Wittwer (1995) reports that the common soybean (Glycine max L.) "provides about two thirds of the world's protein concentrate for livestock feeding, and is a valuable ingredient in formulated feeds for poultry and fish." Consequently, it is important to determine how soybeans will likely respond to rising atmospheric CO2 concentrations with and without concomitant increases in air temperature and under both well-watered and water-stressed conditions. In this summary we provide that information in a brief review of the results of several studies that have investigated these aspects of the subject.
Rogers et al. (2004) grew soybeans from emergence to grain maturity in ambient and CO2-enriched air (372 and 552 ppm CO2, respectively) at the SoyFACE facility of the University of Illinois at Urbana-Champaign, Illinois, USA, while CO2 uptake and transpiration measurements were made from pre-dawn to post-sunset on seven days representative of different developmental stages of the crop. Across the growing season, they found that the mean daily integral of leaf net photosynthesis rose by 24.6% in the elevated CO2 treatment, while mid-day stomatal conductance dropped by 21.9%, in response to the 48% increase in atmospheric CO2 employed in their study. With respect to photosynthesis, they additionally report "there was no evidence of any loss of stimulation toward the end of the growing season," noting that the largest stimulation actually occurred during late seed filling. Nevertheless, they say that the photosynthetic stimulation they observed was only "about half the 44.5% theoretical maximum increase calculated from Rubisco kinetics." Thus, there is an opportunity for soybeans to perhaps become even more responsive to atmospheric CO2 enrichment than they are currently, which potential could well be realized via future developments in the field of genetic engineering.
Bunce (2005) grew soybeans in the field in open-top chambers maintained at atmospheric CO2 concentrations of ambient and ambient +350 ppm at the Beltsville Agricultural Research Center in Maryland, USA, where net CO2 exchange rate measurements were performed on a total of 16 days between 18 July and 11 September of 2000 and 2003, during flowering to early pod-filling. Over the course of this study, daytime net photosynthesis per unit leaf area was 48% greater in the plants growing in the CO2-enriched air, while nighttime respiration per unit leaf area was not affected by elevated CO2. However, because the elevated CO2 increased leaf dry mass per unit area by an average of 23%, respiration per unit mass was significantly lower for the leaves of the soybeans growing in the CO2-enriched air, producing a sure recipe for accelerated growth and higher soybean seed yields.
Working in Australia, Japan and the United States, Ziska et al. (2001b) observed a recurrent diurnal pattern of atmospheric CO2 concentration, whereby maximum values of 440-540 ppm occurred during a three-hour pre-dawn period that was followed by a decrease to values of 350-400 ppm by mid-morning, after which there was a slow but steady increase in the late afternoon and early evening that brought the air's CO2 concentration back to its pre-dawn maximum value. In an attempt to see if the pre-dawn CO2 spikes they observed impacted plant growth, they grew soybeans for one month in controlled-environment chambers under three different sets of conditions: a constant 24-hour exposure to 370 ppm CO2, a constant 370 ppm CO2 exposure during the day followed by a constant 500 ppm CO2 exposure at night, and a CO2 exposure of 500 ppm from 2200 to 0900 followed by a decrease to 370 ppm by 1000, which was maintained until 2200, somewhat mimicking the CO2 cycle they observed in nature. This program revealed that the 24-hour exposure to 370 ppm CO2 and the 370-ppm-day/500-ppm-night treatments produced essentially the same results in terms of biomass production after 29 days. However, the CO2 treatment that mimicked the observed atmospheric CO2 pattern resulted in a plant biomass increase of 20%.
In a study that evaluated a whole range of atmospheric CO2 concentrations, from far below ambient levels to high above them, Allen et al. (1998) grew soybeans for an entire season in growth chambers maintained at atmospheric CO2 concentrations of 160, 220, 280, 330, 660 and 990 ppm. In doing so, they observed a consistent increase in total nonstructural carbohydrates in all vegetative components including roots, stems, petioles and especially the leaves, as CO2 concentrations rose. There was, however, no overall significant effect of treatment CO2 concentration on nonstructural carbohydrate accumulation in soybean reproductive components, including podwalls and seeds, which observations indicate that the higher yields reported in the literature for soybeans exposed to elevated CO2 most likely result from increases in the number of pods produced per plant, and not from the production of larger individual pods or seeds.
The increasing amounts of total nonstructural carbohydrates that were produced with each additional increment of CO2 provided the raw materials to support greater biomass production at each CO2 level. Although final biomass and yield data were not reported in this paper, the authors did present biomass data obtained at 66 days into the experiment. Relative to aboveground biomass measured at 330 ppm CO2, the plants that were grown in sub-ambient CO2 concentrations of 280, 220 and 160 ppm exhibited 12, 33 and 60% less biomass, respectively, while plants grown in atmospheric CO2 concentrations of 660 and 990 ppm displayed 46 and 66% more biomass. Hence, it is likely that soybeans began experiencing increases in total nonstructural carbohydrates and yield as the air's CO2 concentration began to rise with the onset of the Industrial Revolution; and because nonstructural carbohydrate production rises incrementally with incremental increases in the CO2 content of the air, soybeans will likely continue to produce ever more total nonstructural carbohydrates that will sustain ever greater yields as the CO2 content of the air continues to rise in the future.
In a study of two contrasting soybean cultivars, Ziska and Bunce (2000) grew Ripley, which is semi-dwarf and determinate in growth, and Spencer, which is standard-size and indeterminate in growth, for two growing seasons in open-top chambers maintained at atmospheric CO2 concentrations of ambient and ambient plus 300 ppm. Averaged over both years, the elevated CO2 treatment increased photosynthetic rates in the Ripley and Spencer varieties by 76 and 60%, respectively. However, Spencer showed a greater CO2-induced increase in vegetative biomass than Ripley (132 vs. 65%). Likewise, elevated CO2 enhanced seed yield in Spencer by 60% but by only 35% in Ripley, suggesting that cultivar selection for favorable yield responses to atmospheric CO2 enrichment could have a big impact on future farm productivity.
In another study of contrasting types of soybeans, Nakamura et al. (1999) grew nodulated and non-nodulated plants in pots within controlled-environmental cabinets maintained at atmospheric CO2 concentrations of 360 and 700 ppm in combination with low and high soil nitrogen supply for three weeks. They found that at low nitrogen, elevated CO2 increased total plant dry mass by approximately 40 and 80% in nodulated soybeans grown at low and high nitrogen supply, respectively, while non-nodulated plants exhibited no CO2-induced growth response at low nitrogen but an approximate 60% growth enhancement at high nitrogen supply. Hence, it would appear that as the air's CO2 content continues to rise, non-nodulated soybeans will only display increases in biomass if they are grown in nitrogen-rich soils. Nodulated soybeans, however, should display increased growth in both nitrogen-rich and nitrogen-poor soils, with their responses being about twice as large in high as in low soil nitrogen conditions.
In yet another study of soybeans with different genetic characteristics, Ziska et al. (2001a) grew one modern and eight ancestral soybean genotypes in glasshouses maintained at atmospheric CO2 concentrations of 400 and 710 ppm, finding that the elevated CO2 increased photosynthetic rates in all cultivars by an average of 75%. This photosynthetic enhancement led to CO2-induced increases in seed yield that averaged 40%, except for one of the ancestral varieties that exhibited an 80% increase in seed yield. Consequently, since the air's CO2 content is anticipated to continue to rise in the years and decades ahead, plant breeders would be wise to consider utilizing the highly-CO2-responsive ancestral cultivar identified in this study in future breeding programs.
To get a glimpse of what might happen if future temperatures also continue to rise, Ziska (1998) grew soybeans for 21 days in controlled environments having atmospheric CO2 concentrations of approximately 360 (ambient) or 720 ppm and soil temperatures of 25 (ambient) or 30°C. He found that elevated CO2 significantly increased whole plant net photosynthesis at both temperatures, with the greatest effect occurring at 30°C. As time progressed, however, this photosynthetic stimulation dropped from 50% at 13 days into the experiment to 30% at its conclusion eight days later; yet in spite of this partial acclimation, which was far from complete, atmospheric CO2 enrichment significantly enhanced total plant dry weight at final harvest by 36 and 42% at 25 and 30°C, respectively.
Studying the complicating effects of water stress were Serraj et al. (1999), who grew soybeans from seed in pots within a glasshouse until they were four weeks old, after which half of the plants were subjected to an atmospheric CO2 concentration of 360 ppm, while the other half were exposed to an elevated concentration of 700 ppm. In addition, half of the plants at each CO2 concentration were well-watered and half of them were allowed to experience water stress for a period of 18 days. This protocol revealed that short-term (18-day) exposure of soybeans to elevated CO2 significantly decreased daily and cumulative transpirational water losses compared to plants grown at 360 ppm CO2, regardless of water treatment. In fact, elevated CO2 reduced total water loss by 25 and 10% in well-watered and water-stressed plants, respectively. Also, drought stress significantly reduced rates of net photosynthesis among plants of both CO2 treatments. However, plants grown in elevated CO2 consistently exhibited higher photosynthetic rates than plants grown at ambient CO2, regardless of soil water status.
At final harvest, the elevated CO2 treatment had little effect on the total dry weight of plants grown at optimal soil moisture, but it increased the total dry weight of water-stressed plants by about 33%. Also, while root dry weight declined for plants grown under conditions of water stress and ambient CO2 concentration, no such decline was exhibited by plants subjected to atmospheric CO2 enrichment and water stress. As the atmospheric CO2 concentration continues to rise, therefore, soybeans will likely display concurrent increases in photosynthesis and decreases in water loss. Thus, in the future, the water-use efficiency of soybeans will likely be significantly enhanced, allowing plants to better tolerate less frequent rains.
Studying both water and high-temperature stress were Ferris et al. (1999), who grew soybeans in glasshouses maintained at atmospheric CO2 concentrations of 360 and 700 ppm for 52 days, before having various environmental stresses imposed on them for eight days during early seed filling. For the eight-day stress period, some plants were subjected to air temperatures that were 15°C higher than those to which the control plants were exposed, while some were subjected to a water stress treatment in which their soil moisture contents were maintained at 40% of that experienced by the control plants. Averaged across all stress treatments and harvests, this protocol revealed that the high CO2 treatment increased total plant biomass by 41%. Both high-temperature and water-deficit treatments, singly or in combination, reduced overall biomass by approximately the same degree, regardless of CO2 treatment. Thus, even when the greatest biomass reductions of 17% occurred in the CO2-enriched and ambiently grown plants, in response to the combined stresses of high temperature and low soil moisture, plants grown in elevated CO2 still exhibited an average biomass that was 24% greater than that displayed by plants grown in ambient CO2.
Averaged across all stress treatments and harvests, elevated CO2 increased seed yield by 32%. In addition, it tended to ameliorate the negative effects of environmental stresses. CO2-enriched plants that were water stressed, for example, had an average seed yield that was 34% greater than that displayed by water-stressed controls grown at ambient CO2, while CO2-enriched plants exposed to high temperatures produced 38% more seed than their respectively stressed counterparts. In fact, the greatest relative impact of elevated CO2 on seed yield occurred in response to the combined stresses of high temperature and low soil moisture, with CO2-enriched plants exhibiting a seed yield that was 50% larger than that of similarly stressed plants grown in ambient CO2.
In a predictive application of this type of knowledge, but based on a different means of obtaining it, Alexandrov and Hoogenboom (2000) studied how temperature, precipitation and solar radiation influenced soybean yields over a 30-year period in the southeastern United States, after which they used the results they obtained to predict future crop yields based on climate output from various global circulation models of the atmosphere. At ambient CO2 concentrations, the model-derived scenarios pointed to a decrease in soybean yields by the year 2020, due in part to predicted changes in temperature and precipitation. However, when the yield-enhancing effects of a doubling of the air's CO2 concentration were included in the simulations, a completely different projection was obtained: a yield increase.
Shifting to the subject of soybean seed quality, Caldwell et al. (2005) write that "the beneficial effects of isoflavone-rich foods have been the subject of numerous studies (Birt et al., 2001; Messina, 1999)," and that "foods derived from soybeans are generally considered to provide both specific and general health benefits," presumably via these substances. Hence, it is only natural they would wonder how the isoflavone content of soybean seeds may be affected by the ongoing rise in the air's CO2 content, and that they would conduct a set of experiments to find the answer.
The curious scientists grew well-watered and fertilized soybean plants from seed to maturity in pots within two controlled-environment chambers, one maintained at an atmospheric CO2 concentration of 400 ppm and one at 700 ppm. The chambers were initially kept at a constant air temperature of 25°C. At the onset of seed fill, however, air temperature was reduced to 18°C until seed development was complete, in order to simulate average outdoor temperatures at this stage of plant development. In a second experiment, this protocol was repeated, except that the temperature during seed fill was maintained at 23°C, with and without drought (a third treatment), while in a third experiment, seed-fill temperature was maintained at 28°C, with or without drought.
In the first experiment, where air temperature during seed fill was 18°C, the elevated CO2 treatment increased the total isoflavone content of the soybean seeds by 8%. In the second experiment, where air temperature during seed fill was 23°C, the extra CO2 increased total seed isoflavone content by 104%, while in the third experiment, where air temperature during seed fill was 28°C, the CO2-induced isoflavone increase was 101%. Finally, when drought-stress was added as a third environmental variable, the extra CO2 boosted total seed isoflavone content by 186% when seed-fill air temperature was 23°C, while at a seed-fill temperature of 28°C, it increased isoflavone content by 38%.
Under all environmental circumstances studied, enriching the air with an extra 300 ppm of CO2 increased the total isoflavone content of soybean seeds. In addition, the percent increases measured under the stress situations investigated were always greater than the percent increase measured under optimal growing conditions. Consequently, the direct effects of atmospheric CO2 enrichment on the health-promoting properties of soybean seeds would appear to be universally beneficial and a boon to the entire human race, especially in light of the fact that Bernacchi et al. (2005) characterize the soybean as "the world's most important seed legume."
Also writing on the subject of soybean seed quality, Thomas et al. (2003) say "the unique chemical composition of soybean has made it one of the most valuable agronomic crops worldwide," noting that "oil and protein comprise ~20 and 40%, respectively, of the dry weight of soybean seed." Consequently, they explored the effects of elevated CO2 plus temperature on soybeans that were grown to maturity in sunlit controlled-environment chambers with sinusoidally-varying day/night max/min temperatures of 28/18, 32/22, 36/26, 40/30 and 44/34°C and atmospheric CO2 concentrations of 350 and 700 ppm. This work revealed that the effect of temperature on seed composition and gene expression was "pronounced," but that "there was no effect of CO2." In this regard, however, they note that "Heagle et al. (1998) observed a positive significant effect of CO2 enrichment on soybean seed oil and oleic acid concentration," the latter of which parameters their own study found to rise with increasing temperature all the way from 28/18 to 44/34°C. In addition, they determined that "32/22°C is optimum for producing the highest oil concentration in soybean seed," that "the degree of fatty acid saturation in soybean oil was significantly increased by increasing temperature," and that crude protein concentration increased with temperature to 40/30°C.
In commenting on these observations, Thomas et al. note that "the intrinsic value of soybean seed is in its supply of essential fatty acids and amino acids in the oil and protein, respectively." Hence, we conclude that the temperature-driven changes they identified in these parameters, as well as the CO2 effect observed by Heagle et al., bode well for the future production of this important crop and its value to society in a CO2-enriched and warming world. Thomas et al. note, however, that "temperatures during the soybean-growing season in the southern USA are at, or slightly higher than, 32/22°C," and that warming could negatively impact the soybean oil industry in this region. For the world as a whole, however, warming would be a positive development for soybean production; while in the southern United States, shifts in planting zones could readily accommodate changing weather patterns associated with this phenomenon.
In conclusion, as the air's CO2 content continues to rise, soybeans will likely respond by displaying significant increases in growth and yield, with possible improvements in seed quality; and these beneficial effects will likely persist, even if temperatures rise or soil moisture levels decline, regardless of their cause.
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