PHYSIOLOGY OF HIGH YIELDING
CORN AND SOYBEANS
Mark E. Westgate1
I.
Introduction
Canopy Photosynthesis and Grain Yield
a. Corn as a sink limited crop
b. Soybeans as a source limited crop
II.
Managing for Efficient Use of Assimilates
a. Cross pollination of maize
Reproductive Development – Seed formation
b. Asynchrony and abortion
c. Assimilate supply and carbohydrate metabolism
III. Reproductive Development -- Seed Development
a. Rate and duration of seed filling
IV. Concluding Remarks
References
Department of Agronomy, Iowa State University, Ames, IA 50011, EUA.
E-mail: westgate@iastate.edu
This paper is a contribution from the Iowa State University Experiment Station.
Experiment Station Journal Number _____________.
I. INTRODUCTION
This review will outline the plant factors that contribute to high grain
yield in maize (Zea mays L.) and soybean (Glycine max L.) canopies under
field conditions. Because grain yield is determined by the number of grains
per unit area and the average weight per grain, the discussion will
necessarily focus on physiological factors controlling grain formation and
development. The extent to which yield formation is limited by the capacity
of the maize and soybean canopies to produce photoassimilate and deliver
it to the developing flowers and grains will be considered in detail. This
discussion will lead to realistic conclusions about how the maize and
soybean canopies should be managed for optimum use of available
sunlight and grain production.
Average maize and soybean yields typically are only about one-third
to one-fourth of those obtained in ‘maximum yield’ experiments. In most
cases, the primary environmental factor preventing these crops from
producing much greater grain yield is lack of soil moisture. Therefore, this
review also will consider the impact of water deficits during reproductive
development on the success of grain formation and grain growth. The
discussion will focus on the importance of maintaining floral development
prior to pollination and the physiological factors contributing to increased
grain abortion commonly observed during drought. It will also consider how
drought alters the rate and duration of grain development leading to the
production of smaller grains. Finally, several possible ‘physiological
strategies’ to limit abortion and maintain grain growth under water limited
conditions will be discussed.
II. CANOPY PHOTOSYNTHESIS AND GRAIN YIELD
It seems intuitive that grain yield is somehow related to the
production of photosynthate during the season. But there is only limited
evidence in the literature to provide a ‘physiological connection’ between
the primary productivity of the maize and soybean canopies, and their
capacity to produce a large number of grains per unit area. In this section,
we will review some of the physical factors limiting photosynthate
production by a crop canopy, we will examine the documented relationships
between seasonal canopy photosynthesis and grain yield in maize and
soybean, and we will build upon this information to determine whether
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managing these crops for increased photosynthetic capacity is a realistic
approach to improve grain yields.
As the term implies, “photosynthesis” is the physico-chemical
process plant canopies use to convert solar energy into useable
biochemical energy. Obviously, capturing solar radiation in the ‘photosynthetically active range (PAR: approx. 400-700 nm)’ is a primary
consideration. It has been estimated that about 5% of the incident solar
energy is captured by plants. The value is generously high, and might apply
to a rapidly growing canopy (eg. maize, or sugarcane) at high light intensity.
Most crops are much less efficient. Also, the rate of photosynthesis for
individual leaves can be saturated for light at a fraction of the light intensity
typical of field conditions. Assuming that more photosynthesis is needed to
increase grain yield, it is reasonable to consider ways to alter light
interception by the canopy to improve the efficiency and use of incoming
solar radiation. For convenience, reflection of light by the canopy and soil
surface are ignored, and the amount of PAR intercepted by the canopy
(IPAR) is approximated by the difference between the incoming PAR above
the canopy and the transmitted PAR at the soil surface (TPAR). The overall
efficiency of the canopy for light interception is described by a canopy
extinction coefficient, k, which relates the amount of light intercepted per
unit leaf area, IPAR = PAR exp-kLAI. According to this relationship, the
amount of light intercepted – IPAR – should increase exponentially with an
increase in the number of leaf layers (leaf area index = LAI), or with an
increase the efficiency of each leaf layer, k. Does managing the maize and
soybean canopies for increased IPAR lead to an increase in grain yield?

Maize -- a sink limited crop
Countless row spacing and population studies have sought to
identify the optimum management combination for maximizing grain yield.
In theory, decreasing spacing between rows and increasing the distance
between plants should increase light interception between the rows, and
minimize competition between plants for water and nutrients within rows.
The combination of 38 cm row spacing and 7.4 plants m-2 provides a nearly
equidistant pattern of plants. But a general consensus from these ‘row pop’
studies is that maximum maize yields are achieved at an intermediate row
spacing (about 50 cm), and moderately aggressive plant population
densities (8-10 plants m-2). A recent study by Flenet et al. (1996) concluded
3
that the efficiency of light interception of maize canopies increases linearly
with decreasing row spacing. If light interception is limiting, why doesn’t
yield continue to increase with closer rows (eg. 38 cm), which provides an
equidistant spacing between plants?
A study by (Westgate et al., 1996) may provide the answer. In this
example, there was no discernible difference in yield between at 38 cm and
76 cm row spacing. Grain yield increased with plant population density,
however, up to about 9 plants m-2. Increasing plant population had a large
effect on maximum LAI and light interception (LI) achieved by the canopies
– and presumably the total amount of canopy photosynthesis for the
season. There was no difference in light interception between the narrow
(38 cm) and wide (76 cm) row spacings. Evidently, the greater spacing
between plants in the 38-cm rows decreased TPAR between the rows, but
increased TPAR between the plants within the rows. When canopy LI is
plotted vs. LAI for all combinations of row spacing and plant population, it
becomes evident that altering row spacing and plant population density
does not necessarily improve the efficiency of light interception of the
individual leaf layers, k. Greater plant density improves light interception
primarily by adding more leaf layers. Importantly, decreasing row spacing
beyond 76 cm had relatively little impact on overall canopy light
interception.
From a yield formation perspective, there is an optimum amount of
light interception for the maize crop in terms of the maximum achieved by
the canopy, the rate of canopy closure, and the total IPAR accumulated
prior to anthesis. Canopies that can intercept about 95% of incident PAR
when maximum leaf area is achieved at flowering achieve maximum grain
yield. A canopy that ultimately intercepts more than 95% PAR (possible at
high population density), for example, may have a photosynthetic
advantage early in the season because of early canopy closure. But this
advantage does not translate into increased grain production, presumably
because of a low growth rate per plant during flowering (discussed below).
Such results imply that maximizing light interception of the canopy in
an attempt to increase photosynthate production will not necessarily lead to
yield increases. Apparently, the maize canopy produces more photosynthate during the season than can be utilized by grain, even when less
than 100% of the incident PAR is captured. This implies that grain yield in
4
maize is limited by the number and activity of ‘sinks’ for photosynthate
(grains), rather than the ‘source’ of photosynthate for those sinks.
Studies documenting source-sink relations of maize canopies have
utilized large ‘canopy photosynthesis chambers’ to monitor photosynthate
production during the entire growing season (Christy and Porter, 1982).
These chambers enclose a large number of plants without disturbing the
canopy structure, and quantify the rate of photosynthesis by CO 2 depletion
within the chamber. Photosynthetic rates are measured on clear days at
high light intensity, and are corrected for ‘soil respiration’ from bare soil
nearby. Thus, the rates provide an estimate of the potential rate of CO2
fixation for the canopy during the season. Typically, canopy rates increase
with LAI to a maximum at flowering, and decrease thereafter. By integrating
the area under the curve, it is possible to relate ‘seasonal canopy
photosynthesis’ with grain yield for a range of crop management options
and weather conditions.
When similar treatments are compared across years, so that
environment was the main treatment variable, there was a poor correlation
between yield and seasonal canopy photosynthesis (Christy and
Williamson, 1985). There was wide variation in available assimilate during
the four years of this study that showed little correspondence to yield levels.
Likewise, variation in grain yield produced across a wide range of plant
population densities was not related seasonal canopy photosynthesis. But
yield varied directly with the capacity of the canopy to convert available
photosynthate into grain, a term Christy and Williamson coined
Photosynthetic Conversion Efficiency (PCE = grain yield/seasonal photosynthesis). Apparently, the PCE of the maize canopies in these
experiments peaked at a plant density of about 10 plant m-2, which also was
the most efficient canopy for light interception in other studies (Westgate et
al. 1996). Explaining variation in grain yield through differences in PCE is
somewhat biased because grain yield is included in the calculation of PCE.
Nonetheless, this approach underscores the conclusion that high grain yield
in maize is not solely the result of high levels of seasonal photosynthate
production. Physiological factors controlling the efficiency of converting
available photosynthate into grain will be considered later in this review.
Although grain yield in maize generally is not ‘source limited’, current
assimilate supply is critical during flowering and early kernel development.
Shade treatments applied during pollination have a large negative impact
5
on kernel numbers, even under well-watered conditions (Christy et al.,
1986). But the impact of decreasing PAR by 50% during this period on final
grain yield varies with prevailing environmental conditions. In fours years of
study, the variation in grain yield in the unshaded control plots was greater
than the loss in yield caused by shading during pollination or grain filling.
The highest yield was achieved in a relatively cool year with high seasonal
canopy photosynthesis. This was also the year that showed the greatest
effect of shading during reproductive development. Lowest yields were
obtained in hot years with low to medium seasonal canopy photosynthesis.
These results suggested that plant stress associated with higher than
average temperatures affected the capacity of the maize canopies to utilize
the available photosynthate, and decreased yield potential below that
expected from seasonal assimilate production. This possibility was taken
into account by adjusting the seasonal canopy photosynthesis by a heat
stress factor to create a PHS-Stress Index. Remarkably, the PHS-Stress
Index accounted for nearly all the variation in grain yield across the four
yield environments in this study.
Most of the variation in grain yield from year-to-year is due to
differences in grain number per unit area. Grain size is relatively more
stable, but can contribute to lower yields when stress occurs late in the
season (see below). It is well established that the number of grains that
develop on a maize plant is determined by the amount of PAR intercepted
per plant growth during a two-to-three week period around silking. Recent
studies confirm that the relationship between kernel number (KN) and IPAR
is curvilinear for each ear. A minimum IPAR plant–1 of about 0.5 MJ plant-1
d-1 is required to set any kernels. And about 1.5 MJ plant-1 d-1 is required to
set kernels on a second ear. These results help explain why barrenness
increases at high plant densities, and why second (or third) ears set grains
at low plant densities. In both cases, IPAR plant -1 determines the potential
plant growth rate, which is a critical factor for establishing the number of
pollinated flowers that continue to develop into grains.
In summary, the results from a number of field studies lead to the
conclusion that grain yield in maize is ‘sink’ rather than ‘source’ limited.
Therefore, establishing growth conditions that provide high rates of canopy
photosynthesis, while necessary, are not sufficient to ensure high grain
yield. Management strategies that increase seasonal canopy photosynthesis will only be beneficial if they do not interfere with the
establishment of reproductive sinks. The challenge for achieving high grain
6
yield is to e determine optimum plant population density needed for 95% LI
yet ensure a rapid growth rate per plant during silking, which is critical high
grain set.
 Soybeans -- a source limited crop
As was the case for maize, canopy photosynthesis rates for the
soybean canopy increase with LAI < 4, reach a maximum coincident with
flowering and pod set, then decrease during grain filling. In contrast to
maize, however, maximum rates of canopy photosynthesis for soybean are
considerably lower, even at comparable LAI. This raises the possibility that
seasonal canopy fixation might limit grain production. Row spacing and
plant population studies confirm that managing the crop for earlier canopy
closure can increase grain yield. Research from many year/locations in
Iowa, for example, indicate that planting soybeans in narrow (<76 cm) rows
and at high population densities (>350k plant ha-1) provide maximum yield
performance in most environments. Measurements of light interception by
soybean canopies planted at various row spacings confirm that the narrowrow canopies are indeed more efficient at light interception. But is the
difference between light extinction coefficients for 76 cm rows (k = ~0.43)
and 38 cm rows (k = ~0.51) sufficient to explain the yield advantage? In
reality, the advantage in terms of increasing IPAR is small, on the order of 3
to 5 %. As with maize, the major advantage for increasing light interception
occurs in response to plant population and increased leaf area. In fact, a
less efficient canopy (with a lower k) is more likely to achieve higher growth
rates because it has a greater LAI at a given level of light interception.
Planting date studies also show that extending the length of the
growing season also can increase grain yields. Soybean varieties adapted
for Iowa, for example, typically achieve maximum grain yield when planted
in late April or early May. Yields decrease dramatically with later plantings.
The earlier planting extends the duration of both the vegetative (VE-R1) and
reproductive (R1-R8) stages of development. Together, these crop
management studies suggest that increasing the integral of seasonal
canopy photosynthesis is an effective means to increase grain yield in
soybeans. Studies relating seasonal canopy photosynthesis and grain yield
confirm that this is indeed the case (Christy and Williamson, 1985). In
contrast to maize, there is a very close relationship between seasonal
7
canopy photosynthesis and grain yield in soybean — a very clear indication
that yield of soybeans is ‘source limited.’
When viewed from the perspective of canopy photosynthetic rates,
the advantage of planting at populations and row spacings that promote
early canopy closure is obvious. Canopies that enter the flowering and pod
setting stage with high rates of photosynthesis produce the greatest yields.
The variation in yield is associated almost entirely with the number of grains
m-2. In the example above, altering plant density caused yield variation.
But the dependence of yield on grain number holds true for a wide range of
growth conditions. In the Midwest US, soybeans typically are exposed to a
number of stresses at the same time, such as herbicides, nematodes, and
water deficits. Experiments are currently under way to test how soybean
yield is affected by multiple environmental stresses. Preliminary results
indicate that, regardless of the combination of stresses imposed, variation
in grain yield reflects the capacity of the canopy to form seeds. In this
experiment, the highest yielding genotype/treatment combinations were
those that had the greatest biomass and canopy growth rate during
flowering (R1-R3). Treatments that decreased growth rate caused a
corresponding and predictable decrease in seed number, and yield. It is
clear from the results of this study, and those of Egli and Zhen-wen (1991),
that seeds m-2 (and therefore, potential grain yield) depends directly on
canopy growth rate during flowering and pod set. Therefore, it is essential
to manage the soybean crop to achieve its maximum growth rate during this
critical period.
Shading studies confirm this conclusion. Christy et al. (1986)
decreased incident PAR by 50% using shade cloth during vegetative,
flowering-pod set, and pod filling to determine the dependence of seed
number and seed size on current assimilate supply. Decreasing incident
PAR by 50% decreased canopy photosynthetic rates about 35% on
average, indicating that the soybean canopy was saturated for light during
most of the season. As expected for this source-limited crop, decreasing
canopy photosynthesis continuously resulted in a corresponding decrease
in grain yield, caused entirely by a loss of seed numbers. Shading during
flower/pod set and seed filling caused a similar decrease in seed number,
but yield loss was greater in the pod-fill treatment. This result indicates
three things about the ‘indeterminate’ soybean canopy. First, seed number
m-2 is the yield component most sensitive to the decrease in current
assimilate supply. Second, final seed number is not determined until well
8
after seed filling has begun. And third, once seed number is established,
some compensation in seed size is possible, if assimilate is available. Yield
losses occur only when compensation is no longer possible. It is interesting
to note that removing the shade after the vegetative period had a positive
impact on seed number. This likely reflected an increase in growth rate of
the canopy in response to the 50% increase in incident PAR as the plants
reached the flowering stage.
In summary, grain yield in soybean is ‘source limited.’ Therefore,
management strategies that increase seasonal canopy photosynthesis
have the potential to increase grain yield. As was the case in maize, seeds
m-2 is the primary determinant of yield; and this yield component is closely
coupled to the rate of crop growth during flowering and pod set. Maximizing
crop growth rate during this period is essential for maximum grain yield.
Optimum row spacing and plant population can improve the light harvesting
efficiency of the canopy. But providing optimum conditions for plant growth
early in the season likely will have a greater impact on seasonal canopy
photosynthesis – and therefore, on maximizing grain yield.
III. MANAGING FOR EFFICIENT USE OF ASSIMILATES
POTENTIAL YIELD ADVANTAGE FROM OUT-CROSSING
MAIZE HYBRIDS
To this point, managing the maize and soybean crops for high yield
has focused on maximizing light interception and crop growth rate during
the period seed numbers are being determined. This approach seeks to
increase grain set by providing the maximum level of photosynthate
possible to the recently fertilized ovaries. The right combination of row
spacing, population, date of planting and genotype might achieve the goal
of increasing assimilate production, but which combination ensures that
assimilates produced by the crop are used most efficiently for seed
formation and development? To address this question, it is essential to
examine the physiological factors that control seed formation and seed
growth.
Because soybean flowers are predominately self-pollinated,
maximizing crop growth rate at flowering may be the best way to maximize
grain yield on a field scale. The pistillate flowers of maize, however, are
largely cross-pollinated – i.e. with pollen produced by other plants. Maize
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breeders have long taken advantage of cross-pollination of genetically
dissimilar inbreds to produce highly productive hybrids – a phenomenon
known as heterosis. Cross-pollination occurs naturally in the field of maize
plants as well, but in a typical monoculture, all the plants are genetically
related. All the seed are the product of sib- or self-pollination. So, instead
of realizing a yield gain from heterosis, there is actually a slight yield penalty
associated with the first generation of inbreeding depression. It may be
possible to eliminate this inbreeding depression (and thereby realize a yield
gain) by adopting a planting strategy that ensures a high degree of crosspollination between hybrids in the same field. Several years of large-scale
field trials have shown that planting hybrids from different companies
together in an alternate row pattern provided a 4 bu/a yield advantage over
the same hybrids grown in monoculture in adjacent plots. The yield
advantage resulted from greater seed number and increased seed size.
There was no yield advantage to mixing two hybrids from the same
company. Obviously, careful hybrid selection is the key to this strategy.
Hybrids must flower (shed pollen and exsert silks) at the same time. And
they also must not have a common parent. The first requirement is
relatively easy to meet. A comparison of the flowering characteristics of 75
locally adapted hybrids from Western Minnesota showed it quite possible to
identify 10 to 12 hybrids that flowered within 25 GDU (1 day) of one
another. The second requirement is more difficult because seed companies
do not share pedigree information readily. But selecting hybrids from
different companies, though not foolproof, is a reasonable starting point, as
our field trials have clearly shown.
In summary, this field study shows that out-crossing maize hybrids
can provide a ‘free’ yield advantage beyond that expected from maximizing
crop growth rate during flowering. The yield advantage results from an
increase in sink demand (grain number and size), which is consistent with
the conclusion that maize is a ‘sink limited’ crop.
IV. REPRODUCTIVE DEVELOPMENT – SEED FORMATION
Under most growing conditions, grain yield in maize and soybean is
only a fraction of the maximum yields recorded for these crops. The
formation and development of the reproductive sinks, which are the
economically valuable parts of the crop, are highly vulnerable to stresses,
particularly water stress. Lack of soil moisture during flowering and early
seed formation decrease the number of grains that develop. And moisture
10
stress during seed filling results in smaller grains. In both soybean and
maize, the period of seed formation is the most sensitive to drought in terms
of yield losses. The impact of drought decreases dramatically as the grain
approaches physiological maturity.
Early reproductive development is particularly vulnerable to drought
because much of the development involves expansion growth, which is
inhibited severely by lack of water. In maize, the inhibition of growth leads
to two important problems – asynchrony in male and female flower
development, and abortion of newly formed zygotes with the ovaries. The
next sections describe the yield losses that occur in maize due to these
developmental problems, and discusses the central role of assimilate
supply in improving grain set under drought conditions.
 Asynchrony in flower development and kernel abortion in maize
Evidence from long-term breeding trials at CIMMYT in Mexico
clearly underscore the importance of maintaining synchrony between male
and female flower development to improve yield performance of maize
under severe drought conditions (Edmeades et al., 2000). Recurrent
selection for improved grain yield under severe drought produced
genotypes with a shorter anthesis-silking interval (ASI) and more rapid ear
growth rate during drought. There was no yield advantage under irrigated
conditions, but selection increased the proportion on plants in the population that produced a seed-bearing ear.
Presumably, the shorter ASI increased the number of successful
pollinations of exposed silks. Breeders routinely select for close synchrony
between pollen shed and silk emergence in the hopes that all the silks will
emerge when there is sufficient pollen being shed to ensure their
pollination. As drought inhibits ear and silk growth, an increasing number of
flowers fail to become pollinated. Is the solution to this dilemma of
asynchrony an increase in the amount or duration of pollen shed, or a
change in the pattern of silk emergence? The distinction between these two
possibilities is important because they lead to very different selection
strategies.
To answer this question, Bassetti and Westgate (1994) established
a number of asynchronous plots within a large field, which provided a single
source for pollen shed. Asynchrony included silk emergence prior to pollen
11
shed (protogyny) as well as silk emergence after pollen shed (protandry).
As expected, maximum kernel set occurred in plots whose silks began to
emerge within one or two days of anthesis (50% of plants shedding pollen.
Kernel set decreased dramatically in plots whose silk emergence started
after the peak rate of pollen shed. By examining the pattern of kernel set
on ears collected from the various asynchrony plots, they could determine
whether silk emergence or pollen shed limited kernel set. There ware
perfect kernel set only on ears whose silks began to emerge within one day
of anthesis. Ears collected from plants whose silks began to emerge later
(3, 5, 7, 9, 11 days) showed progressively greater loss of kernels at tip
positions, ultimately progressing to the base of the ear. But ears with 3, 5
or 7 days of anthesis all had perfect kernel set in the lower portion of the
ear (positions 5-15). This result indicated that the intensity of pollen shed
was sufficient up 7 days after anthesis to ensure pollination of all exposed
silks. At this point, the rate of pollen shed was about 125 grains cm-2 d-1.
The loss of kernels at apical ear positions must have resulted from lack of
silk emergence. With asynchrony beyond 7 days, loss of kernels resulted
from lack of silk emergence and lack of sufficient pollen.
The results of this study indicated that late emerging silks were at
risk of not being pollinated even under well-watered conditions. Any delay
in ear development or silk growth due to drought would only worsen this
situation. Bassetti and Westgate (1994) also observed that plots whose
silks began to emerge in advance of pollen shed by as many as six days
also had a high level of kernel set and grain yield. The success of these
protogynous plots suggests that one possible strategy to overcome the
negative effects of drought on the synchrony between silk emergence and
pollen shed is to select for genotypes that naturally initiate silk emergence
prior to pollen shed. The immediate advantage of this shift in development
in favor of earlier silk emergence is that any stress-induced delay in silk
emergence would actually improve the synchrony in flowering. A subtler,
but equally important, benefit of selecting for protogynous plants is the
increased priority for ear growth prior to anthesis.
These results also highlighted the need to define the flowering
process in maize on a more rigorous quantitative basis than that currently
being used to define dates of silking and anthesis. Silk emergence on an
individual ear is a progress process, which may take up to 10 days to
complete. Likewise, the process of pollen shed from an individual tassel
progresses in intensity over the course of several days. The process of
12
pollination itself depends not on the percentage of the population shedding
pollen or silking, but on the actual density of pollen grains being shed, and
the number of silks that are exposed to that pollen each day. By exposing
receptive silks on different plants to a wide range of pollen densities
occurring naturally in the field, Bassetti and Westgate (1994) discovered
that >95% of all exposed silks were successfully pollinated when the
density of pollen shed reaching the silks was >125 grains cm-2 d-1. At lower
densities of pollen shed, the percent kernel set decreased rapidly. This
minimum density of pollen shed was nearly identical to that observed in the
asynchrony experiments described earlier. With these basic quantitative
measures of flowering dynamics and a curve relating pollen density to
kernel set, it is now possible to predict in a quantitative manner the potential
number of kernels set each day in the field, and the potential number of
kernels ha-1 set by the end of pollen shed. In the example provided, which
is taken from actual field data, the greatest intensity of kernel set occurs 2
to 4 days after anthesis. Afterwards, kernel set decreased dramatically
because silk emerge too late to become pollination. This approach, of
course, provides potential kernel numbers because stress-induced abortions have not been taken into account.
Even if pollination is successful, fewer kernels may develop under
drought conditions because a higher percentage of zygotes abort a few
days after fertilization (Westgate and Boyer, 1986). For plant growing in the
field, a short-term water deficit during pollination can decrease kernel
number per ear by 50% (Schussler and Westgate, 1994); the same level of
water stress imposed on the same genotype grown in a growth chamber
can cause a complete failure of kernel set (i.e. 100% abortion) (Schussler
and Westgate, 1991). Results from a large number of related studies aimed
at understanding the physiological basis for this increase in kernel abortion
have lead to the conclusion that abortion is directly related to the inhibition
of ovary growth. Regardless of genotype, growth conditions, or stress level,
inhibition of ovary growth lead to a decrease in kernel number per ear. In
all cases, plants were hand pollinated with abundant pollen. Measurements
of ovary weight in maize populations selected for short ASI during drought
support this conclusion. Plants with short ASI under drought conditions
have larger ovaries at the time of pollination. The practical outcome of these
studies is that maintenance of rapid ovary growth is essential for high kernel
set when stress occurs during pollination.
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
Assimilate supply and carbohydrate metabolism
The decrease in kernel numbers in response to shading, decreased
kernel numbers per plant at low IPAR, and the severe inhibition of
photosynthesis at low leaf water potential, all imply that the inhibition of
ovary growth during drought is somehow linked to the current supply of
photosynthate. The model relating ovary growth to photosynthate supply
proposed by Zinselmeier et al. (1999) suggests that rapid ovary growth
occurs when there is an ample supply of photosynthate from current
photosynthesis and from reserves. Under mild stress conditions,
photosynthesis is inhibited and ovaries depend on mobilized reserves to
continue growing. As stress becomes more severe, lack of current
photosynthate and depletion of reserves cause the ovaries to abort. If this
model is accurate, it should be possible to maintain the supply of
photosynthate to the ovaries under stressful environments. First, and most
obvious, is maintaining the production of photosynthate at low leaf water
potential. To the author’s knowledge, there are no published reports
indicating this is possible. Small improvements associated with osmotic
adjustment have not been sufficient to sustain reproductive development. A
second possibility is to increase the contribution of assimilates remobilized
from temporary storage tissues, such as the stem internode, and rachis.
Third, sustaining metabolic activity within the water stressed ovaries could
increase partitioning of available assimilate to the ear.
To be successful with the latter two strategies, a number of
‘physiological barriers’ need to be overcome. First is the fact that the
developing ovaries are competing with a large number of well-established
sinks. These sinks have priority for assimilates from both current and
reserve sources. Second is the fact that the temporary storage tissues
(stem internodes, rachis) are still active sinks during pollination. They
contain very high concentrations of sugars, but the sugar is primarily
glucose, which cannot be remobilized. The third barrier to overcome is the
inhibition of carbohydrate metabolism within the ovary itself. This inhibition
of metabolism makes this weak sink an even poorer competitor for
assimilates.
To determine which of these ‘barriers’ was most important to
overcome, it was necessary to resolve whether the failure of kernels to
develop during drought was due entirely to the lack of current assimilate
supply. This was done by comparing the kernel set in plants whose
14
photosynthesis rates were inhibited to the same extent and duration by low
leaf water potential or by low light intensity. Presumably, both treatments
would cause the same reduction in kernel set if current assimilate supply
controlled ovary abortion. The results of this experiment indicated that lack
of current photosynthate accounted for about 70% of the kernel loss
observed in droughted plants. The additional loss of kernels was due to
another, as yet unknown, factor (Schussler and Westgate, 1991). Sucrose
feeding experiments, in which supplemental sucrose was supplied by stem
infusion, lead to the same basic conclusion. Adding enough sucrose to
account for the sugar that would have been produced had photosynthesis
been able to continue at low leaf water potential, recovered about 70% of
the kernels lost in droughted plants without stem infusion. Related
experiments proved that sucrose was the active agent causing the recovery
of kernel numbers (Zinselmeier et al. 1995, 1999).
These experiments clearly demonstrated that maintaining the
current supply of photosynthate was critical for improving kernel set during
drought. But it is not realistic to infuse sucrose into plants in the field! A
possible alternative is to increase the contribution of reserve sugars when
photosynthesis is inhibited. To test this possibility, three treatments were
established in the field designed to vary the level of reserve sugars in the
plant prior to imposing a water deficit during pollination. A 50% shade
treatment decreased sugar levels (and concentration) relative to the control
plants in full sun. And a widely spaced treatment increased sugar levels,
presumable to the genetic potential for the hybrids in the study. At
pollination, a water stress of similar intensity and duration was imposed on
all three treatments and plants were hand pollinated with abundant pollen.
The inhibition of photosynthesis was the same in all three treatments as
well. The control plants at a normal plant density in full sun set about 50%
fewer kernels when water stressed during pollination. Shaded plants with a
lower level of reserves prior to pollination set even fewer kernels. But the
increased accumulation of reserve sugars in the spaced plants did not
render them less sensitive to the water stress. Thus, is was possible to
make plants more sensitive by shading, but it was not possible to decrease
their sensitivity by increasing the level of reserves (Schussler and
Westgate, 1994).
Examination of the type of sugars accumulating in the stem
internodes and rachis (cob) at the time of pollination, revealed why altering
sugar levels along would not be sufficient to increase assimilate availability
15
to the developing ovaries. At pollination, well over 30% of the weight of the
cob is in the form of sugars. But only about 2% of that sugar is in a form
than can be remobilized, i.e. sucrose. Likewise, the sugars in the ear stalk
(shank) are predominantly reducing sugars (glucose + fructose); sugars in
the stem internode below the ear node are about equally distributed
between reducing sugars and sucrose. Thus, none of these structures is an
ideal source of sucrose for remobilization. In fact, just the opposite occurs
when water is withheld; sucrose accumulates rapidly in the cob and shank,
and sucrose levels remain fairly stable in the stem internodes. Evidently,
these structures continue to function physiologically as sinks for assimilate
during pollination. High levels of acid invertase (AI), which is typical of
growing tissues, in the cob at this time support the accumulation of glucose.
And the inhibition of AI in droughted plants is consistent with the
accumulation of sucrose.
It will be exceedingly difficult to alter the pattern of sucrose
accumulation in the stem internodes, cob and shank tissues given our
current state of knowledge about mechanisms of sugar metabolism and
storage in these tissues. The mechanism(s) of sucrose import and export
are not known. The biochemistry of carbohydrate metabolism is not fully
characterized. Tissue- and temporally-specific promoters are lacking for
possible transgenic approaches. And, most importantly, the pattern of
sucrose accumulation is coupled to tissue development. It likely will be
necessary to alter development of these structures in order to accelerate or
enhance their capacity for exporting sucrose during pollination.
The fact that not all of the kernel loss in water stressed plants could
be accounted for by lack of assimilate supply implied that other factors also
contributed to the increase in kernel abortion. The failure of kernels to
develop when pollinations occurred at low ovary water potential suggested
that kernel set might depend on conditions within the pistillate flowers
themselves. Preliminary measurements on isolated ovaries showed that
water decreased the capacity of ovaries to utilize sucrose in vitro (Schussler
and Westgate, 1991). A developmental profile of the carbohydrate status of
ovaries samples from well-watered and water-stressed plants revealed that
a brief water deficit at silk emergence dramatically altered the reducing
sugar, sucrose, and starch levels within the ovaries. Most notable was a
large increase in the amount and concentration of sucrose relative to the
control plants. The rapid decrease in sucrose content at silk emergence in
the control plants may serve to maintain sucrose unloading from the phloem
16
into the pedicel region of the ovary. If so, the high concentrations of
sucrose that develop in water stressed ovaries may limit the capacity for
continued phloem unloading, thereby decreasing ovary ‘sink strength.’ This
possibility is supported by estimates of sugar concentrations in the ovary
apoplasm (Westgate, unpublished), which clearly indicated a large
decreased in reducing sugar/sucrose ratios in the apoplasm of waterstressed ovaries. This result suggested that the capacity for sucrose
hydrolysis had been impaired. Measurements of ovary acid invertase
activity indicated that, indeed, extractable acid invertase activity within the
ovaries was dramatically inhibited at low ovary water potential. The
physiological basis for the inhibition of invertase activity is not fully
understood, but evidence from Anderson et al. (2000) shows that
transcription of the soluble form of acid invertase (Ivr2) decreases during
water stress. Parallel analyses of the insoluble form of acid invertase (Ivcw)
have not been reported. But the activities of both the soluble and insoluble
forms of invertase are inhibited to the same extent by water deficits
(Zinselmeier et al., 1995). Importantly, the level of (insoluble) invertase
activity is directly related to the rate of ovary growth. The recovery of kernel
numbers in response to stem infusion of sucrose corresponds to a recovery
of ovary acid invertase activity (Zinselmeier et al., 1999). These results
provide strong support for the central role of carbohydrate metabolism in
establishing the young kernels as a sink for photosynthate. Water stress
caused a lesion in carbohydrate metabolism within the ovaries, which must
be overcome to increase kernel set during drought.
Could this ‘lesion’ in metabolism also explain the more rapid loss of
starch within water-deficient ovaries? Typically during silk emergence and
pollination, ovary starch levels are increasing slowly (actually declining on a
concentration basis). But the level and concentration of starch decrease
dramatically when water is withheld, even though sucrose concentrations
are well above control levels. Evidently the sucrose that accumulated,
whether from starch hydrolysis or phloem unloading, is not being
metabolized by the ovaries. Sucrose infusion into the stems of water
stressed plants reverses the drought-induced loss of starch. And as was
the case for invertase activity, the recovery of ovary starch level is closely
correlated with kernel set (Zinselmeier et al. 1999). Water stress had little
impact on activities of enzymes in the pathway from glucose to starch, such
as ADP-glucose pyrophosphorylase or starch synthases. The most
sensitive enzymes were the invertases. These results indicate that loss of
invertase activity apparently is the key ‘metabolic’ lesion caused by a water
17
deficit. It explains the rapid accumulation of sucrose and the loss of starch
in the ovaries. And the subsequent decrease in reproductive sink strength
when drought occurs during pollination.
In summary, grain yield in maize remains highly vulnerable to water
deficits during pollination in large part because ovary carbohydrate
metabolism is inhibited. This inhibitions disrupts the flux of assimilates to
the ovaries, and slows ovary growth. The decrease in ovary growth
translates directly to an increased probability of reproductive failure – i.e.
kernel abortion.
Current and future strategies to maintain zygote (kernel) development during drought include developing a greater understanding of the
molecular controls of sucrose and starch accumulation in storage tissues
prior to anthesis; determining the molecular basis for the inhibition of ovary
invertase activity at low ovary water potential, and identifying genes whose
activity is related to the inhibition of ovary growth under drought conditions.
V. REPRODUCTIVE DEVELOPMENT - SEED DEVELOPMENT
Once the number of seeds has been established, the only
reproductive adjustment possible when canopy photosynthesis is inhibited
by adverse environmental conditions is to limit the extent of seed
development. Fortunately, the sensitivity of grain yield to drought decreases
as reproductive development progresses towards physiological maturity in
both maize and soybeans.
Drought during seed filling generally results in the production of
smaller seeds. Possible physiological explanations for producing smaller
seeds include loss of current assimilate supply due to accelerated leaf
senescence, decreased sink capacity possible resulting from fewer cells or
less cell volume, or inhibition of storage product synthesis due to premature
desiccation. The remainder of this review will consider the evidence
supporting these possibilities for the maize and soybean crops.
18

Rate and duration of seed filling
Under well watered and fertilize conditions, maize kernels typically
achieve their maximum volume early in development. Kernel moisture
remains fairly stable during linear grain filling, but begins to decrease while
kernels are rapidly filling. Maximum dry weight is achieved during a period
of ‘terminal’ desiccation.
In a greenhouse study, Westgate and Grant (1989) showed that a
brief water deficit during linear filling had little impact on dry matter
accumulation of maize kernels, but did cause a substantial decrease in
kernel water content. The change in water content of the kernels was not
reflected in kernel water potential, which did not change despite a large
decrease in leaf water potential. The remarkable stability of kernel water
potential in the water-deficient plants implies that developing grains are
hydraulically isolated from the water status of the plant. The actual
mechanism that makes this possible is not known. In maize and soybean,
there are no direct vascular connections between the maternal tissue and
the embryos. And special ‘apopolastic barriers’ have been proposed
(Bradford, 1994), but direct evidence for such a barrier is lacking.
Regardless of the mechanism, the maintenance of stable water potentials
within the developing seed should allow metabolism to continue even under
severe drought conditions.
These results of this short-term experiment indicated two things
about grain development during drought. First, the smaller grains that
typically develop under drought conditions probably result from a shorter
grain filling period, rather than a decrease in grain fill rate. Second, drought
did indeed alter the water status of the seed, by decreasing its water
content, even though the water loss was not evident from measurements of
grain water potential. This suggested that there might be connection
between grain moisture content and the duration of grain filling. To test this
possibility, a long-term water deficit was imposed on plant grown in the
field. Irrigation water was withheld after seed number was established, so
that any yield adjustments must result from a decrease in grain weight. The
water deficit decreased ear-leaf water potential over a period of several
weeks, and caused the leaves to senesce prematurely. Leaf photosynthesis
was inhibited at leaf water potentials below –1.2 MPa. After this point, grain
filling depended primarily on mobilization of reserves. Periodic measurements of grain mass showed that kernels on water deficient plants
19
continued to fill at the control rate, confirming the results of the short-term
greenhouse study. The water-deficient plants produced smaller grains
because they ceased filling sooner after anthesis. The decrease in grain
yield from 11.1 to 9.1 Mg ha-1 in this experiment was due entirely to the
decrease in grain size. The embryos within the kernels showed the same
general response. Water deficient plants produced smaller embryos
because of a shorter duration of filling.
What was the physiological basis for the shorter duration of filling?
One possibility was lack of assimilate. It is well known that carbohydrate
reserves in the stem are remobilized to support kernel growth, and that
under severe stress, grain growth will continue until these reserves are
nearly depleted (Westgate and Boyer, 1985; Simmons and Jones, 1985).
Measurements of non-structural carbohydrate in leaves, vegetative stalk,
and reproductive stalks revealed that assimilate levels decreased in the
water-stressed plants relative to levels in the well-watered controls. But
carbohydrates in the vegetative stalk were not completely depleted when
grain filling ceased (about 50 days after anthesis), and carbohydrates
began to accumulate thereafter. Also, there was no indication that
carbohydrate accumulation in the grain was altered due to a lack of
photoassimilate. These data support the conclusion that assimilate supply
was not the primary cause of a shorter filling period in the water deficient
plants. The fact that carbohydrates continue to accumulate in the vegetative
stalk of well-watered plants throughout grain filling supports this conclusion.
Measurements of grain water status showed that kernels on the
water-deficient plants reached the same maximum water content as did the
well-watered plants, but began to lose moisture sooner (but not faster) after
anthesis. This premature desiccation was consistent with the decrease in
moisture content observed by Westgate and Grant (1989) earlier. The fact
that the kernels on the water-deficient plants achieved the same maximum
water volume as did kernels on well-watered plants indicated that the
potential grain size was the same in both treatments. But the premature
desiccation raised the possibility that the change in grain water status early
in filling actually affected the duration of the grain filling process. If so, there
should be a consistent relationship between grain moisture status and grain
development, regardless of the treatments imposed. When compared on a
tissue moisture basis, the developmental pattern of kernel and embryo
water potential were nearly identical for the well-watered and waterdeficient treatments. Likewise, data examined from other studies shows a
20
very consistent pattern of dry matter accumulation when development is
normalized on a kernel moisture basis. Regardless of genotype or
environment, kernels ceased to accumulate dry matter at about 30 %
moisture (Egli and Tekrony 1997, Westgate and Boyer, 1986). The same is
true of kernel development when water deficit treatments are imposed at
different times during grain filling. Withholding water from plants at the
kernel blister stage (rapid water uptake), dough stage (early grain filling), or
dent stage (late grain filling) had dramatically different effects on final kernel
dry matter. But kernels in all treatments ceased to accumulate dry matter at
about the same moisture content – approx. 30%.
Evidence from a host of sources including in vitro measurements of
enzyme activities at low moisture contents (Rupley et al., 1983), enzyme
activities extracted from dry seeds (Muhitch, 1991), and the physical
properties of water in dry seeds (Vertucci, 1989) all point to the conclusion
that the osmotic conditions in the endosperm and embryo late in grain filling
do not directly inhibit the activity of enzymes responsible for storage product
synthesis. Rather, the decrease in storage product synthesis probably
reflects a decreased capacity for protein synthesis (Bewley, 1981; Kermode
et al., 1989). Desiccation itself may be a developmental queue for
terminating transcription and translation of synthetic proteins and initiating
the synthesis of proteins required for desiccation tolerance, eg. dehydrins.
If so, the premature desiccation caused by drought during grain filling
causes smaller kernels to be produced because they reach the minimum
moisture content that supports metabolism sooner after anthesis.
Maintaining grain filling then requires modifications in grain development
that either increase the maximum water volume early in filling, or prevent
premature desiccation from occurring. Current studies are investigating the
importance of increasing maximum cell volume as a means to achieve this
goal.
The soybean embryo undergoes a similar pattern of development,
but maximum dry weight is achieved coincident with maximum water
content (and therefore, maximum fresh weight). The embryo desiccates
rapidly thereafter. As was the case in maize, drought during grain filling
shortens the duration of filling, resulting in smaller seeds (Meckel et al.,
1984). Water deficits severe enough to inhibit leaf photosynthesis
completely had little effect on the rate of dry matter accumulation by the
embryo – at least on the short term (Westgate et al., 1989). Part of the
reason embryo could continue to develop was that they exhibited the same
21
type of hydraulic isolation from changes in plant water status that was
observed in maize. There also was an increased rate of mobilization of
carbohydrate and reduced N from the vegetative tissues and pod wall.
Interestingly, the embryos from water deficient plants also exhibited an
increased capacity for sucrose uptake from the surrounding free space,
which apparently compensated for the decrease in apoplast sucrose
concentration being by the maternal tissues. This study indicated that
embryo growth rate is maintained in soybean by a coordinated shift in
metabolism among the vegetative and reproductive tissues.
This
coordinated adjustment allows embryo growth to continue until reserves are
depleted.
The fact that soybean embryos reached maximum water volume
and dry weight at the same time suggest that embryo water status might
also be an important determinant of grain fill duration. In vitro culture
studies show that soybean cotyledons will continue to accumulate dry
matter as long as can continue to expand in water content and volume.
Embryo removed from pods early in grain filling achieve much greater mass
than their in planta counterparts (Egli, 1990). This type of evidence implies
that embryo mass in planta is limited, at least in part, by the surrounding
pericarp (pod) walls. This possibility was tested by placing small tubes
around developing pods to restrict their expansion. The results clearly show
that embryos with limit maximum water volume develop into smaller seeds.
Related studies indicate that restricting volume shortens the grain fill period,
and that the ‘restriction’ is reversible during most of the grain filling period.
Whether water deficits during grain filling limit maximum embryo volume in
a similar manner has not been examined. But it is a reasonable possibility
since numerous studies confirm that, regardless of treatment or growth
conditions, grain filling in soybean ceases at about 60% moisture.
In summary, embryos that store a large amount of protein in vacuole
(eg. soybean embryos, maize embryos), protein accumulation continues
until maximum water volume is achieved. In seeds that store predominately
starch (egg. maize, wheat) grain fill duration is determined by the maximum
cell volume established early in seed development, and by the onset of
desiccation later in development. Drought shortens the duration of grain
filling by causing premature desiccation and/or by limiting the maximum cell
volume.
22
VI. CONCLUDING REMARKS
These studies have raised a number of questions regarding the
control of grain filling and the impact that adverse environmental conditions
have on the capacity of developing seeds to reach their potential size. How
do environmental conditions early in grain filling regulate the duration of the
filling process? Under what conditions does lack of assimilate supply limit
the duration of grain filling, rather than seed water status? And finally, how
is seed composition (eg. protein, oil, starch content) maintained under
conditions that alter the rate and duration of grain filling? Because lack of
available soil moisture is the primary environmental limitation for high grain
yields, answers to these questions will lead to rational targets for genetic
modification, physiological selection, and practical management strategies
to improve grain production across a range of environments.
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