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CROP PHYSIOLOGY & METABOLISM

Rising Atmospheric Carbon Dioxide and Seed Yield of Soybean Genotypes

Climate Stress Laboratory, USDA-ARS, Bldg 046A, 10300 Baltimore Avenue, Beltsville, MD 20705

Corresponding author (ziskal{at}ba.ars.usda.gov)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
If intraspecific variation to rising atmospheric CO₂ exists in soybean [Glycine max (L.) Merr.], such variation could be used to select for optimal, high-yielding cultivars. To quantify the range and determine the basis for variation in seed-yield with increasing CO₂, eight ancestral and one modern soybean cultivar differing in determinacy, maturity group, and morphology were grown to reproductive maturity at two CO₂ partial pressures, 40 Pa (ambient) and 71 Pa (elevated). Experiments were replicated three times in temperature controlled glasshouses during 1998 and 1999. Although all cultivars showed a significant increase in seed yield with elevated CO₂,(40%) Mandarin, an ancestral indeterminate cultivar, showed a greater relative response of seed yield to increased CO₂ than did all other cultivars (80%). The observed variation in seed yield response to CO₂ was not correlated with any vegetative parameter. At maturity, significant correlations in the relative response of seed yield to CO₂ were observed for both pod weight per plant and seed weight from branches. The later observation suggests that the sensitivity of seed yield response to CO₂ was associated with plasticity in the ability to form new seed in axillary branches in a high CO₂ environment. Genotypic differences in the seed yield response among existing ancestral soybeans suggests that sufficient germplasm is available for breeders to begin selecting lines which maximize soybean yield in response to increasing atmospheric CO₂.

Abbreviations: AHI, apparent harvest index • DAS, days after sowing • PPFD, photosynthetic photon flux density

	INTRODUCTION

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FEW STUDIES have attempted to utilize genotypic variation in the response to increasing atmospheric CO₂ as a means to maximize growth or yield within a given agricultural species. Significant variation in yield by elevated CO₂ has been observed among cultivars of cowpea [Vigna unguiculata (L.) Walp.] (Ahmed et al., 1993), rice (Oryza sativa L.) (Ziska et al., 1996; Moya et al., 1998), and wheat (Triticum aestivum L.) (Manderscheid and Weigel, 1997). Genotypic variation in the response of early growth of tomato (Lycopersicon esculentum Mill.) (Lindhout and Pet, 1990) and wild radish (Raphunus raphanistrum L.) (Curtis et al., 1994) to elevated CO₂ have also been observed. Heritable variation in the response to elevated CO₂ has, in fact been observed in wild radish with respect to stomatal response (Case et al., 1998). If variation can be exploited to convert additional atmospheric CO₂ into seed yield, then significant increases in productivity could be achieved with relatively low input and minor environmental costs.

It has been argued that empirical selection for yield will automatically select genotypes that are the most responsive to rising atmospheric CO₂ (Kimball, 1985). That is, in the future as atmospheric CO₂ continues to rise, breeders will naturally select the most CO₂ sensitive cultivar. However, it needs to be emphasized that many current cultivars utilized by breeders and growers generally show less seed yield response than vegetative response with a subsequent decline in apparent harvest index as CO₂ increases (Cure and Acock, 1986; Prior and Rogers, 1995). This has been observed not only for soybean (‘Bragg’, Baker et al., 1989; ‘Fiskeby’, ‘Clark’, Ziska et al., 1998), but also for rice (Moya et al., 1998) and wheat (Manderscheid and Weigel, 1997). This suggests that agronomic cultivars in current use may be ill-suited to maximize the seed yield response with increasing atmospheric CO₂; consequently, evaluation of a wider range of germplasm may be necessary to maximize the seed yield response to future CO₂ levels. At present, no systematic effort to select for CO₂ responsiveness for yield among soybean cultivars has been attempted.

To exploit genotypic variation efficiently, it is necessary to know which physiological or morphological traits are associated with the maximum seed yield response to elevated CO₂. Obviously, the primary basis for the increase in growth and yield is the CO₂-induced stimulation of photosynthesis. However, it can be difficult to predict the response of seed yield from individual leaf measurements since changes in the amount of acclimation or down-regulation can influence the long-term response of photosynthesis to elevated CO₂ (Bunce, 1992).

In contrast to interspecific comparisons (Bunce, 1997), no data have established whether intraspecific variation in growth stimulation by elevated CO₂ is related to differences in photosynthetic response or acclimation, although the possibility cannot be dismissed. Other responses are also affected by CO₂ and could alter the allocation or partitioning of photosynthate among different organs with subsequent affects on photosynthetic acclimation and productivity. In rice for example, the ability to respond reproductively to increased CO₂ in the field is associated with increased tiller formation (Moya et al., 1998). Newer cultivars which limit tillering show a poorer seed yield response to elevated CO₂ (Moya et al., 1998).

One difficulty in selecting soybean genotypes which are CO₂ sensitive is that space and time constraints limit the number of lines which can be examined concurrently at a high CO₂ environment. However, most U.S. genotypes were derived from a small number of ancestral soybean cultivars brought into the USA in the early 1900s (Carter et al., 1993). In the current experiment, we utilize these genotypes (which represent an assortment of morphologies, determinacies, and maturity groups) to assess the sensitivity of seed yield to an enriched CO₂ environment. By using ancestral lines as a starting point, we also attempted to identify characteristics associated with seed yield responsiveness to CO₂. Given the rapid rate of atmospheric CO₂ increase, and the time necessary for a new cultivar to be developed, quantification of genotypic variation in seed yield and the basis for such variation is a crucial step in any breeding effort to maximize yield with higher atmospheric CO₂.

	MATERIALS AND METHODS

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Experimental Treatments
Soybean was grown to maturity (March through July, Run 1; July through early December, Run 2; July through December, Run 3) in air-conditioned glasshouses located at Beltsville, MD in 1998 and 1999. Glasshouses were designed to maintain maximum and minimum temperatures between 31 and 17°C, respectively. Air temperature was monitored with shielded, aspirated thermocouples located near the top of each glasshouse. Blowers circulated air continuously through heat exchangers which produced an air speed of ca 0.5 m s^-1. Relative humidity inside the glasshouses was not controlled, but was at or near that of ambient outside air. Carbon dioxide partial pressure was controlled 24 h a day by a WMA-2 infra-red analyzer (PP systems, Haverhill, MA) which injected CO₂ if levels dropped below 36 and 70 Pa, respectively, for each glasshouse. The CO₂ treatments were switched between experimental runs to limit microclimate effects. No significant differences in average air temperature were observed during a given experimental run between glasshouses (23.2, 22.9°C; 21.5, 21.2°C and 21.9, 22.0°C for ambient and elevated CO₂ respectively). Average daily photosynthetic photon flux density (PPFD) inside the glasshouses was 21.3, 13.4, and 14.7 mol m^-2 day^-1 for Runs 1 to 3 respectively, with no difference in light interception between glasshouses in a given run. No supplemental lighting was used.

A 21x datalogger (Campbell Scientific, Logan, UT) recorded PPFD, temperature and CO₂ partial pressure in both glasshouses at 30-s intervals. Average daytime values of ambient and elevated CO₂ partial pressure were 37.8, 69.1; 37.7, 72.1, and 38.1, 71.2 Pa for Runs 1 through 3, respectively. Average 24-h values were higher than the set point for the ambient CO₂ treatment (43.0, 40.7, and 41.5 Pa for Runs 1–3), because of high (40–50 Pa) ambient nighttime CO₂ experienced at this site (see Ziska et al., 1998).

Cultivars and Growth Conditions
Seed from nine soybean cultivars, (eight ancestral and one modern) were used in all runs (Table 1). These cultivars represent a range of morphologies, indeterminate and determinate types, and maturity groups. All seed was obtained from the USDA Soybean Germplasm collection at Urbana, IL. Three to four seeds per cultivar were sown in either 25- or 30-cm diam pots (20–25 L) filled with vermiculite. For each experiment 10 pots (five of each size) of a given cultivar were assigned to a CO₂ treatment. Twenty-five-centimeter pots were used for the initial harvest. Plants from a given cultivar were grouped together but groups spaced so as to minimize mutual shading. Plants within a given cultivar were spaced about 30 cm apart. Both individual plants and groups were rotated weekly inside a glasshouse until flowering to minimize border effects. All pots were watered daily to the drip point with a complete nutrient solution containing 13.5 mM nitrogen (ammonium and nitrate, see Robinson, 1984). All pots were thinned to one plant per pot at 10 d after sowing (DAS) in all runs.

Vegetative and Reproductive Measurements
For all cultivars, the initial sampling to determine growth was at 10 DAS. Subsequent harvests occurred, respectively, with the appearance of initial bloom (31–44 DAS, depending on maturity group) and again at seed maturity (92–121 DAS). Average number of days until flowering was 39, 34, and 35 DAS for Runs 1 to 3. Overall, flowering occurred earlier in Runs 2 and 3 because of shorter days. For a given experiment, no change in days to initial flowering or maturity occurred as a result of CO₂ treatment for a given cultivar. At flowering, five plants for a given cultivar and CO₂ treatment were cut at ground level and separated into leaf laminae, stems (including petioles) and roots. Leaf area was determined photometrically with a leaf area meter (Li 3000, LI-COR, Lincoln, NE). Dry weights were obtained separately for leaves, stems, and roots. The plant parts were dried at 65°C for a minimum of 72 h or until dry weight was constant, and weighed.

Pods were hand harvested at maturity and threshed with a small custom made thresher. Maturity was determined when 95% of the pods on an individual plant had turned brown and vegetative growth had ceased. At maturity, stem weight, pod number, node number, pod weight, axillary branching, and the average weight of 50 seed were obtained for all experimental runs, cultivars and treatments. Because of leaf senescence in soybean, harvest index was calculated as the ratio of seed to stem plus pod biomass at maturity. This is typically done for commercial soybean and is referred to as the apparent harvest index or AHI (Schapaugh and Wilcox, 1980). For Run 3, pods obtained from axillary branches were harvested separately from main stem pods for all treatments.

Statistical Analyses
Because only two glasshouses were available, a randomized complete block design was used with runs over time as replications (blocks). For each run, CO₂ treatment was randomly assigned to a given glasshouse and cultivars randomly assigned within that glasshouse. The entire experiment was replicated three times from 1998 through 1999. The mean value for five plants per CO₂ treatment from a given run was used as a single replicate. The data were analyzed in two ways. For vegetative and reproductive characteristics, the effect of CO₂ partial pressure was tested for individual cultivars by a one-way ANOVA. To examine sensitivity in the responsiveness of seed yield to elevated CO₂ between cultivars, the ratio of the mean value at elevated (E) to that at ambient CO₂ (A) for a given experimental run was calculated with variation among cultivars in this ratio tested using a one way ANOVA. Correlations between the relative seed yield increase with elevated CO₂ and other growth parameters were calculated by simple regression with cultivar means as variables. Unless otherwise indicated, differences were treated as significant at the P < 0.05 level.

	RESULTS

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No significant differences were observed in the absolute rates of leaf assimilation between the 2nd and 5th terminal leaflet at a given CO₂ treatment; consequently, both positions were combined for analysis (Table 2). For all soybean cultivars, exposure to elevated CO₂ resulted in a significant stimulation of leaf photosynthesis, with an average increase of 75% (Table 2). No differences in photosynthetic stimulation were observed between the short- and long-term response to elevated CO₂ for a given cultivar, suggesting that photosynthetic acclimation did not occur during the measurement period (Table 2). The measurement period (i.e., up to the fifth trifoliolate) corresponded approximately with the appearance of flowers or early pod fill for all cultivars.

View larger version (15K): [in this window] [in a new window]   Fig. 1. Variation in the ratio of seed yield (g plant-1) at elevated (71 Pa, E) to that at ambient (40 Pa, A) carbon dioxide for eight ancestral and one modern soybean cultivar over three runs of the experiment. To test for differences among cultivars in the responsiveness of seed yield to elevated CO2, the ratio of the mean value at elevated (E) to that at ambient CO2 (A) for a given experimental run was calculated. Variation among cultivars in this ratio was tested using one way ANOVA, with three replicates. The mean seed yield response of Mandarin was significantly (P = 0.05) higher than the other cultivars. Cultivars are listed alphabetically

View larger version (23K): [in this window] [in a new window]   Fig. 2. The percentage stimulation of seed yield for nine soybean cultivars grown at elevated CO2 (71 Pa, E) relative to the ambient CO2 treatment (40 Pa, A) over three runs of the experiment. Cultivars are listed according to the relative response of seed yield to elevated CO2. * indicates a significant difference (P < 0.05) relative to ambient CO2 for individual cultivars. Bars are ±se

View larger version (17K): [in this window] [in a new window]   Fig. 3. Change in the ratio of branch and main stem seed weight per plant at elevated (71 Pa, E) to that at ambient (40 Pa, A) carbon dioxide in relation to the increase in total seed yield for the entire plant. r2 was significant for the change in branch seed weight per plant. AR = Arksoy; CN = CNS; DU = Dunfield; HA = Harrow; MA = Manchu; MN = Mandarin; MU = Mukden; S = S-100; WI = Williams. Data are from Run 3. Each point is the average of five plants

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

If photosynthetic response is not correlated with yield sensitivity among cultivars, then photosynthetic partitioning may be a more relevant parameter. In the current study, the vegetative response at flowering was not a good predictor of seed yield sensitivity to elevated CO₂. In addition, partitioning among vegetative structures (e.g., specific leaf weight, root to shoot ratio, leaf to stem ratio) or changes in determinacy or maturity group (i.e., time to flowering), were also not correlated with the relative sensitivity of seed yield to elevated CO₂ (data not shown).

As might be expected, measurements made at maturity were better predictors of seed yield sensitivity. It is not surprising that increased pod weight was associated with increased seed yield at elevated CO₂. What is somewhat surprising, however, is that the increase in seed yield was not evenly distributed between main stem and axillary seed production. Seed yield sensitivity to CO₂ was related to the ability to produce additional seed on axillary branches. Increased axillary branching in response to elevated CO₂ also showed a good correlation with seed yield sensitivity (r = 0.57), but the correlation was not significant (P = 0.10). The situation observed here is somewhat analogous to that observed in field-grown rice in that branching (or tillering) is correlated with the ability of seed yield to respond strongly to elevated CO₂ (Moya et al., 1998).

If a cultivar such as Mandarin shows promise in the glasshouse, will it perform equally well in the field? Clearly, the response of single plants may differ from that of large scale canopies. Changes in planting density may be especially crucial if, in fact, axillary branching is required to optimize seed yield response. Yet, because the cost of screening large numbers of cultivars to CO₂ in the field remains prohibitive, glasshouse trials may serve as an initial step in determining variation and seed yield sensitivity to CO₂. Recent work with a modern soybean cultivar, Spencer, suggests that in some cases, glasshouse screening for yield sensitivity to rising CO₂ can transfer to field conditions (Ziska and Bunce, 2000). Obviously, confirmation of such an approach will require additional field studies of promising cultivars observed in the glasshouse.

This does not mean that all glasshouse observations should be dismissed. For example, in the current study, elevated CO₂ significantly reduced AHI in some cultivars. This indicates that, in general, vegetative growth is more sensitive to increases in CO₂ than reproductive development as has been observed previously for soybean in the field (e.g., Baker et al., 1989). The current study also suggests that the reduction in AHI may occur in part because elevated CO₂ can also reduce key reproductive parameters. For example, the observed decline in AHI was associated with a reduction in the number of pods per node at elevated CO₂ for three of the four cultivars showing a significant reduction in AHI (Manchu, Mukden and S-100). The reduction in pods per node may have limited the relative increase in seed yield for these cultivars. Overall, no cultivar examined demonstrated an increase in either pods per node or seeds per pod (although there is a clear difference in seeds per pod between the modern cultivar Williams and ancestral lines). Presumably, maintaining or increasing these parameters (in addition to increasing pod number, average seed weight, etc.), could result in a greater stimulation of both relative seed yield and potentially, AHI in a field trial.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Clearly, any organized effort to utilize genotypic variation to increase seed yield in soybean or other important agronomic plants as atmospheric CO₂ increases, is still in its initial stages. We recognize that experiments examining genotypic variation in a glasshouse may not always mimic larger scale responses in the field. However, because of the high costs associated with maintaining an elevated CO₂ environment, it is difficult to determine the full range of genotypic variability for large numbers of cultivars using a traditional field approach. On the basis of these initial results, there appears to be significant variation in the sensitivity of seed yield to elevated CO₂ among ancestral soybean cultivars. While the stimulation of photosynthesis remains the driving force for increases in growth and yield in response to elevated CO₂, variation in either the absolute rates or relative degree of stimulation was not associated with the observed sensitivity of seed yield reported here for soybean. Vegetative response or differences in vegetative partitioning among organs at flowering was also poorly correlated with seed yield variation. Interestingly, one factor which may predict seed yield sensitivity is seed production on axillary branches. Overall, data from the current study demonstrate that there is significant variation in seed yield sensitivity among soybean cultivars, and that such sensitivity may be associated with plasticity related to the production of axillary branches and additional seed production at a future, elevated level of carbon dioxide.

	ACKNOWLEDGMENTS

 
We thank Dr. Jeff Baker for his review and suggestions to the manuscript.

Received for publication May 11, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 

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This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (6) Citing Articles via Google Scholar Google Scholar Articles by Ziska, L. H. Articles by Caulfield, F. A. Search for Related Content PubMed Articles by Ziska, L. H. Articles by Caulfield, F. A. Agricola Articles by Ziska, L. H. Articles by Caulfield, F. A. Related Collections Soybean Plant and Environment Interactions Seed Production