fisiologia sojamilho mark e. westgate

8/4/2019 Fisiologia SojaMilho Mark E. Westgate

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PHYSIOLOGY OF HIGH YIELDING

CORN AND SOYBEANS

Mark E. Westgate1

I. Introduction

I. Canopy Photosynthesis and Grain Yield

a. Corn as a sink limited cropb. Soybeans as a source limited crop

II. Managing for Efficient Use of Assimilates

c. Cross pollination of maize

III. Reproductive Development Seed formation

d. Asynchrony and abortion

e. Assimilate supply and carbohydrate metabolism

IV. Reproductive Development -- Seed Development

f. Rate and duration of seed filling

V. Concluding Remarks

References

Department of Agronomy, Iowa State University, Ames, IA 50011, EUA.E-mail:[email protected]

This paper is a contribution from the Iowa State University Experiment Station.Experiment Station Journal Number _____________.
mailto:[email protected]:[email protected]:[email protected]


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I. INTRODUCTION

This review will outline the plant factors that contribute to high grainyield in maize (Zea mays L.) and soybean (Glycine maxL.) canopies underfield conditions. Because grain yield is determined by the number of grainsper unit area and the average weight per grain, the discussion willnecessarily focus on physiological factors controlling grain formation anddevelopment. The extent to which yield formation is limited by the capacityof the maize and soybean canopies to produce photoassimilate and deliverit to the developing flowers and grains will be considered in detail. Thisdiscussion will lead to realistic conclusions about how the maize andsoybean canopies should be managed for optimum use of availablesunlight and grain production.

Average maize and soybean yields typically are only about one-thirdto one-fourth of those obtained in maximum yield experiments. In mostcases, the primary environmental factor preventing these crops fromproducing much greater grain yield is lack of soil moisture. Therefore, thisreview also will consider the impact of water deficits during reproductivedevelopment on the success of grain formation and grain growth. Thediscussion will focus on the importance of maintaining floral developmentprior to pollination and the physiological factors contributing to increasedgrain abortion commonly observed during drought. It will also consider howdrought alters the rate and duration of grain development leading to theproduction of smaller grains. Finally, several possible physiologicalstrategies to limit abortion and maintain grain growth under water limitedconditions will be discussed.

II. CANOPY PHOTOSYNTHESIS AND GRAIN YIELD

It seems intuitive that grain yield is somehow related to theproduction of photosynthate during the season. But there is only limitedevidence in the literature to provide a physiological connection betweenthe primary productivity of the maize and soybean canopies, and theircapacity to produce a large number of grains per unit area. In this section,we will review some of the physical factors limiting photosynthateproduction by a crop canopy, we will examine the documented relationshipsbetween seasonal canopy photosynthesis and grain yield in maize andsoybean, and we will build upon this information to determine whether

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managing these crops for increased photosynthetic capacity is a realisticapproach to improve grain yields.

As the term implies, photosynthesis is the physico-chemicalprocess plant canopies use to convert solar energy into useablebiochemical energy. Obviously, capturing solar radiation in the photosyn-thetically active range (PAR: approx. 400-700 nm) is a primaryconsideration. It has been estimated that about 5% of the incident solarenergy is captured by plants. The value is generously high, and might applyto a rapidly growing canopy (eg. maize, or sugarcane) at high light intensity.Most crops are much less efficient. Also, the rate of photosynthesis forindividual leaves can be saturated for light at a fraction of the light intensitytypical of field conditions. Assuming that more photosynthesis is needed toincrease grain yield, it is reasonable to consider ways to alter light

interception by the canopy to improve the efficiency and use of incomingsolar radiation. For convenience, reflection of light by the canopy and soilsurface are ignored, and the amount of PAR intercepted by the canopy(IPAR) is approximated by the difference between the incoming PAR abovethe canopy and the transmitted PAR at the soil surface (TPAR). The overallefficiency of the canopy for light interception is described by a canopyextinction coefficient, k, which relates the amount of light intercepted per

unit leaf area, IPAR = PAR exp-kLAI. 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 anincrease the efficiency of each leaf layer, k. Does managing the maize andsoybean canopies for increased IPAR lead to an increase in grain yield?

Maize -- a sink limited crop

Countless row spacing and population studies have sought toidentify 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, andminimize competition between plants for water and nutrients within rows.The combination of 38 cm row spacing and 7.4 plants m-2 provides a nearlyequidistant pattern of plants. But a general consensus from these row popstudies is that maximum maize yields are achieved at an intermediate rowspacing (about 50 cm), and moderately aggressive plant populationdensities (8-10 plants m-2). A recent study by Flenet et al. (1996) concluded

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that the efficiency of light interception of maize canopies increases linearlywith decreasing row spacing. If light interception is limiting, why doesntyield continue to increase with closer rows (eg. 38 cm), which provides anequidistant spacing between plants?

A study by (Westgate et al., 1996) may provide the answer. In thisexample, there was no discernible difference in yield between at 38 cm and76 cm row spacing. Grain yield increased with plant population density,however, up to about 9 plants m-2. Increasing plant population had a largeeffect on maximum LAI and light interception (LI) achieved by the canopies

and presumably the total amount of canopy photosynthesis for theseason. There was no difference in light interception between the narrow(38 cm) and wide (76 cm) row spacings. Evidently, the greater spacingbetween plants in the 38-cm rows decreased TPAR between the rows, but

increased TPAR between the plants within the rows. When canopy LI isplotted vs. LAI for all combinations of row spacing and plant population, itbecomes evident that altering row spacing and plant population densitydoes not necessarily improve the efficiency of light interception of theindividual leaf layers, k. Greater plant density improves light interceptionprimarily by adding more leaf layers. Importantly, decreasing row spacingbeyond 76 cm had relatively little impact on overall canopy lightinterception.

From a yield formation perspective, there is an optimum amount oflight interception for the maize crop in terms of the maximum achieved bythe canopy, the rate of canopy closure, and the total IPAR accumulatedprior to anthesis. Canopies that can intercept about 95% of incident PARwhen maximum leaf area is achieved at flowering achieve maximum grainyield. A canopy that ultimately intercepts more than 95% PAR (possible athigh population density), for example, may have a photosyntheticadvantage early in the season because of early canopy closure. But thisadvantage does not translate into increased grain production, presumablybecause of a low growth rate per plant during flowering (discussed below).

Such results imply that maximizing light interception of the canopy inan attempt to increase photosynthate production will not necessarily lead toyield increases. Apparently, the maize canopy produces more photo-synthate during the season than can be utilized by grain, even when lessthan 100% of the incident PAR is captured. This implies that grain yield in

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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 haveutilized large canopy photosynthesis chambers to monitor photosynthateproduction during the entire growing season (Christy and Porter, 1982).These chambers enclose a large number of plants without disturbing thecanopy structure, and quantify the rate of photosynthesis by CO2 depletionwithin the chamber. Photosynthetic rates are measured on clear days athigh light intensity, and are corrected for soil respiration from bare soilnearby. Thus, the rates provide an estimate of the potential rate of CO2fixation for the canopy during the season. Typically, canopy rates increasewith LAI to a maximum at flowering, and decrease thereafter. By integratingthe area under the curve, it is possible to relate seasonal canopy

photosynthesis with grain yield for a range of crop management optionsand weather conditions.

When similar treatments are compared across years, so thatenvironment was the main treatment variable, there was a poor correlationbetween yield and seasonal canopy photosynthesis (Christy andWilliamson, 1985). There was wide variation in available assimilate duringthe four years of this study that showed little correspondence to yield levels.Likewise, variation in grain yield produced across a wide range of plantpopulation densities was not related seasonal canopy photosynthesis. Butyield varied directly with the capacity of the canopy to convert availablephotosynthate into grain, a term Christy and Williamson coinedPhotosynthetic Conversion Efficiency (PCE = grain yield/seasonal photo-synthesis). Apparently, the PCE of the maize canopies in theseexperiments peaked at a plant density of about 10 plant m-2, which also wasthe most efficient canopy for light interception in other studies (Westgate etal. 1996). Explaining variation in grain yield through differences in PCE issomewhat 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 photosynthateproduction. Physiological factors controlling the efficiency of convertingavailable photosynthate into grain will be considered later in this review.

Although grain yield in maize generally is not source limited, currentassimilate supply is critical during flowering and early kernel development.Shade treatments applied during pollination have a large negative impact

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on kernel numbers, even under well-watered conditions (Christy et al.,1986). But the impact of decreasing PAR by 50% during this period on finalgrain yield varies with prevailing environmental conditions. In fours years ofstudy, the variation in grain yield in the unshaded control plots was greaterthan the loss in yield caused by shading during pollination or grain filling.The highest yield was achieved in a relatively cool year with high seasonalcanopy photosynthesis. This was also the year that showed the greatesteffect of shading during reproductive development. Lowest yields wereobtained in hot years with low to medium seasonal canopy photosynthesis.These results suggested that plant stress associated with higher thanaverage temperatures affected the capacity of the maize canopies to utilizethe available photosynthate, and decreased yield potential below thatexpected from seasonal assimilate production. This possibility was takeninto account by adjusting the seasonal canopy photosynthesis by a heat

stress factor to create a PHS-Stress Index. Remarkably, the PHS-StressIndex accounted for nearly all the variation in grain yield across the fouryield environments in this study.

Most of the variation in grain yield from year-to-year is due todifferences in grain number per unit area. Grain size is relatively morestable, but can contribute to lower yields when stress occurs late in theseason (see below). It is well established that the number of grains thatdevelop on a maize plant is determined by the amount of PAR interceptedper plant growth during a two-to-three week period around silking. Recentstudies confirm that the relationship between kernel number (KN) and IPARis curvilinear for each ear. A minimum IPAR plant1 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 toset kernels on a second ear. These results help explain why barrennessincreases at high plant densities, and why second (or third) ears set grainsat low plant densities. In both cases, IPAR plant-1 determines the potentialplant growth rate, which is a critical factor for establishing the number ofpollinated flowers that continue to develop into grains.

In summary, the results from a number of field studies lead to theconclusion that grain yield in maize is sink rather than source limited.Therefore, establishing growth conditions that provide high rates of canopyphotosynthesis, while necessary, are not sufficient to ensure high grainyield. Management strategies that increase seasonal canopy photo-synthesis will only be beneficial if they do not interfere with theestablishment of reproductive sinks. The challenge for achieving high grain

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yield is to e determine optimum plant population density needed for 95% LIyet ensure a rapid growth rate per plant during silking, which is critical highgrain set.

Soybeans -- a source limited crop

As was the case for maize, canopy photosynthesis rates for thesoybean canopy increase with LAI < 4, reach a maximum coincident withflowering and pod set, then decrease during grain filling. In contrast tomaize, however, maximum rates of canopy photosynthesis for soybean areconsiderably lower, even at comparable LAI. This raises the possibility thatseasonal canopy fixation might limit grain production. Row spacing andplant population studies confirm that managing the crop for earlier canopy

closure can increase grain yield. Research from many year/locations inIowa, for example, indicate that planting soybeans in narrow (350k plant ha-1) provide maximum yieldperformance in most environments. Measurements of light interception bysoybean canopies planted at various row spacings confirm that the narrow-row canopies are indeed more efficient at light interception. But is thedifference between light extinction coefficients for 76 cm rows (k= ~0.43)and 38 cm rows (k= ~0.51) sufficient to explain the yield advantage? Inreality, 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 interceptionoccurs in response to plant population and increased leaf area. In fact, aless efficient canopy (with a lowerk) is more likely to achieve higher growthrates because it has a greater LAI at a given level of light interception.

Planting date studies also show that extending the length of thegrowing season also can increase grain yields. Soybean varieties adaptedfor Iowa, for example, typically achieve maximum grain yield when plantedin 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 cropmanagement studies suggest that increasing the integral of seasonalcanopy photosynthesis is an effective means to increase grain yield insoybeans. Studies relating seasonal canopy photosynthesis and grain yieldconfirm that this is indeed the case (Christy and Williamson, 1985). Incontrast to maize, there is a very close relationship between seasonal

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canopy photosynthesis and grain yield in soybean a very clear indicationthat 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 promoteearly canopy closure is obvious. Canopies that enter the flowering and podsetting stage with high rates of photosynthesis produce the greatest yields.The variation in yield is associated almost entirely with the number of grainsm-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 ofgrowth conditions. In the Midwest US, soybeans typically are exposed to anumber of stresses at the same time, such as herbicides, nematodes, andwater deficits. Experiments are currently under way to test how soybeanyield is affected by multiple environmental stresses. Preliminary results

indicate that, regardless of the combination of stresses imposed, variationin grain yield reflects the capacity of the canopy to form seeds. In thisexperiment, the highest yielding genotype/treatment combinations werethose that had the greatest biomass and canopy growth rate duringflowering (R1-R3). Treatments that decreased growth rate caused acorresponding and predictable decrease in seed number, and yield. It isclear 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 oncanopy growth rate during flowering and pod set. Therefore, it is essentialto manage the soybean crop to achieve its maximum growth rate during thiscritical 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 seednumber and seed size on current assimilate supply. Decreasing incidentPAR by 50% decreased canopy photosynthetic rates about 35% onaverage, indicating that the soybean canopy was saturated for light duringmost of the season. As expected for this source-limited crop, decreasing

canopy photosynthesis continuously resulted in a corresponding decreasein grain yield, caused entirely by a loss of seed numbers. Shading duringflower/pod set and seed filling caused a similar decrease in seed number,but yield loss was greater in the pod-fill treatment. This result indicatesthree things about the indeterminate soybean canopy. First, seed numberm-2 is the yield component most sensitive to the decrease in currentassimilate supply. Second, final seed number is not determined until well

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after seed filling has begun. And third, once seed number is established,some compensation in seed size is possible, if assimilate is available. Yieldlosses occur only when compensation is no longer possible. It is interestingto note that removing the shade after the vegetative period had a positiveimpact on seed number. This likely reflected an increase in growth rate ofthe canopy in response to the 50% increase in incident PAR as the plantsreached the flowering stage.

In summary, grain yield in soybean is source limited. Therefore,management strategies that increase seasonal canopy photosynthesishave the potential to increase grain yield. As was the case in maize, seedsm-2 is the primary determinant of yield; and this yield component is closelycoupled to the rate of crop growth during flowering and pod set. Maximizingcrop growth rate during this period is essential for maximum grain yield.

Optimum row spacing and plant population can improve the light harvestingefficiency of the canopy. But providing optimum conditions for plant growthearly in the season likely will have a greater impact on seasonal canopyphotosynthesis and therefore, on maximizing grain yield.

III. MANAGING FOR EFFICIENT USE OF ASSIMILATES

POTENTIAL YIELD ADVANTAGE FROM OUT-CROSSINGMAIZE HYBRIDS

To this point, managing the maize and soybean crops for high yieldhas focused on maximizing light interception and crop growth rate duringthe period seed numbers are being determined. This approach seeks toincrease grain set by providing the maximum level of photosynthatepossible to the recently fertilized ovaries. The right combination of rowspacing, population, date of planting and genotype might achieve the goalof increasing assimilate production, but which combination ensures thatassimilates produced by the crop are used most efficiently for seedformation and development? To address this question, it is essential to

examine the physiological factors that control seed formation and seedgrowth.

Because soybean flowers are predominately self-pollinated,maximizing crop growth rate at flowering may be the best way to maximizegrain yield on a field scale. The pistillate flowers of maize, however, arelargely cross-pollinated i.e. with pollen produced by other plants. Maize

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breeders have long taken advantage of cross-pollination of geneticallydissimilar inbreds to produce highly productive hybrids a phenomenonknown as heterosis. Cross-pollination occurs naturally in the field of maizeplants as well, but in a typical monoculture, all the plants are geneticallyrelated. All the seed are the product of sib- or self-pollination. So, insteadof realizing a yield gain from heterosis, there is actually a slight yield penaltyassociated with the first generation of inbreeding depression. It may bepossible to eliminate this inbreeding depression (and thereby realize a yieldgain) by adopting a planting strategy that ensures a high degree of cross-pollination between hybrids in the same field. Several years of large-scalefield trials have shown that planting hybrids from different companiestogether in an alternate row pattern provided a 4 bu/a yield advantage overthe same hybrids grown in monoculture in adjacent plots. The yieldadvantage resulted from greater seed number and increased seed size.

There was no yield advantage to mixing two hybrids from the samecompany. Obviously, careful hybrid selection is the key to this strategy.Hybrids must flower (shed pollen and exsert silks) at the same time. Andthey also must not have a common parent. The first requirement isrelatively easy to meet. A comparison of the flowering characteristics of 75locally adapted hybrids from Western Minnesota showed it quite possible toidentify 10 to 12 hybrids that flowered within 25 GDU (1 day) of oneanother. The second requirement is more difficult because seed companiesdo not share pedigree information readily. But selecting hybrids fromdifferent companies, though not foolproof, is a reasonable starting point, asour field trials have clearly shown.

In summary, this field study shows that out-crossing maize hybridscan provide a free yield advantage beyond that expected from maximizingcrop growth rate during flowering. The yield advantage results from anincrease in sink demand (grain number and size), which is consistent withthe conclusion that maize is a sink limited crop.

IV. REPRODUCTIVE DEVELOPMENT SEED FORMATION

Under most growing conditions, grain yield in maize and soybean isonly a fraction of the maximum yields recorded for these crops. Theformation and development of the reproductive sinks, which are theeconomically valuable parts of the crop, are highly vulnerable to stresses,particularly water stress. Lack of soil moisture during flowering and earlyseed formation decrease the number of grains that develop. And moisture

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stress during seed filling results in smaller grains. In both soybean andmaize, the period of seed formation is the most sensitive to drought in termsof yield losses. The impact of drought decreases dramatically as the grainapproaches physiological maturity.

Early reproductive development is particularly vulnerable to droughtbecause much of the development involves expansion growth, which isinhibited severely by lack of water. In maize, the inhibition of growth leadsto two important problems asynchrony in male and female flowerdevelopment, and abortion of newly formed zygotes with the ovaries. Thenext sections describe the yield losses that occur in maize due to thesedevelopmental problems, and discusses the central role of assimilatesupply 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 Mexicoclearly underscore the importance of maintaining synchrony between maleand female flower development to improve yield performance of maizeunder severe drought conditions (Edmeades et al., 2000). Recurrentselection for improved grain yield under severe drought producedgenotypes with a shorter anthesis-silking interval (ASI) and more rapid eargrowth rate during drought. There was no yield advantage under irrigatedconditions, but selection increased the proportion on plants in the popu-lation that produced a seed-bearing ear.

Presumably, the shorter ASI increased the number of successfulpollinations of exposed silks. Breeders routinely select for close synchronybetween pollen shed and silk emergence in the hopes that all the silks willemerge when there is sufficient pollen being shed to ensure theirpollination. As drought inhibits ear and silk growth, an increasing number offlowers fail to become pollinated. Is the solution to this dilemma ofasynchrony an increase in the amount or duration of pollen shed, or a

change in the pattern of silk emergence? The distinction between these twopossibilities is important because they lead to very different selectionstrategies.

To answer this question, Bassetti and Westgate (1994) establisheda number of asynchronous plots within a large field, which provided a singlesource for pollen shed. Asynchrony included silk emergence prior to pollen

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shed (protogyny) as well as silk emergence after pollen shed (protandry).As expected, maximum kernel set occurred in plots whose silks began toemerge within one or two days of anthesis (50% of plants shedding pollen.Kernel set decreased dramatically in plots whose silk emergence startedafter the peak rate of pollen shed. By examining the pattern of kernel seton ears collected from the various asynchrony plots, they could determinewhether silk emergence or pollen shed limited kernel set. There wareperfect kernel set only on ears whose silks began to emerge within one dayof anthesis. Ears collected from plants whose silks began to emerge later(3, 5, 7, 9, 11 days) showed progressively greater loss of kernels at tippositions, ultimately progressing to the base of the ear. But ears with 3, 5or 7 days of anthesis all had perfect kernel set in the lower portion of theear (positions 5-15). This result indicated that the intensity of pollen shedwas 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 ofsilk emergence. With asynchrony beyond 7 days, loss of kernels resultedfrom lack of silk emergence and lack of sufficient pollen.

The results of this study indicated that late emerging silks were atrisk of not being pollinated even under well-watered conditions. Any delayin ear development or silk growth due to drought would only worsen thissituation. Bassetti and Westgate (1994) also observed that plots whosesilks began to emerge in advance of pollen shed by as many as six daysalso had a high level of kernel set and grain yield. The success of theseprotogynous plots suggests that one possible strategy to overcome thenegative effects of drought on the synchrony between silk emergence andpollen shed is to select for genotypes that naturally initiate silk emergenceprior to pollen shed. The immediate advantage of this shift in developmentin favor of earlier silk emergence is that any stress-induced delay in silkemergence would actually improve the synchrony in flowering. A subtler,but equally important, benefit of selecting for protogynous plants is theincreased priority for ear growth prior to anthesis.

These results also highlighted the need to define the floweringprocess in maize on a more rigorous quantitative basis than that currentlybeing used to define dates of silking and anthesis. Silk emergence on anindividual ear is a progress process, which may take up to 10 days tocomplete. Likewise, the process of pollen shed from an individual tasselprogresses in intensity over the course of several days. The process of

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pollination itself depends not on the percentage of the population sheddingpollen or silking, but on the actual density of pollen grains being shed, andthe number of silks that are exposed to that pollen each day. By exposingreceptive silks on different plants to a wide range of pollen densitiesoccurring naturally in the field, Bassetti and Westgate (1994) discoveredthat >95% of all exposed silks were successfully pollinated when thedensity of pollen shed reaching the silks was >125 grains cm-2 d-1. At lowerdensities of pollen shed, the percent kernel set decreased rapidly. Thisminimum density of pollen shed was nearly identical to that observed in theasynchrony experiments described earlier. With these basic quantitativemeasures of flowering dynamics and a curve relating pollen density tokernel set, it is now possible to predict in a quantitative manner the potentialnumber of kernels set each day in the field, and the potential number ofkernels 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 2to 4 days after anthesis. Afterwards, kernel set decreased dramaticallybecause silk emerge too late to become pollination. This approach, ofcourse, provides potential kernel numbers because stress-induced abor-tions have not been taken into account.

Even if pollination is successful, fewer kernels may develop underdrought conditions because a higher percentage of zygotes abort a fewdays after fertilization (Westgate and Boyer, 1986). For plant growing in thefield, a short-term water deficit during pollination can decrease kernelnumber per ear by 50% (Schussler and Westgate, 1994); the same level ofwater stress imposed on the same genotype grown in a growth chambercan cause a complete failure of kernel set (i.e. 100% abortion) (Schusslerand Westgate, 1991). Results from a large number of related studies aimedat understanding the physiological basis for this increase in kernel abortionhave lead to the conclusion that abortion is directly related to the inhibitionof ovary growth. Regardless of genotype, growth conditions, or stress level,inhibition of ovary growth lead to a decrease in kernel number per ear. Inall cases, plants were hand pollinated with abundant pollen. Measurements

of ovary weight in maize populations selected for short ASI during droughtsupport this conclusion. Plants with short ASI under drought conditionshave larger ovaries at the time of pollination. The practical outcome of thesestudies is that maintenance of rapid ovary growth is essential for high kernelset when stress occurs during pollination.

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Assimilate supply and carbohydrate metabolism

The decrease in kernel numbers in response to shading, decreasedkernel numbers per plant at low IPAR, and the severe inhibition ofphotosynthesis at low leaf water potential, all imply that the inhibition ofovary growth during drought is somehow linked to the current supply ofphotosynthate. The model relating ovary growth to photosynthate supplyproposed by Zinselmeier et al. (1999) suggests that rapid ovary growthoccurs when there is an ample supply of photosynthate from currentphotosynthesis and from reserves. Under mild stress conditions,photosynthesis is inhibited and ovaries depend on mobilized reserves tocontinue growing. As stress becomes more severe, lack of currentphotosynthate and depletion of reserves cause the ovaries to abort. If thismodel is accurate, it should be possible to maintain the supply of

photosynthate to the ovaries under stressful environments. First, and mostobvious, is maintaining the production of photosynthate at low leaf waterpotential. To the authors knowledge, there are no published reportsindicating this is possible. Small improvements associated with osmoticadjustment have not been sufficient to sustain reproductive development. Asecond possibility is to increase the contribution of assimilates remobilizedfrom temporary storage tissues, such as the stem internode, and rachis.Third, sustaining metabolic activity within the water stressed ovaries couldincrease partitioning of available assimilate to the ear.

To be successful with the latter two strategies, a number ofphysiological barriers need to be overcome. First is the fact that thedeveloping ovaries are competing with a large number of well-establishedsinks. These sinks have priority for assimilates from both current andreserve sources. Second is the fact that the temporary storage tissues(stem internodes, rachis) are still active sinks during pollination. Theycontain very high concentrations of sugars, but the sugar is primarilyglucose, which cannot be remobilized. The third barrier to overcome is theinhibition of carbohydrate metabolism within the ovary itself. This inhibition

of metabolism makes this weak sink an even poorer competitor forassimilates.

To determine which of these barriers was most important toovercome, it was necessary to resolve whether the failure of kernels todevelop during drought was due entirely to the lack of current assimilatesupply. This was done by comparing the kernel set in plants whose

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photosynthesis rates were inhibited to the same extent and duration by lowleaf water potential or by low light intensity. Presumably, both treatmentswould cause the same reduction in kernel set if current assimilate supplycontrolled ovary abortion. The results of this experiment indicated that lackof current photosynthate accounted for about 70% of the kernel lossobserved in droughted plants. The additional loss of kernels was due toanother, as yet unknown, factor (Schussler and Westgate, 1991). Sucrosefeeding experiments, in which supplemental sucrose was supplied by steminfusion, lead to the same basic conclusion. Adding enough sucrose toaccount for the sugar that would have been produced had photosynthesisbeen able to continue at low leaf water potential, recovered about 70% ofthe kernels lost in droughted plants without stem infusion. Relatedexperiments proved that sucrose was the active agent causing the recoveryof kernel numbers (Zinselmeier et al. 1995, 1999).

These experiments clearly demonstrated that maintaining thecurrent supply of photosynthate was critical for improving kernel set duringdrought. But it is not realistic to infuse sucrose into plants in the field! Apossible alternative is to increase the contribution of reserve sugars whenphotosynthesis is inhibited. To test this possibility, three treatments wereestablished in the field designed to vary the level of reserve sugars in theplant prior to imposing a water deficit during pollination. A 50% shadetreatment decreased sugar levels (and concentration) relative to the controlplants in full sun. And a widely spaced treatment increased sugar levels,presumable to the genetic potential for the hybrids in the study. Atpollination, a water stress of similar intensity and duration was imposed onall three treatments and plants were hand pollinated with abundant pollen.The inhibition of photosynthesis was the same in all three treatments aswell. The control plants at a normal plant density in full sun set about 50%fewer kernels when water stressed during pollination. Shaded plants with alower level of reserves prior to pollination set even fewer kernels. But theincreased accumulation of reserve sugars in the spaced plants did notrender them less sensitive to the water stress. Thus, is was possible to

make plants more sensitive by shading, but it was not possible to decreasetheir sensitivity by increasing the level of reserves (Schussler andWestgate, 1994).

Examination of the type of sugars accumulating in the steminternodes and rachis (cob) at the time of pollination, revealed why alteringsugar levels along would not be sufficient to increase assimilate availability

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to the developing ovaries. At pollination, well over 30% of the weight of thecob is in the form of sugars. But only about 2% of that sugar is in a formthan can be remobilized, i.e. sucrose. Likewise, the sugars in the ear stalk(shank) are predominantly reducing sugars (glucose + fructose); sugars inthe stem internode below the ear node are about equally distributedbetween reducing sugars and sucrose. Thus, none of these structures is anideal source of sucrose for remobilization. In fact, just the opposite occurswhen 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 assimilateduring pollination. High levels of acid invertase (AI), which is typical ofgrowing tissues, in the cob at this time support the accumulation of glucose.And the inhibition of AI in droughted plants is consistent with theaccumulation of sucrose.

It will be exceedingly difficult to alter the pattern of sucroseaccumulation in the stem internodes, cob and shank tissues given ourcurrent state of knowledge about mechanisms of sugar metabolism andstorage in these tissues. The mechanism(s) of sucrose import and exportare not known. The biochemistry of carbohydrate metabolism is not fullycharacterized. Tissue- and temporally-specific promoters are lacking forpossible transgenic approaches. And, most importantly, the pattern ofsucrose accumulation is coupled to tissue development. It likely will benecessary to alter development of these structures in order to accelerate orenhance their capacity for exporting sucrose during pollination.

The fact that not all of the kernel loss in water stressed plants couldbe accounted for by lack of assimilate supply implied that other factors alsocontributed to the increase in kernel abortion. The failure of kernels todevelop when pollinations occurred at low ovary water potential suggestedthat kernel set might depend on conditions within the pistillate flowersthemselves. Preliminary measurements on isolated ovaries showed thatwater decreased the capacity of ovaries to utilize sucrose in vitro (Schussler

and Westgate, 1991). A developmental profile of the carbohydrate status ofovaries samples from well-watered and water-stressed plants revealed thata brief water deficit at silk emergence dramatically altered the reducingsugar, sucrose, and starch levels within the ovaries. Most notable was alarge increase in the amount and concentration of sucrose relative to thecontrol plants. The rapid decrease in sucrose content at silk emergence inthe control plants may serve to maintain sucrose unloading from the phloem

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into the pedicel region of the ovary. If so, the high concentrations ofsucrose that develop in water stressed ovaries may limit the capacity forcontinued phloem unloading, thereby decreasing ovary sink strength. Thispossibility is supported by estimates of sugar concentrations in the ovaryapoplasm (Westgate, unpublished), which clearly indicated a largedecreased in reducing sugar/sucrose ratios in the apoplasm of water-stressed ovaries. This result suggested that the capacity for sucrosehydrolysis had been impaired. Measurements of ovary acid invertaseactivity indicated that, indeed, extractable acid invertase activity within theovaries was dramatically inhibited at low ovary water potential. Thephysiological basis for the inhibition of invertase activity is not fullyunderstood, but evidence from Anderson et al. (2000) shows thattranscription of the soluble form of acid invertase (Ivr2) decreases duringwater stress. Parallel analyses of the insoluble form of acid invertase (Ivcw)

have not been reported. But the activities of both the soluble and insolubleforms of invertase are inhibited to the same extent by water deficits(Zinselmeier et al., 1995). Importantly, the level of (insoluble) invertaseactivity is directly related to the rate of ovary growth. The recovery of kernelnumbers in response to stem infusion of sucrose corresponds to a recoveryof ovary acid invertase activity (Zinselmeier et al., 1999). These resultsprovide strong support for the central role of carbohydrate metabolism inestablishing the young kernels as a sink for photosynthate. Water stresscaused a lesion in carbohydrate metabolism within the ovaries, which mustbe overcome to increase kernel set during drought.

Could this lesion in metabolism also explain the more rapid loss ofstarch within water-deficient ovaries? Typically during silk emergence andpollination, ovary starch levels are increasing slowly (actually declining on aconcentration basis). But the level and concentration of starch decreasedramatically when water is withheld, even though sucrose concentrationsare well above control levels. Evidently the sucrose that accumulated,whether from starch hydrolysis or phloem unloading, is not beingmetabolized by the ovaries. Sucrose infusion into the stems of water

stressed plants reverses the drought-induced loss of starch. And as wasthe case for invertase activity, the recovery of ovary starch level is closelycorrelated with kernel set (Zinselmeier et al. 1999). Water stress had littleimpact on activities of enzymes in the pathway from glucose to starch, suchas ADP-glucose pyrophosphorylase or starch synthases. The mostsensitive enzymes were the invertases. These results indicate that loss ofinvertase activity apparently is the key metabolic lesion caused by a water

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deficit. It explains the rapid accumulation of sucrose and the loss of starchin the ovaries. And the subsequent decrease in reproductive sink strengthwhen drought occurs during pollination.

In summary, grain yield in maize remains highly vulnerable to waterdeficits during pollination in large part because ovary carbohydratemetabolism is inhibited. This inhibitions disrupts the flux of assimilates tothe ovaries, and slows ovary growth. The decrease in ovary growthtranslates directly to an increased probability of reproductive failure i.e.kernel abortion.

Current and future strategies to maintain zygote (kernel) deve-lopment during drought include developing a greater understanding of themolecular controls of sucrose and starch accumulation in storage tissues

prior to anthesis; determining the molecular basis for the inhibition of ovaryinvertase activity at low ovary water potential, and identifying genes whoseactivity 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 onlyreproductive adjustment possible when canopy photosynthesis is inhibitedby adverse environmental conditions is to limit the extent of seeddevelopment. Fortunately, the sensitivity of grain yield to drought decreasesas reproductive development progresses towards physiological maturity inboth maize and soybeans.

Drought during seed filling generally results in the production ofsmaller seeds. Possible physiological explanations for producing smallerseeds include loss of current assimilate supply due to accelerated leafsenescence, decreased sink capacity possible resulting from fewer cells orless cell volume, or inhibition of storage product synthesis due to premature

desiccation. The remainder of this review will consider the evidencesupporting these possibilities for the maize and soybean crops.

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Rate and duration of seed filling

Under well watered and fertilize conditions, maize kernels typicallyachieve their maximum volume early in development. Kernel moistureremains fairly stable during linear grain filling, but begins to decrease whilekernels are rapidly filling. Maximum dry weight is achieved during a periodof terminal desiccation.

In a greenhouse study, Westgate and Grant (1989) showed that abrief water deficit during linear filling had little impact on dry matteraccumulation of maize kernels, but did cause a substantial decrease inkernel water content. The change in water content of the kernels was notreflected in kernel water potential, which did not change despite a largedecrease in leaf water potential. The remarkable stability of kernel water

potential in the water-deficient plants implies that developing grains arehydraulically isolated from the water status of the plant. The actualmechanism that makes this possible is not known. In maize and soybean,there are no direct vascular connections between the maternal tissue andthe 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 potentialswithin the developing seed should allow metabolism to continue even undersevere drought conditions.

These results of this short-term experiment indicated two thingsabout grain development during drought. First, the smaller grains thattypically develop under drought conditions probably result from a shortergrain filling period, rather than a decrease in grain fill rate. Second, droughtdid indeed alter the water status of the seed, by decreasing its watercontent, even though the water loss was not evident from measurements ofgrain water potential. This suggested that there might be connectionbetween grain moisture content and the duration of grain filling. To test thispossibility, a long-term water deficit was imposed on plant grown in the

field. Irrigation water was withheld after seed number was established, sothat any yield adjustments must result from a decrease in grain weight. Thewater deficit decreased ear-leaf water potential over a period of severalweeks, and caused the leaves to senesce prematurely. Leaf photosynthesiswas inhibited at leaf water potentials below 1.2 MPa. After this point, grainfilling depended primarily on mobilization of reserves. Periodic measu-rements of grain mass showed that kernels on water deficient plants

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continued to fill at the control rate, confirming the results of the short-termgreenhouse study. The water-deficient plants produced smaller grainsbecause they ceased filling sooner after anthesis. The decrease in grainyield from 11.1 to 9.1 Mg ha-1 in this experiment was due entirely to thedecrease in grain size. The embryos within the kernels showed the samegeneral response. Water deficient plants produced smaller embryosbecause 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 carbohydratereserves in the stem are remobilized to support kernel growth, and thatunder severe stress, grain growth will continue until these reserves arenearly 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 thewater-stressed plants relative to levels in the well-watered controls. Butcarbohydrates in the vegetative stalk were not completely depleted whengrain filling ceased (about 50 days after anthesis), and carbohydratesbegan to accumulate thereafter. Also, there was no indication thatcarbohydrate accumulation in the grain was altered due to a lack ofphotoassimilate. These data support the conclusion that assimilate supplywas not the primary cause of a shorter filling period in the water deficientplants. The fact that carbohydrates continue to accumulate in the vegetativestalk of well-watered plants throughout grain filling supports this conclusion.

Measurements of grain water status showed that kernels on thewater-deficient plants reached the same maximum water content as did thewell-watered plants, but began to lose moisture sooner (but not faster) afteranthesis. This premature desiccation was consistent with the decrease inmoisture content observed by Westgate and Grant (1989) earlier. The factthat the kernels on the water-deficient plants achieved the same maximumwater volume as did kernels on well-watered plants indicated that thepotential grain size was the same in both treatments. But the premature

desiccation raised the possibility that the change in grain water status earlyin filling actually affected the duration of the grain filling process. If so, thereshould be a consistent relationship between grain moisture status and graindevelopment, regardless of the treatments imposed. When compared on atissue moisture basis, the developmental pattern of kernel and embryowater potential were nearly identical for the well-watered and water-deficient treatments. Likewise, data examined from other studies shows a

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very consistent pattern of dry matter accumulation when development isnormalized on a kernel moisture basis. Regardless of genotype orenvironment, kernels ceased to accumulate dry matter at about 30 %moisture (Egli and Tekrony 1997, Westgate and Boyer, 1986). The same istrue of kernel development when water deficit treatments are imposed atdifferent times during grain filling. Withholding water from plants at thekernel blister stage (rapid water uptake), dough stage (early grain filling), ordent stage (late grain filling) had dramatically different effects on final kerneldry matter. But kernels in all treatments ceased to accumulate dry matter atabout the same moisture content approx. 30%.

Evidence from a host of sources including in vitro measurements ofenzyme activities at low moisture contents (Rupley et al., 1983), enzymeactivities extracted from dry seeds (Muhitch, 1991), and the physical

properties of water in dry seeds (Vertucci, 1989) all point to the conclusionthat the osmotic conditions in the endosperm and embryo late in grain fillingdo not directly inhibit the activity of enzymes responsible for storage productsynthesis. Rather, the decrease in storage product synthesis probablyreflects a decreased capacity for protein synthesis (Bewley, 1981; Kermodeet al., 1989). Desiccation itself may be a developmental queue forterminating transcription and translation of synthetic proteins and initiatingthe synthesis of proteins required for desiccation tolerance, eg. dehydrins.If so, the premature desiccation caused by drought during grain fillingcauses smaller kernels to be produced because they reach the minimummoisture content that supports metabolism sooner after anthesis.Maintaining grain filling then requires modifications in grain developmentthat either increase the maximum water volume early in filling, or preventpremature desiccation from occurring. Current studies are investigating theimportance of increasing maximum cell volume as a means to achieve thisgoal.

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 desiccatesrapidly thereafter. As was the case in maize, drought during grain fillingshortens the duration of filling, resulting in smaller seeds (Meckel et al.,1984). Water deficits severe enough to inhibit leaf photosynthesiscompletely had little effect on the rate of dry matter accumulation by theembryo at least on the short term (Westgate et al., 1989). Part of thereason embryo could continue to develop was that they exhibited the same

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type of hydraulic isolation from changes in plant water status that wasobserved in maize. There also was an increased rate of mobilization ofcarbohydrate and reduced N from the vegetative tissues and pod wall.Interestingly, the embryos from water deficient plants also exhibited anincreased capacity for sucrose uptake from the surrounding free space,which apparently compensated for the decrease in apoplast sucroseconcentration being by the maternal tissues. This study indicated thatembryo growth rate is maintained in soybean by a coordinated shift inmetabolism among the vegetative and reproductive tissues. Thiscoordinated adjustment allows embryo growth to continue until reserves aredepleted.

The fact that soybean embryos reached maximum water volumeand dry weight at the same time suggest that embryo water status might

also be an important determinant of grain fill duration. In vitro culturestudies show that soybean cotyledons will continue to accumulate drymatter as long as can continue to expand in water content and volume.Embryo removed from pods early in grain filling achieve much greater massthan their in planta counterparts (Egli, 1990). This type of evidence impliesthat embryo mass in planta is limited, at least in part, by the surroundingpericarp (pod) walls. This possibility was tested by placing small tubesaround developing pods to restrict their expansion. The results clearly showthat 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 ina similar manner has not been examined. But it is a reasonable possibilitysince numerous studies confirm that, regardless of treatment or growthconditions, 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 continuesuntil maximum water volume is achieved. In seeds that store predominately

starch (egg. maize, wheat) grain fill duration is determined by the maximumcell volume established early in seed development, and by the onset ofdesiccation later in development. Drought shortens the duration of grainfilling by causing premature desiccation and/or by limiting the maximum cellvolume.

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VI. CONCLUDING REMARKS

These studies have raised a number of questions regarding thecontrol of grain filling and the impact that adverse environmental conditionshave on the capacity of developing seeds to reach their potential size. How

do environmental conditions early in grain filling regulate the duration of thefilling process? Under what conditions does lack of assimilate supply limitthe duration of grain filling, rather than seed water status? And finally, howis seed composition (eg. protein, oil, starch content) maintained underconditions that alter the rate and duration of grain filling? Because lack ofavailable soil moisture is the primary environmental limitation for high grainyields, answers to these questions will lead to rational targets for geneticmodification, physiological selection, and practical management strategiesto improve grain production across a range of environments.

REFERENCES

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BASSETTI, P.; WESTGATE, M.E. Floral asynchrony and kernel set inmaize quantified by image analysis. Agronomy Journal, v.86, p.699-703, 1994.

BEWLEY, J.D. Protein synthesis. In: PALEG, L.G; ASPINALL, D. (eds.).The Physiology and Biochemistry of Drought Resistance inPlants. Sydney: Academic Press, 1981. p.261-282.

BRADFORD, K.J. Water stress and the water relations of seed

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CHRISTY, A.L.; PORTER, C.A. Canopy photosynthesis and yield insoybean. In: GOVINDGE (ed.). Photosynthesis: Development,Carbon Metabolism and Plant Productivity. Academic Press, 1982.v.2, p.499-511.

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CHRISTY, A.L.; WILLIAMSON, D.R. Characteristics of CO2 fixation andproductivity of corn and soybeans. In: LUDDEN, P,W.; BURRIS, J.E.(eds.). Nitrogen Fixation and CO2 Metabolism. Elsevier Science Pub.Co., 1985.

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FLENET, F.; KINIRY, J.R.; BOARD, J.E.; WESTGATE, M.E.; REICOSKY,D.C. Row spacing effects on light extinction coefficients of corn,sorghum, soybean, and sunflower. Agronomy Journal, v.88, p.185-190, 1996.

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desiccation and abscisic acid in seed development: A comparison ofthe evidence from whole seeds and isolated embryos. In: STAN-WOOD, P.C.; M.B.; McDONALD, M.B. (eds.). Seed Moisture.Madison: Crop Sci. Soc. Amer., 1989. v.14, p.23-50.

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MECKEL, L.; EGLI, D.B.; PHILLIPS, R.E.; RADCLIFFE, D.; LEGGET, J.E.Effect of moisture stress on seed growth in soybeans. AgronomyJournal, v.76, p.647-650, 1984.

MUHITCH, M.J. Tissue distribution and developmental patterns of NADH-dependent and ferridoxin-dependent glutamate synthase activities inmaize (Zea mays L.) kernels. Physiologia Plantarum, v.81, p.481-488, 1991.

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fisiologia sojamilho mark e. westgate

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