is primarily
regulated by the sink strengths of the sink organs, while
neither the source nor the transport path are dominating
0> 1.00 B
c: factors in regulating dry matter partitioning. Moreover,
'e
o
0.75
oLrl\.~ OA
~
CO~ it has been discussed that the potential growth rate may
~a:s
0'0 000
~ 0 quantitatively reflect the sink strength of an organ. Based
Co o 000 0
o 0 on these conclusions, dry matter partitioning in several
o
~a:s 0.50 0
o o crops has been modelled as a function of the potential
E o o
o o growth rates of the plant organs (Jones et al., 1980, 1989;
e
Q
0.25
o 0 Lieth and Pasian, 1991; De Koning, 1994; Grossman and
o

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0
0.00 linn n. 0 oQ 0 Dejong, 1994; Heuvelink and Bertin, 1994; Marcelis,
a 5 10 15
1994; Wermelinger et al., 1991).
In most of these models the plant is considered to
Number of fruits on the plant
consist of a set of sink organs which derive their assimil-
Fig. 1. The daily fraction of dry matter partitioned into the fruits of ates for growth from one common assimilate pool. The
cucumber as a function of total dry weight (A) or number (B) of pool with the assimilates is replenished by photosynthesis
actively growing fruits on a cucumber plant. The partitioning was in the source organs. Part of the assimilates from the
measured non-destructively on three replicate plants each day during a
growing season (redrawn from Marcelis, 1993c). assimilate pool are used for maintenance respiration and
the remaining assimilates are available for growth. Thus,
Table 1. The growth rate and relative growth rate (RGR) of maintenance respiration is assumed to have priority above
cucumber fruits at day 19 after anthesis when different fresh growth. Growth respiration of an organ is linearly related
weights were achieved by retaining six or no competing fruits on to its growth rate. The growth rates of the organs are
a plant during 6, 12 or 18 d from anthesis determined by the amount of assimilates in the assimilate
Assimilate supply was assumed not to constrain fruit growth, except pool and sink strengths of the sink organs. Differences in
when the six competing fruits were present on the plant (data are based growth rates between sink organs depend on differences
on results of Marcelis, 1993b).
in sink strengths. Hence, dry matter partitioning depends
Duration of Weight a Growth rate" RGR a on the sink strengths. Using potential growth rate as a
competition (d) (g) (g d -1) (g g-l d-1) measure of sink strength, the fraction of dry matter
0 1393 a 52 a 0.038 a
partitioned into each sink is proportional to its potential
6 1209 b 49 ab 0.040 a growth rate relative to the total potential growth rate of
12 670 c 49 ab 0.072 b all sinks together.
18 395 d 40 b 0.102 c
Continuous (19 d) 356 d 12 c 0.034 a
The utilization of assimilates in the sink can be related
to the level of assimilates by a curvilinear relationship,
a Means followed by the same letter were not significantly different obeying Michaelis-Menten kinetics (Patrick, 1988).
(P~0.05).
Yi = Ypot,iA/(Km,i + A) ( 1)
observed for tomato fruits (De Koning, 1994). However, where Yi is the flux for dry weight growth of organ i
in peach, fruit growth generally did not fully reach the (including growth respiration); Ypot,i is the flux for poten-
potential growth rate after removal of competing fruits tial growth of organ i (including growth respiration), the
(Grossman and Dejong, 1995). Moorby (1968) also maximum rate under the prevailing conditions for A -+ 00;
found indications that sink size is not an important Km,i is the Michaelis-Menten constant, which determines
determinant of sink strength, as he observed a poor the affinity for assimilates (low K m value means high
correlation between the size of individual potato tubers affinity); A is the level of assimilates available for growth.
and the amount of photosynthate transported into them. As the dry matter partitioning into an organ can be
 Sink strength and dry matter partitioning 1287

characterized by the ratio between its growth and that of situation two properties of the sink (potential growth rate
all organs together, in a plant with n organs the fraction and affinity for assimilates) determine its sink strength.
of dry matter partitioned into organ i (fd can be When the affinity differs between two organs the dry
calculated as matter partitioning changes with source strength, such
that the organ with the lowest Km-value gets an increasing
fi = Ypot.J(Km.i + A)
---=---.:...--:....-=..:..:----
n
(2) fraction of dry matter when assimilate supply decreases
I (Ypot)(Km.j+A)) (Fig.2B). Hence, an hierarchy or priority in dry matter
j=l partitioning between organs may be explained by two
From eqn. 2 it can be deduced that when all organs have properties of the sink organs. In fact, this calculation
the same affinity for assimilates (Km-value), the fraction procedure is a simplified version of that of Minchin et al.
of dry matter distributed to an organ equals the ratio of (1993). It ignores the transport resistance (resistance is
its potential growth rate to that of all organs together set to zero) and assimilate concentration in the sink region
(eqn. 3). In this case dry matter partitioning is not affected is not simulated. As discussed before, transport resistance
by source strength (Fig. 2A). As discussed before, source is generally not a dominating factor in dry matter
strength indeed has generally no direct effect on dry partitioning. Moreover, proper estimates of transport
matter partitioning. resistance and photosynthate concentrations at the source
(loading) and sink (unloading) regions are difficult to
Ypot,i
fi= n (3) obtain (Cooper and Thornley, 1976; Brouwer, 1983;
I Ypot,j Makela and Sievanen, 1987), which may limit the possibil-
j=l ities for application and validation of models with trans-
In those cases where source strength has a direct effect port resistances and photosynthate concentrations. The

Downloaded from jxb.oxfordjournals.org by guest on July 6, 2011

on partitioning the fraction of dry matter partitioned into level of assimilate availability that an organ experiences
an organ can be calculated according to eqn. 2. In this increases with source strength, but decreases with sink

10.0 1.6
A

-
<5
",
7.5 1.2
N
5Q
E
C7l
b
-
....
)(
5.0 0.8 .
Ui
0

e
)(
:1 :::J
U:' u:::
2.5 0.4

0.0 I-------'---~ _ _......... _ __"_ _~_ _'___ ___l 0.0

10.0 1.6
B
82

-
"':"CIJ

<5
7.5

51
E
~
5.0
-....
0

)( Ratio 51/52
:1
u:: 2.5

0.0 I - - _ - - - ' -_ _..L...-_--'-_ _..L.-_----'_ _....J..-_----''---_....J 0.0

0 250 500 750 1000

Assimilate concentration (mol m'~

Fig. 2. Assimilate fluxes into two hypothetical sink organs (Sl and 52) and the ratio of these fluxes as a function of the level of assimilate supply
(assimilate concentration in the assimilate pool of the plant). Fluxes are described by Michaelis-Menten kinetics (eqn. 1). The two sinks have
different potential growth rates: 7 and 10 x 10- 9 mol S-l for sinks 1 and 2, respectively. The Km-values of sinks 1 and 2 are both 50 mol m -3 (A)
or 25 and 50 mol m -3, respectively (B).
1288 Marcelis

strengths of the plant's organs. Therefore, several authors fraction of dry matter partitioned into the generative
(Hansen, 1989; Marcelis, 1994; Bertin, 1995) used the parts was well predicted by the ratio between their
source:sink ratio, expressed as the ratio of total plant potential growth rate and that of the total plant
growth rate to total potential growth rate, as a measure (fruits+vegetative parts) (Fig.3B). Marcelis (1994)
for the level of assimilates available for growth. showed that the partitioning among the individual fruits
In a model for dry matter partitioning in cucumber could also be reasonably simulated by a model based on
(Marcelis, 1994), the potential growth rate of each fruit potential growth rates. However, the growth rate of
was described as a function of both its temperature sum young fruits was often somewhat overestimated and that
after anthesis and the actual temperature. The potential of old fruits underestimated, because of dominance
growth rate of the vegetative parts was described as a among fruits. Taking the Km-values of the fruits into
function of the temperature. During a growing season account, the simulation of the competition between young
the potential growth rate of the fruits changed consider- and old fruits improved.
ably due to changes in number and age of the fruits on The number and timing of the fruits on the plant was
the plant (Fig. 3A). During most of the time the actual shown to have a strong impact on model results (Marcelis,
growth rate was far less than the potential growth rate 1994). The formation rate of non-aborting fruits was
(the average ratio between actual and potential rate was calculated as a function of the source:sink ratio and the
0.35). Thus, sink demand exceeded assimilate supply. The temperature. However, there were some deviations
between the simulated and measured formation rate of
30
non-aborting fruits. As our knowledge on fruit abortion
is limited, while abortion has a large effect on dry matter
partitioning, more research is needed on the regulation

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of fruit abortion.
20
Wareing and Patrick (1975) and Patrick (1988)
emphasized the importance of identifying whether organ
growth is either limited by assimilate supply (source
limited) or saturated by assimilate supply (sink limited),
10
because this might have implications for the regulation
of organ growth. Under sink limitation, organ growth
solely depends on its potential capacity to accumulate
assimilates (potential growth). Under source limitation,
0
organ growth depends on the source strength and may
also depend on the organ's potential capacity and affinity
1.00 to accumulate assimilates and on the hydraulic resistance.
B However, often the term source-limitation is interpreted
as organ growth being determined only by the source,
C)
c 0.75 while sink-limitation is interpreted as organ growth only
'2
0 determined by the sinks. Farrar (1993c) suggested aban-
~cu doning the traditional attempts to speak of sink- or
c. 0.50 source-limitation, because control of fluxes (growth) will
'-
Q)
=:
cu be shared by both source and sink rather than centred
E on any single one. The results on cucumber indicate that
c
e 0.25 although growth may be source limited, the fraction of
dry matter partitioned into an organ can, to a great
extent, be related to its potential growth rate relative to
0.00 that of other organs. Thus, although source limited, the
10-Apr 10-May 9-Jun fraction of dry matter partitioned into each organ is still
primarily regulated by the sinks. However, the absolute
Fig. 3. Time-course of the actual (A, .) and potential growth rate of
fruits (A, D) and the measured (B, -0-) and simulated (B, - ) growth rates of the organs also depend strongly on the
fraction of dry matter partitioned into the fruits of cucumber. According source strength.
to eqn. 3, dry matter partitioning into the fruits was simulated as the The study on cucumber has shown that most of the
potential growth of the fruits divided by that of the total plant (fruits
and vegetative parts). Potential growth rate of the vegetative parts was data on dry matter partitioning can be described by the
9.1 g d -1. Calculation of fruit potential growth rate was based on variation among organs in their potential capacity to
measurements of temperature and dates of anthesis and harvest of the accumulate assimilates (potential growth rate). For other
non-aborting fruits. (A) Measured actual rates from Marcelis (l992a)
and calculated potential rates were based on a model described by crops there are also indications that dry matter parti-
Marcelis (1994). (B) From Marcelis (1994). tioning into an organ is proportional to the potential
 Sink strength and dry matter partitioning 1289
growth rate of that organ (Jones et al., 1980, 1989; Lieth in the partitioning of assimilates in wheat ears. Australian
and Pasian, 1991; De Koning, 1994; Grossman and Journal of Plant Physiology 10, 313-27.
Coombe BG. 1976. The development of fleshy fruits. Annual
Delong, 1994; Heuvelink and Bertin, 1994; Wermelinger Review of Plant Physiology 27, 507-28.
et al., 1991). This corroborates that the hydraulic resist- Cooper AJ, Thornley JHM. 1976. Response of dry matter
ance of the transport path is negligible in most cases. partitioning, growth and carbon and nitrogen levels in the
Although these studies have identified the potential capa- tomato plant to changes in root temperature: experiment and
city to accumulate assimilates as an important determin- theory. Annals of Botany 40, 1139-52.
ant of sink strength, the mechanism determining this Daie J. 1985. Carbohydrate partitioning and metabolism in
crops. Horticultural Reviews 7, 69-108.
potential capacity is not elucidated yet. At least for De Koning ANM. 1994. Development and dry matter distribu-
cucumber fruits, neither cell number nor the initial assimil- tion in tomato: a quantitative approach. Dissertation,
ate supply are essential in determining this capacity. It Agricultural University, Wageningen.
could be worthwhile studying whether the maximum rate Dejong TM, Walton EF. 1989. Carbohydrate requirements of
of unloading or utilization and compartmentation in the peach fruit growth and respiration. Tree Physiology 5,329-35.
Dekhuijzen HM, Verkerke DR. 1986. The effect of temperature
sink organ are important determinants of the potential on development and dry-matter accumulation of Vicia faba
growth rate, and how these processes are controlled by seeds. Annals of Botany 58, 869-85.
hormones or, as suggested by Farrar (1992), by sucrose. Dennett MD, Auld BA, Elston J. 1978. A description of leaf
In addition, the use of molecular tools may help in a growth in Vicia faba L. Annals of Botany 42, 223-32.
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strength and dry matter partitioning (Frommer and temperature on the growth of individual leaves of Vida faba
L. in the field. Annals of Botany 43, 197-208.
Sonnewald, 1995). Egli DB. 1988. Alterations in plant growth and dry matter
distribution in soybean. Agronomy Journal 80, 86-90.

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Egli DB, Wardlaw IF. 1980. Temperature response of seed
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