Journal of Experimental Botany, Vol. 47, Special Issue, pp. 1239-1243, August 1996
Journal of
Experimental
Botany
The mechanism of assimilate partitioning and
carbohydrate compartmentation in fruit in relation
to the quality and yield of tomato
L.C. Ho
Department of Annual Crops, Horticulture Research International, Wellesbourne, Warwick CV359EF, UK
Abstract
The limitation of tomato yield was investigated in a
number of cultivars with contrasting fruiting habits.
Unless light is limiting, yield is mainly restricted by the
number or the size of the fruit (l.e, the sink strength)
rather than the supply of assimilate (i.e, the source
strength). Fruit size is determined by both cell number
and cell size. The rate of fruit expansion is affected
by assimilate supply, temperature and water relations
in the plant. The size or the growth rate ofa tomato
fruit is regulated by the import of assimilate and water.
The sink strength for assimilate of a tomato fruit measured by the rate of assimilate import may be related
to the routes of sugar transport into the sink cells
during fruit development. Enzymic regulation of the
hydrolysis of sucrose by sucrose synthase and the
accumulation of starch by ADPG pyrophosphorylase
may determine the rate of assimilate import in the
young fruit. Vacuolar invertase activity may determine
the sugar composition of a mature fruit, but may not
affect the overall dry matter accumulation of a tomato
fruit. While yield is determined by the balance between
source and sink strengths of the plant, quality is determined by the transport and metabolism of sugars
within the fruit.
Key words: Assimilate partitioning, sink strength, sugar
transport, carbohydrate metabolism, tomato fruit.
Introduction
Glasshouse-grown tomato is a high yielding crop. An
annual yield of 550 tonnes per hectare by the best
growers represents a fruit yield of 24 kg per plant. This
is mainly achieved by prolonging the cropping season to
exploit the intrinsic character of high fruit production in
© Oxford University Press 1996
tomato. Even taking into account that up to 95% of the
harvested fruit is water, the partitioning of dry matter in
the plant into fruit is very high with a harvest index
above 65% (Ho, 1984). It is plausible that future tomato
yield improvement can be gained from the manipulation of dry matter partitioning more in favour of
fruit growth.
In recent years, great progress has been made in the
regulation of the import of assimilate and the compartmentation of imported sucrose in tomato fruit. Based on
the relationship between enzyme activity and the accumulation of sugars, tentative biochemical markers for sink
strength in storage cells of tomato fruit have been identified (Damon et aI., 1988; Robinson et al., 1988; Yelle
et al., 1991; Sun et al., 1992; Dali et al., 1992; Wang
et aI., 1993a). Furthermore, the routes of unloading or
the post-phloem intercellular transport and the nature of
membrane transport in tomato fruit have also been
assessed (Damon et al., 1988; Johnson et aI., 1988; Fieuw
and Willenbrink, 1991; Offler and Horder, 1992; Ruan
and Patrick, 1995). Advances in molecular biology and
success in genetic engineering make it possible to quantify
the regulatory roles of these rate-limiting enzymes and
putative membrane sugar transporters in the accumulation of sugars in tomato fruit (Dickinson et al., 1991;
Worrell et al., 1991; Bennett et al., 1992; Wang et al.,
1993b, 1994; Micallef et al., 1995; Frommer and
Sonnewald, 1995). The question is, can the manipulation
of enzymes for sugar metabolism and transporters for
sugar membrane transport improve the fruit size or the
fruit chemical composition?
The aim of this paper is to assess how much the fruit
yield, fruit growth and sugar accumulation in the storage
cells of tomato fruit can benefit from our understanding
of the mechanism of assimilate partitioning and carbohydrate compartmentation in fruit.
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Received 14 August 1995; Accepted 15 September 1995
1240
Ho
the product of fruit number and fruit size, as the measure
of total sink strength for fruit, determines the partitioning
of assimilate in tomato plants, but increase in fruit size
appears to be the more effective way to improve the
harvest index and the yield in tomato.
Assimilation and assimilate partitioning
Tomato yield is proportional to the availability of photoassimilate, as the annual yield is related to days of bright
sunshine in a light-limited country, such as England
(Bewley, 1929). Shading up to 25% light loss leads to a
similar proportional yield loss (Cockshull et al., 1992).
This relationship implies that tomato yield can be sourcelimiting and that partitioning of assimilate to fruit growth
is a constant proportion of assimilate production.
The total sink strength of all tomato fruit, the strongest
sink for assimilate, may dominate the partitioning of
assimilate in the plant. Tomato plants with different
growing habits, i.e. determinate (bush type) and indeterminate (single stem), and different fruiting habits, i.e.
beefsteak (large in size but few in number), round
(medium in both size and number) and cherry (small in
size but numerous in number), accumulate similar
amounts of dry matter per plant when they are grown in
similar environments (Table 1). However, the partitioning
of dry matter is substantially affected by both growing
and fruiting habits. For instance, among indeterminate
types, cherry tomatoes accumulate the highest proportion
of dry matter in leaves, stem and truss stalk, but the
lowest in the fruit. Despite the high fruit number of
cherry tomato (2-4 times more than others), the small
size of the fruit (4-8 times less than the others) may be
the main cause of the low partitioning to fruit (Table 2).
The fruit yields of beefsteak and round tomatoes are
similar but nearly double that of cherry tomato. Thus,
The final fruit size of a tomato is determined by a number
of ~nternal and external factors at fruit set and during
fruit development. It is likely that the size difference
among fruit of different cultivars or at different truss
positions or in different positions in the truss, is potentially determined before fruit enlargement. It has been
demonstrated that the differences in cell number in the
pericarp of ovary before anthesis can largely account for
differences in actual fruit size among cultivars (Bohner
and Bangerth, 1988a; Ho, 1992) and in different fruit
positions (Bohner and Bangerth, 1988b). Although the
regulation of cell division before anthesis in tomato fruit
is not fully understood, cell number in the pre-anthesis
ovary can be affected by assimilate supply (Bohner and
Bangerth, 1988b) or gamma irradiation (Bohner and
Bangerth, 1988a), or growth regulators (Bunger-Kibler
and Bangerth, 1982). The cell division period in the ovary
after anthesis is rather short, being complete within 2
weeks after anthesis (Ho and Hewitt, 1986), so the final
cell number is proportional to the cell number of the
ovary before anthesis and potential fruit size is largely
determined by the cell division activity before anthesis.
Once the potential fruit size is fixed, the actual fruit size
is a consequence of cell enlargement.
In general, the rate of fruit enlargement is in proportion
to assimilate supply as determined by the irradiance level
(Ehret and Ho, 1986). This relationship is obvious when
plants are kept at positive water potential (Grange and
Andrews, 1994). However, because of the high priority
of assimilate partitioning to fruit and an efficient remobilization of reserves to sustain transport, the fruit expansion
rate can be sustained up to 22 h after the plant is darkened
(~earce et aI., 1993a). The apparent diurnal fruit expanSIOn patterns observed in the glasshouse (Ehret and Ho,
1986; Pearce et al., 1993b) are mainly the result of a
temperature effect associated with irradiance; both the
rate of carbon import (Walker and Ho, 1977) and of
fruit expansion (Pearce et aI., 1993a) are linearly enhanced
1. Dry matter partitioning in tomato plants 112 dafter
sowing
Cultivars
Plant dry wt.
(g)
% Plant dry wt. in
Leaves
Indetermediate
Cleopatra
(beefsteak)
Counter (round)
Sweet 100 (cherry)
Determinate
FM6203
FM785
UC82b
Sign, P
Cvs
Types
Stem
Truss
Fruit
216.7
43.4
21.3
2.53
32.8
198.0
202.6
33.9
45.0
18.4
25.4
3.83
6.36
43.8
23.3
198.2
218.5
138.6
48.7
47.4
50.8
16.6
21.3
12.9
3.02
2.78
3.46
31.7
28.5
32.9
<0.001
<0.001
0.001
0.009
0.02
n.s.
0.04
n.s.
0.015
0.004
Table 2. The number and size of tomato fruit in relation to yield
Types
Beefsteak
Round
Cherry
Fruit number
per truss
5
9
22
Average fruit
fro wt. (g)
150
80
20
Yield per
truss (g)
750
720
440
Dry matter
content (%)
5.5
6.0
8.0
Relative yield
Fr. wt.
Dry wt.
1.04
1.00
0.61
1.05
1.00
0.85
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Tab~e
Assimilate import and fruit growth
Assimilate partitioning in tomato
Sugar transport and metabolism
The accumulation of sugars in the storage cells of tomato
fruit is crucial to both the size and the taste. In a ripe
tomato fruit, about half of the dry matter is hexose which
accounts for 65% of the soluble solute in the fruit juice
(Ho and Hewitt, 1986). As the accumulation of hexose
accounts for the principal part of the dry matter accumulation in tomato fruit, the metabolism of the imported
sucrose and the transport of sugars for the accumulation
of hexose in the vacuole of the storage cells may itself
control the rate of assimilate import (Ho, 1988).
Based on the transport of asymmetrically labelled
radioactive sucrose and the composition of apoplastic
sap, sucrose may be either unloaded symplastically or/and
apoplastically within the tomato fruit (Damon et al.,
1988). When sucrose is unloaded symplastically through
plasmodesmata, it may be hydrolysed by sucrose synthase
in the cytosol (Robinson et al., 1988), and when unloaded
apoplastically, it may be hydrolysed by cell wall bound
acid invertase. Consequently, hexose is the principal form
of sugar in the apoplastic sap (Damon et al., 1988).
Based on the frequency of the plasmodesmata and the
surface area of the plasma membrane of the storage cells,
it has been suggested that symplastic intercellular transport may be sufficient to account for the import of
assimilate by the fruit in the early stage of fruit development, while apoplastic transport may be the main route
of sugar transport in the fruit later on (Johnson et aI.,
1988; Offier and Horder, 1992). The transport of the
symplastic or apoplastic tracers confirms that the facility
for symplastic post-phloem intercellular transport tends
to be greatly reduced during fruit development (Ruan
and Patrick, 1995). While the transition from symplastic
to apoplastic transport within the fruit is plausible, the
exact timing and the manner of change are not certain.
Because the membrane transport of sugars appears to be
related to the presence of sulphydryl protein and the
activity of H + -ATPase at the membrane, it may be an
energy-dependent and carrier-mediated process (Ruan
and Patrick, 1995). Future research on the regulation of
membrane transport of sugars may provide the much
needed information to improve the accumulation of
sugars in tomato.
Hydrolysis of sucrose has long been suggested as the
rate-limiting step for assimilate transport for tomato fruit
growth (Walker et aI., 1978). Although acid invertase
(AI) exists in tomato fruit, most likely in both the cell
wall and vacuole, the hydrolysis of sucrose by this enzyme
is unlikely to be the limiting step for assimilate import
for the following reasons. (1) The activity of AI did not
change with the rate of dry matter accumulation, or the
relative growth of the fruit or fruit size (Johnson et al.,
1988; Sun et al., 1992; Wang et al., 1993a, b). (2) The
differential change of AI activity during fruit maturation
in sucrose or hexose accumulating tomatoes mainly affect
the composition of the storage sugars rather than the rate
of assimilate import (Miron and Schaffer, 1991; Stommel,
1992; Dali et al., 1992). (3) The activity of AI in different
fruit tissues during fruit development is much higher than
that required for the hydrolysis of all imported sucrose,
and is thus unlikely to be the limiting factor for the
regulation of assimilate import (Demnitz-King, 1993).
However, until the activity of AI in the cell wall can be
quantified, the regulatory role of AI for the apoplastic
transport of sugars can not be completely ruled out.
In contrast, sucrose synthase (SS) may play an important role in regulating the import of sucrose. The activity
of SS increased to a peak about 3 weeks after anthesis
and then declined to an undetectable level at the mature
green stage (Yelle et al., 1988; Stommel, 1992; Dali et al.,
1992; Demnitz-King, 1993). This transient pattern of SS
activity during fruit development is in parallel to the
accumulation of starch (Robinson et al., 1988). In fact,
the change of SS activity has been reported to be linearly
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by temperature in the range between 10°C and 30 °C.
Therefore, temperature has the most profound effect on
fruit metabolism and fruit expansion when assimilate and
water supply are not limiting. Although the maximal fruit
expansion rate is related to the final fruit size under
similar growing conditions (Grange and Andrews, 1993),
the short-term effect of temperature on fruit expansion
does not necessarily increase the final size of the fruit. In
practice, increased temperature in the glasshouse can
reduce the duration of fruit growth thus resulting in
smaller fruit size (De Koning, 1994). Therefore, the final
size of a tomato fruit is determined by the rate and the
duration of fruit expansion.
As a berry, tomato fruit expansion is greatly affected
by the water relations in the plant. For example, when
the plant is under water stress at midday, the rate of fruit
expansion can be reduced even though the light and
temperature conditions may favour fruit expansion
(Pearce et al., 1993b). For this reason, both the rate of
expansion (Pearce et al., 1993b) and the final fruit size
(Ehret and Ho, 1986) are reduced linearly by increasing
salinity in the growing media. However, within the range
of electrical conductivity (EC) between 2 and 12
mS em - 1, the reduction in fruit size is mainly due to the
reduction of water rather than dry matter accumulation
in the fruit (Ho et al., 1987). It was suggested that
assimilate import rate in fruit grown at high salinity may
be sustained by higher phloem sap concentration to
compensate for lower phloem sap volume resulting from
water stress in the plant. Therefore, fruit expansion rate
can be affected by assimilate and water import independently. In this sense, fruit expansion rate can only be used
to assess the rate of assimilate import in tomato fruit
when the water relations are well defined.
1241
1242
Ho
accumulated, either sucrose or hexose. The possible role
of SPS on re-synthesis of sucrose for the accumulation of
sugar in the vacuole is not yet known.
Conclusions
Although the yield of tomato can be limited by assimilate
supply (source strength), the potential yield is determined
by the fruit number and size (sink strength). The partitioning of dry matter for fruit production can be enhanced
more efficiently by increasing fruit size. Increasing the cell
number in the pre-anthesis ovary (potential fruit size)
may also be an efficient way to increase fruit size.
However, in practice, the actual fruit size can be manipulated effectively by altering the light, temperature and
water relations to alter either the rate or the duration of
fruit expansion. Both the sucrose metabolism and transport may affect the accumulation of dry matter in tomato
fruit, and thus the fruit quality. There may be multiple
control points during fruit development to regulate both
the import of assimilate and the accumulation of sugars.
Therefore, improvement of sugar transport and metabolism in the storage cell alone may have relatively small
impact on fruit yield. Further improvement of tomato
yield and quality will depend on a concerted effort in
research on the regulation of fruit number and size as
well as the regulation of water relations and sucrose
metabolism and transport inside the tomato fruit.
Acknowledgements
This work is supported by BBSRC formerly AFRC of the UK.
At the closure of the research site at Littlehampton, I dedicate
this paper to all my colleagues over the last 25 years for their
contributions to glasshouse crops research.
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