Published in Crop Sci. 43:2083-2088 (2003).
© 2003 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
CROP PHYSIOLOGY & METABOLISM
Short Periods of Water Stress during Seed Filling, Leaf Senescence, and Yield of Soybean
R. E. Brevedana and
D. B. Egli*,b
a Dep. of Agronomy, Universidad Nacional del Sur, 8000, Bahia Blanca, Argentina
b Dep. of Agronomy, University of Kentucky, Lexington, KY 40546-0091
* Corresponding author (degli{at}uky.edu).
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ABSTRACT
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The effects of short periods of water stress during seed-filling on leaf senescence, seed-fill duration, and yield of soybean [Glycine max (L.) Merrill] are not well understood. Short stress periods were investigated in two greenhouse experiments with cultivar Elgin 87 grown in soil-filled pots. All pots received adequate water until the beginning of growth stage R6 when a continuous water-stress treatment (pots received 40% of the water needed to bring controls to pot capacity) was initiated and maintained until maturity. Water stress was relieved in other pots (watered as the control) after 5 or 13 d in Exp. 1 and 3 or 6 d in Exp. 2. Each treatment was replicated six to eight times in a completely randomized design. The carbon exchange rate was rapidly reduced by continuous water stress resulting in earlier maturity, significantly lower yield (39%), and smaller seeds (25–33%). The carbon exchange rate rapidly increased to near control levels in the early stress-relief treatment, but it was always less than the control for the rest of seed filling. These plants matured sooner and produced significantly lower yields (10–23%) and smaller seeds (9–17%) than control plants. Late stress relief also reduced yield and seed size relative to the control. Yield and seed size of both stress relief treatments, however, were greater than the continuous stress treatment. Water stress-induced acceleration of senescence could not be stopped by eliminating the stress after a short period. Short periods of water stress during seed filling may, therefore, have larger than expected effects on yield.
Abbreviations: CER, carbon exchange rate
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INTRODUCTION
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THE LENGTH of the seed-filling period is an important determinate of yield of all grain crops including soybean (Egli, 1998). Seed-fill duration is under genetic control (Metz et al., 1985; Smith and Nelson, 1987), and it is sensitive to temperature (Egli and Wardlaw, 1980) and stress. Nitrogen (Egli et al., 1985; Hayati et al., 1995) and water (Meckel et al., 1984; Smiciklas et al., 1989; Frederick et al., 1991) stress during seed filling shortened the seed-filling period and reduced yield.
Water stress generally accelerates leaf senescence (Thomas and Stoddart, 1980; Gan and Amasino, 1997) as shown for chick pea (Cicer arietinum L.)(Davies et al., 1999), maize (Zea mays L.) (Aparicio-Tejo and Boyer, 1983), soybean (de Souza et al., 1997), and sunflower (Helianthus annuus L.) (Whitfield et al., 1989). Soybean plants subjected to continuous water stress from the beginning of growth stage R6 (early in seed filling) until maturity lost N and chlorophyll from their leaves more rapidly than controls in two greenhouse experiments (de Souza et al., 1997). Stress shortened the seed-filling period (R7 occurred up to 7 d earlier) resulting in smaller seeds (maximum reduction of 32%) and lower yield (up to 44%).
Water stress initiated during vegetative or early reproductive growth of soybean usually reduces yield by reducing the number of seeds per unit area (Doss et al., 1974; Sionit and Kramer, 1977; Ashley and Ethridge, 1978; Egli et al., 1983; Korte et al., 1983) while stress during seed filling reduces seed size (weight per seed) (Ashley and Ethridge, 1978; Egli et al., 1983; Korte et al., 1983; Meckel et al., 1984; Smiciklas et al., 1989; Vieira et al., 1992; de Souza et al., 1997). Seeds per unit area and yield can be reduced by short periods of stress during flowering and pod set (Shaw and Laing, 1966), but the effect of short periods of stress during seed filling on senescence, seed-fill duration, seed size and yield are not well documented. Shaw and Laing (1966) withheld water for 1-wk periods during seed filling, reducing seed size and yield, but the effects on photosynthesis, leaf senescence, and seed-fill duration were not determined.
Continuous stress during seed filling accelerates senescence and reduces yield (de Souza et al., 1997), but short periods of stress are probably more common in many humid environments where soybean is grown. Hence, the objective of this work was to test the hypothesis that short periods of water stress during seed filling in soybean would initiate a nonreversible acceleration of leaf senescence, resulting in a shorter seed-filling period, smaller seeds, and lower yields.
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MATERIALS AND METHODS
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Seeds of soybean cultivar Elgin 87 (Maturity group II) were planted in 4.0-L plastic pots filled with 3.75 kg of silt loam surface soil in a greenhouse at Lexington, KY (38° 2' N latitude and 84°29' W longitude) on 29 July 1998 (Exp. 1) and 2 March 1999 (Exp. 2). Five seeds were planted in each pot and the seedlings were thinned to one per pot at roughly growth stage V1 (Fehr and Caviness, 1977). Greenhouse air temperature was maintained between 20 and 30°C and the plants in both experiments reached growth stage R6 at approximately 60 d after planting. Supplemental radiation (approximately 100–200 µmol m-2 s-1) was provided by high pressure sodium lamps.
The plants were fertilized at approximately weekly intervals with 0.6 g pot-1 of a complete fertilizer (20-20-20; Peters Professional fertilizer, Peters Fertilizer Products, W.R. Grace & Co. Fogelsville, PA). The seeds were not inoculated with Bradyrhizobium japonicum and the roots were not nodulated.
All plants received adequate supplies of water until the beginning of growth stage R6 when two levels of soil moisture were imposed. Pot water holding capacity was estimated when the treatments were initiated by saturating pots with water and weighing them at dawn, after they had drained overnight. Pots were weighed each day in the morning, at midday, and in late afternoon and water was added after each weighing to bring the pots in the nonstressed control treatment to pot capacity. At the same times, the continuous-stress treatment received 40% of the water added to the nonstressed pots. The water supplied to some pots in the continuous-stress treatment was increased to the nonstress control level 5 and 13 d after the continuous stress was initiated in Exp. 1. The 13-d treatment occurred late in seed filling when senescence was nearly complete, so the stress intervals were shortened to 3 and 6 d in Exp. 2. All treatments were maintained until the plants reached growth stage R8 (95% brown pods).
Carbon exchange rate (CER) of a fully expanded leaf from a constant nodal position near the top of the main stem of five plants from each treatment was measured at mid-day with a LI-6400 portable photosynthesis system (LI-COR, Lincoln, NE) at approximately 2-d intervals. A LI-COR 6400-02B Red/Blue light source was used to maintain photosynthetically active radiation at 1500 µmol m-2 s-1 during the measurements.
Whole plants were harvested from six to eight pots when the continuous-stress treatment was initiated (1 d before initiation in Exp. 2), when the stress-relief treatments were applied and at growth stage R7 in Exp. 1 or 5 d after the second stress-relief treatment was applied in Exp. 2. Total leaf area (LI-COR Model 3100 leaf area meter) (4 replications) and seed dry weight were determined and the youngest fully expanded leaf was harvested for N, chlorophyll, and carbohydrate determinations. Chlorophyll from two 12-mm diameter leaf punches from the center leaflet was extracted overnight in 5 mL of ethanol and determined as described by Holden (1976). The area of the two side leaflets was determined with a LI-COR 3100 leaf area meter and the leaflets were freeze dried, weighed, and ground for analysis. Total N was determined by the Kjeldahl method (Nelson and Sommers, 1973; Heberer et al., 1985). Soluble sugars, including reducing sugars, hydrolyzed sucrose, and other nonreducing sugars, and total nonstructural carbohydrates (after hydrolyzing starch with 
-amylase and amyloglucosidase) were extracted with benzoic acid and determined colormetrically (Heberer et al., 1985). Starch (expressed in glucose units) was taken as the difference between total nonstructural carbohydrates and soluble sugars multiplied by 0.9.
A completely randomized design with six to eight replications was used in both experiments.
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RESULTS
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Imposition of water stress caused a rapid reduction in CER in both experiments (Fig. 1) and the CER of plants from the continuous-stress treatment approached zero well before nonstressed control plants as reported previously (de Souza et al., 1997). The other indicators of senescence, including leaf area, and leaf N and chlorophyll levels (Fig. 2 and 3), also declined more rapidly in the continuous-stress treatment than in the nonstressed control.
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Fig. 1. Effect of water stress on carbon exchange rate (CER) during seed filling. Stress was applied early in seed filling at the beginning of growth stage R6. The time of application of the stress-relief treatments is shown on the x axis by S1 (early) and S2 (late). Bars represent ± one standard error of the mean. Some error bars were omitted to avoid excessive clutter.
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Fig. 2. Effect of water stress on leaf N and chlorophyll levels during seed filling, Exp. 1. Stress was applied early in seed filling at the beginning of growth stage R6. The time of application of the early stress-relief treatment is shown on the x axis by S1. The late stress-relief treatment had minimal effects on leaf N and chlorophyll levels and the data are not included. Treatments had no significant (P = 0.05) effect on leaf N levels at growth stage R7 (mean = 0.88 g m-2), but chlorophyll levels of the stressed treatments (180 g m-2) were significantly (P = 0.05) less than the control (230 g m-2). Means with asterisks are significantly (P = 0.05) lower than the control.
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Fig. 3. Effect of water stress on leaf area, and leaf N and chlorophyll levels during seed filling, Exp. 2. Stress was applied early in seed filling at the beginning of growth stage R6. The time of application of the stress-relief treatments is shown on the x axis by S1 (early) and S2 (late). Means with asterisks are significantly (P = 0.05) lower than the control.
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Bringing the water level of the stressed plants back to control levels at 5 (Exp. 1) or 3 (Exp. 2) d after the stress was initiated rapidly (2–4 d) restored CER to levels near (Exp. 1) or equal to (Exp. 2) control plants (Fig. 1). Following this initial increase, the CER of these plants was always less than the control plants for the remainder of the seed-filling period. The response to stress relief at 6 or 13 d after stress initiation was much smaller than from the early treatment. Carbon exchange rate reached minimal levels first in the continuous-stress treatment, followed by the stress-relief treatments and then the control plants in both experiments (Fig. 1).
The other indicators of leaf senescence also responded to stress-relief with the decline in leaf area, chlorophyll, and N arrested when the stress was relieved and there was a tendency for the levels to remain between those of the control and continuously stressed plants (Fig. 2 and 3), although the differences were not always statistically significant.
The yield of plants exposed to continuous water stress was significantly (P = 0.05) less (39%) than the nonstressed controls (Table 1). The stressed plants matured sooner in Exp. 2, and produced significantly (P = 0.05) smaller seeds (25–33%) in both experiments. There was no significant effect of stress on pods per plant but there were small reductions in seeds per plant, suggesting that the stress was applied after the critical period for pod set (Egli, 1998), as intended. The yield of the early stress-relief treatment was not reduced as much (only 10–23% below the nonstressed plants) as the continuous-stress treatment. This reduction was also a result of smaller seeds (9–17%) and earlier maturity, relative to the nonstressed plants. The yield of the late stress-relief treatment was less than the early stress treatment but larger than the continuous-stress treatment, as was seed size, but these differences were not always significant (Table 1).
Soluble sugar levels in the leaves in both experiments did not change during the sampling period and were not affected by the stress treatments (average levels for all treatments were 1.40 ± 0.07 g m-2 in Exp. 1 and 1.60 ± 0.07 g m-2 leaf area in Exp. 2). Leaf starch levels of nonstressed control plants increased 33% during the early stages of seed filling in Exp. 1, but decreased by 62% in Exp. 2 (Fig. 4). Such variation among environments was reported previously (Egli, 1999) and it was attributed to changes in solar radiation and photosynthesis between the flowering and podset period, and seed filling. Leaf starch levels of the plants exposed to continuous water stress were significantly lower (P = 0.05) than the control by 5 to 6 d after application of the stress, as reported by de Souza et al. (1997), and both of the rewatering treatments stopped or slowed this decrease in starch levels. Most of the treatment differences had disappeared by physiological maturity in Exp. 1, but sampling stopped before physiological maturity in Exp. 2.
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Fig. 4. Effect of water stress on leaf starch levels during seed filling. Stress was applied early in seed filling at the beginning of growth stage R6. The time of application of the stress relief treatments is shown on the x axis by S1 (early) and S2 (late). The final sample in Exp. 1 was taken when each treatment reached physiological maturity (growth stage R7, Fehr and Caviness, 1977) and they are grouped together disregarding the time scale on the x axis. Means with asterisks are significantly (P = 0.05) lower than the control.
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DISCUSSION
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Our objective was to evaluate the effect of water stress during seed filling without reducing sink size, so the stress treatments were not imposed until the beginning of growth stage R6 to avoid inducing high levels of pod and seed abortion (Egli et al., 1983). Reducing sink size concurrently with reductions in photosynthesis would minimize change in source-sink ratios which could influence the response to the stress treatments. We were successful in inducing significant stress during seed filling with only small changes in sink size (seeds per plant). These results are consistent with earlier suggestions that the end of the critical period for pod and seed number determination was near the beginning of growth stage R6 (Board and Tan, 1995; Egli, 1998).
Continuous water stress accelerated leaf senescence, shown by rapid declines in CER, leaf N, chlorophyll, and leaf area, as reported previously (Sionit and Kramer, 1977; de Souza et al., 1997). Huber et al. (1984) also reported accelerated senescence in water- stressed soybean plants that were exposed to ambient or enriched CO2 (ambient + 300 µL L-1 CO2). The water stress induced acceleration of leaf senescence led to reductions in seed size and yield, also in agreement with previous reports (Sionit and Kramer, 1977; de Souza et al., 1997).
Relief from water stress increased CER immediately and also affected other indicators of senescence (leaf area, leaf N and chlorophyll). Huber et al. (1984) reported similar results on the CER of field-grown soybean plants; however, they did not report the reproductive growth stages when the stress was initiated and relieved. The senescence process, involving both a loss of photosynthetic capacity and cellular disassembly (Stoddart and Thomas, 1982) is highly coordinated (Crafts-Brandner et al., 1990), so it is not surprising that all aspects of senescence that we measured responded to the imposition and relief of water stress. Pic et al. (2002) also reported that all components of the senescence process of pea (Pisum sativum L.) responded to mild water stress.
Rewatering the plants after a relatively short stress period (3–5 d) did not completely eliminate the effects of water stress on the senescence process. In spite of the rapid recovery of CER, expected from previous reports for soybean (Huber et al., 1984) and other crops (Boyer, 1971), it was lower than the nonstressed control throughout seed filling in both experiments. This carry-over effect resulted in earlier maturity, smaller seeds, and lower yields in comparison to the nonstressed control.
Stored assimilates can serve as a buffer in plants experiencing water stress during seed filling (Ludlow and Muchow, 1990; Sadras and Conner, 1991). The proportion of yield from remobilized reserves may increase, but there may be no change in the absolute amount of remobilized assimilate (Bidinger et al., 1977; Hall et al., 1989). The water-stress treatments in our experiments induced substantial differences in leaf starch levels during seed filling (Fig. 4), but most of these differences disappeared by physiological maturity (Exp. 1), suggesting that water stress and stress relief had minimal effects on starch levels in abscised leaf tissue at the end of seed filling.
Leaf senescence was initiated sooner in the water-stressed plants than in controls, and, once initiated, it could not be stopped by rewatering the plants. Stoddart and Thomas (1982) suggested that stress-induced senescence, which may be different from programmed senescence, could be reversed if the stress was relieved before senescence progressed too far. Senescence had apparently progressed far enough after 3 to 5 d of stress in our experiments to be nonreversible. The level of stress that the soybean plant can tolerate without inducing irreversible senescence remains to be determined, but it is possible that both the degree of stress (i.e., magnitude of the reduction in leaf water potential) and the rate at which the stress develops may be important.
In many humid environments where soybean is grown, especially those with shallow soils that have low total water-holding capacity, short periods of water stress during seed filling may be more likely than long periods of continuous stress. The data presented here suggest that soybean yields may be more susceptible to these short periods of stress than expected. A relatively short period of stress during seed filling can have a significant impact on soybean yield (up to 23% in our experiments) and the effect may be relatively transparent to the producer until harvest. The traditional symptoms of water stress—wilted leaves—are usually not obvious; instead, the normal senescence process, with the usual visual manifestation of leaf yellowing and abscission, changes in pod color from green to brown, is simply accelerated. This acceleration is not obvious without comparison with nonstressed plants. Record high yields may require a complete absence of water stress during seed filling.
Our results were obtained in pots in a greenhouse where stress developed quickly (CER was reduced by nearly 70% in 3 d in Exp. 2), whereas water stress in the field would probably develop more slowly. More research is needed to define better the relationships among stress-induced acceleration of leaf senescence, stress levels, and the rate of stress development to provide better estimates of its potential effect in field environments.
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NOTES
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Published with the approval of the Director of the Kentucky Agric. Exp. Stn. as paper No. 03-06-001.
Received for publication January 31, 2003.
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ABSTRACT
INTRODUCTION
