From Climate Change Reconsidered, a work of the Nongovernmental International Panel on Climate Change
Plants grown in elevated CO2 environments often exhibit some degree of photosynthetic acclimation or down regulation, which is typically characterized by long-term rates of photosynthesis that are somewhat lower than what would be expected on the basis of measurements made during short-term exposure to CO2-enriched air. These downward adjustments result from modest long-term decreases in the activities and/or amounts of the primary plant carboxylating enzyme rubisco. Acclimation is said to be present when the photosynthetic rates of long-term CO2-enriched plants are found to be lower than those of long-term non-CO2-enriched plants when the normally CO2-enriched plants are measured during brief exposures to ambient CO2 concentrations. In this section, we review research that has been published on acclimation in agricultural, desert, grassland and woody species.
Several studies have examined the effects of elevated CO2 on acclimation in agricultural crops. Ziska (1998), for example, reported that soybeans grown at an atmospheric CO2 concentration of 720 ppm initially exhibited photosynthetic rates that were 50 percent greater than those observed in control plants grown at 360 ppm. However, after the onset of photosynthetic acclimation, CO2-enriched plants displayed subsequent photosynthetic rates that were only 30 percent greater than their ambiently grown counterparts. In another study, Theobald et al. (1998) grew spring wheat at twice-ambient atmospheric CO2 concentrations and determined that elevated CO2 reduced the amount of rubisco required to sustain enhanced rates of photosynthesis, which led to a significant increase in plant photosynthetic nitrogen-use efficiency. CO2-induced increases in photosynthetic nitrogen-use efficiency have also been reported in spring wheat by Osborne et al. (1998).
In an interesting study incorporating both hydroponically and pot-grown wheat plants, Farage et al. (1998) demonstrated that low nitrogen fertilization does not lead to photosynthetic acclimation in elevated CO2 environments, as long as the nitrogen supply keeps pace with the relative growth rate of the plants. Indeed, when spring wheat was grown at an atmospheric CO2 concentration of 550 ppm in a free-air CO2 enrichment (FACE) experiment with optimal soil nutrition and unlimited rooting volume, Garcia et al. (1998) could find no evidence of photosynthetic acclimation.
CO2-induced photosynthetic acclimation often results from insufficient plant sink strength, which can lead to carbohydrate accumulation in source leaves and the triggering of photosynthetic end product feedback inhibition, which reduces net photosynthetic rates. Indeed, Gesch et al. (1998) reported that rice plants—which have relatively limited potential for developing additional carbon sinks—grown at an atmospheric CO2 concentration of 700 ppm exhibited increased leaf carbohydrate contents, which likely reduced rbcS mRNA levels and rubisco protein content. Similarly, Sims et al. (1998) reported that photosynthetic acclimation was induced in CO2-enriched soybean plants from the significant accumulation of nonstructural carbohydrates in their leaves. However, in growing several different Brassica species at 1,000 ppm CO2, Reekie et al. (1998) demonstrated that CO2-induced acclimation was avoided in species having well-developed carbon sinks (broccoli and cauliflower) and only appeared in those lacking significant sink strength (rape and mustard). Thus, acclimation does not appear to be a direct consequence of atmospheric CO2 enrichment but rather an indirect effect of low sink strength, which results in leaf carbohydrate accumulation that can trigger acclimation.
In some cases, plants can effectively increase their sink strength, and thus reduce the magnitude of CO2-induced acclimation, by forming symbiotic relationships with certain species of soil fungi. Under such conditions, photosynthetic down regulation is not triggered as rapidly, or as frequently, by end product feedback inhibition, as excess carbohydrates are mobilized out of source leaves and sent belowground to symbiotic fungi. Indeed, Louche-Tessandier et al. (1999) report that photosynthetic acclimation in CO2-enriched potatoes was less apparent when plants were simultaneously colonized by a mycorrhizal fungus. Thus, CO2-induced acclimation appears to be closely related to the source:sink balance that exists within plants, being triggered when sink strength falls below, and source strength rises above, critical thresholds in a species-dependent manner.
Acclimation is generally regarded as a process that reduces the amount of rubisco and/or other photosynthetic proteins, which effectively increases the amount of nitrogen available for enhancing sink development or stimulating other nutrient-limited processes. In the study of Watling et al. (2000), for example, the authors reported a 50 percent CO2-induced reduction in the concentration of PEP-carboxylase, the primary carboxylating enzyme in C4 plants, within sorghum leaves. Similarly, Maroco et al. (1999) documented CO2-induced decreases in both PEP-carboxylase and rubisco in leaves of the C4 crop maize.
In some cases, however, acclimation to elevated CO2 is manifested by an “up-regulation” of certain enzymes. When Gesch et al. (2002) took rice plants from ambient air and placed them in air containing 700 ppm, for example, they noticed a significant increase in the activity of sucrose-phosphate synthase (SPS), which is a key enzyme involved in the production of sucrose. Similarly, Hussain et al. (1999) reported that rice plants grown at an atmospheric CO2 concentration of 660 ppm displayed 20 percent more SPS activity during the growing season than did ambiently grown rice plants. Such increases in the activity of this enzyme could allow CO2-enriched plants to avoid the onset of photosynthetic acclimation by synthesizing and subsequently exporting sucrose from source leaves into sink tissues before they accumulate and trigger end product feedback inhibition.
In an interesting experiment, Gesch et al. (2000) took ambiently growing rice plants and placed them in an atmospheric CO2 concentration of 175 ppm, which reduced photosynthetic rates by 45 percent. However, after five days exposure to this sub-ambient CO2 concentration, the plants manifested an up-regulation of rubisco, which stimulated photosynthetic rates by 35 percent. Thus, plant acclimation responses can involve both an increase or decrease in specific enzymes, depending on the atmospheric CO2 concentration.
In summary, many peer-reviewed studies suggest that as the CO2 content of the air slowly but steadily rises, agricultural species may not necessarily exhibit photosynthetic acclimation, even under conditions of low soil nitrogen. If a plant can maintain a balance between its sources and sinks for carbohydrates at the whole-plant level, acclimation should not be necessary. Because earth’s atmospheric CO2 content is rising by an average of only 1.5 ppm per year, most plants should be able to either (1) adjust their relative growth rates by the small amount that would be needed to prevent low nitrogen-induced acclimation from ever occurring, or (2) expand their root systems by the small amount that would be needed to supply the extra nitrogen required to take full advantage of the CO2-induced increase in leaf carbohydrate production. In the event a plant cannot initially balance its sources and sinks for carbohydrates at the whole-plant level, CO2-induced acclimation represents a beneficial secondary mechanism for achieving that balance through redistributing limiting resources away from the plant’s photosynthetic machinery to strengthen sink development or enhance other nutrient-limiting processes.
Chaparral and Desert Species
Roberts et al. (1998) conducted a FACE experiment in southern California, USA, exposing Adenostoma fassciculatum shrubs to atmospheric CO2 concentrations of 360 and 550 ppm while they studied the nature of gas-exchange in this chaparral species. After six months of CO2 fumigation, photosynthetic acclimation occurred. However, because of reductions in stomatal conductance and transpirational water loss, the CO2-enriched shrubs exhibited leaf water potentials that were less negative (and, hence, less stressful) than those of control plants. This CO2-induced water conservation phenomenon should enable this woody perennial to better withstand the periods of drought that commonly occur in this southern California region, while the photosynthetic down regulation it exhibits should allow it to more equitably distribute the limiting resources it possesses among different essential plant physiological processes.
Huxman and Smith (2001) measured seasonal gas exchange during an unusually wet El Niño year in an annual grass (Bromus madritensis ssp. rubens) and a perennial forb (Eriogonum inflatum) growing within FACE plots established in the Mojave Desert, USA, which they maintained at atmospheric CO2 concentrations of 350 and 550 ppm. The elevated CO2 consistently increased net photosynthetic rates in the annual grass without inducing photosynthetic acclimation. In fact, even as seasonal photosynthetic rates declined post-flowering, the reduction was much less in the CO2-enriched plants. However, elevated CO2 had no consistent effect on stomatal conductance in this species. By contrast, Eriogonum plants growing at 550 ppm CO2 exhibited significant photosynthetic acclimation, especially late in the season, which led to similar rates of net photosynthesis in these plants in both CO2 treatments. But in this species, elevated CO2 reduced stomatal conductance over most of the growing season. Although the two desert plants exhibited different stomatal and photosynthetic responses to elevated CO2, both experienced significant CO2-induced increases in water use efficiency and biomass production, thus highlighting the existence of different, but equally effective, species-specific mechanisms for responding positively to atmospheric CO2 enrichment in a desert environment.
In another study conducted at the Mojave Desert FACE site, Hamerlynck et al. (2002) determined that plants of thedeciduous shrub Lycium andersonii grown in elevated CO2 displayed photosynthetic acclimation, as maximum rubisco activity in the plants growing in the CO2-enriched air was 19 percent lower than in the plants growing in ambient air. Also, the elevated CO2 did not significantly impact rates of photosynthesis. Leaf stomatal conductance, on the other hand, was consistently about 27 percent lower in the plants grown in the CO2-enriched air; and during the last month of the spring growing season, the plants in the elevated CO2 plots displayed leaf water potentials that were less negative than those exhibited by the control plants growing in ambient air. Hence, as the CO2 content of the air increases, Lycium andersonii will likely respond by exhibiting significantly enhanced water use efficiency, which should greatly increase its ability to cope with the highly variable precipitation and temperature regimes of the Mojave Desert. The acclimation observed within the shrub’s photosynthetic apparatus should allow it to reallocate more resources to producing and sustaining greater amounts of biomass. Thus, it is likely that future increases in the air’s CO2 content will favor a “greening” of the American Mojave Desert.
In summary, the few studies of the acclimation phenomenon that have been conducted on chaparral and desert plants indicate that although it can sometimes be complete, other physiological changes, such as the reductions in stomatal conductance that typically produce large increases in water use efficiency, often more than compensate for the sometimes small to negligible increases in photosynthesis.
In nearly every reported case of photosynthetic acclimation in CO2-enriched plants, rates of photosynthesis displayed by grassland species grown and measured at elevated CO2 concentrations are typically greater than those exhibited by control plants grown and measured at ambient CO2 concentrations (Davey et al., 1999; Bryant et al., 1998).
As mentioned in prior sections, CO2-induced photosynthetic acclimation often results from insufficient plant sink strength, which can lead to carbohydrate accumulation in source leaves and the triggering of photosynthetic end-product feedback inhibition, which reduces rubisco activity and rates of net photosynthesis (Roumet et al., 2000). As one example of this phenomenon, Rogers et al. (1998) reported that perennial ryegrass grown at an atmospheric CO2 concentration of 600 ppm and low soil nitrogen exhibited leaf carbohydrate contents and rubisco activities that were 100 percent greater and 25 percent less, respectively, than those observed in control plants grown at 360 ppm CO2, prior to a cutting event. Following the cutting, which effectively reduced the source:sink ratio of the plants, leaf carbohydrate contents in CO2-enriched plants decreased and rubisco activities increased, completely ameliorating the photosynthetic acclimation in this species. However, at high soil nitrogen, photosynthetic acclimation to elevated CO2 did not occur. Thus, photosynthetic acclimation appears to result from the inability of plants to develop adequate sinks at low soil nitrogen, and is not necessarily induced directly by atmospheric CO2 enrichment.
In some cases, plants can effectively increase their sink strength and thus reduce the magnitude of CO2-induced acclimation by forming symbiotic relationships with certain species of soil fungi. Under such conditions, photosynthetic down regulation is not triggered as rapidly, or as frequently, by end-product feedback inhibition, as excess carbohydrates are mobilized out of source leaves and sent belowground to symbiotic fungi. Staddon et al. (1999) reported that photosynthetic acclimation was not induced in CO2-enriched Plantago lanceolata plants that were inoculated with a mycorrhizal fungus, while it was induced in control plants that were not inoculated with the fungus. Thus, CO2-induced acclimation appears to be closely related to the source:sink balance that exists within plants, and is triggered when sink strength falls below, and source strength rises above, certain critical thresholds in a species-dependent manner.
As the CO2 content of the air slowly but steadily rises, these peer-reviewed studies suggest that grassland species may not exhibit photosynthetic acclimation if they can maintain a balance between their sources and sinks for carbohydrates at the whole-plant level. But in the event this balancing act is not initially possible, acclimation represents a beneficial secondary mechanism for achieving that balance by redistributing limiting resources away from the plant’s photosynthetic machinery to strengthen its sink development and/or nutrient-gathering activities.
Trees grown for long periods of time in elevated CO2 environments often, but not always (Marek et al., 2001; Stylinski et al., 2000; Bartak et al., 1999; Schortemeyer et al., 1999), exhibit some degree of photosynthetic acclimation or down regulation, which is typically characterized by modestly reduced rates of photosynthesis (compared to what might be expected on the basis of short-term exposure to CO2-enriched air) that result from a long-term decrease in the activity and/or amount of the primary plant carboxylating enzyme rubisco (Kubiske et al., 2002; Egli et al., 1998). This acclimation response in plants accustomed to growing in CO2-enriched air is characterized by short-term reductions in their rates of net photosynthesis when measured during short-term exposure to ambient air relative to net photosynthesis rates of comparable plants that have always been grown in ambient air.
Jach and Ceulemans (2000) grew one-year-old Scots pine seedlings for two additional years at twice-ambient atmospheric CO2 concentrations and reported that the elevated CO2 increased the trees’ mean rate of net photosynthesis by 64 percent. However, when measured during a brief return to ambient CO2 concentrations, the normally CO2-enriched seedlings exhibited an approximate 21 percent reduction in average net photosynthesis rate relative to that of seedlings that had always been exposed to ambient air. Similarly, Spunda et al. (1998) noted that a 350-ppm increase in the air’s CO2 concentration boosted rates of net photosynthesis in fifteen-year-old Norway spruce trees by 78 percent; but when net photosynthesis in the normally CO2-enriched trees was measured at a temporary atmospheric CO2 concentration of 350 ppm, an 18 percent reduction was observed relative to what was observed in comparable trees that had always been grown in ambient air. After reviewing the results of 15 different atmospheric CO2 enrichment studies of European forest species growing in field environments maintained at twice-ambient CO2 concentrations, Medlyn et al. (1999) found that the mean photosynthetic acclimation effect in the CO2-enriched trees was characterized by an average reduction of 19 percent in their rates of net photosynthesis when measured at temporary ambient CO2 concentrations relative to the mean rate of net photosynthesis exhibited by those trees that had always been exposed to ambient air. Nonetheless, in nearly every reported case of CO2-induced photosynthetic acclimation in trees, the photosynthetic rates of trees growing and measured in CO2-enriched air have still been much greater than those exhibited by trees growing and measured in ambient air.
CO2-induced photosynthetic acclimation, when it occurs, often results from insufficient plant sink strength, which can lead to carbohydrate accumulation in source leaves and the triggering of photosynthetic end-product feedback inhibition, which results in reduced rates of net photosynthesis. Pan et al. (1998), for example, reported that apple seedlings grown at an atmospheric CO2 concentration of 1600 ppm had foliar starch concentrations 17-fold greater than those observed in leaves of seedlings grown at 360 ppm CO2, suggesting that this phenomenon likely triggered the reductions in leaf net photosynthesis rates they observed. Similarly, Rey and Jarvis (1998) reported that the accumulation of starch within leaves of CO2-enriched silver birch seedlings (100 percent above ambient) may have induced photosynthetic acclimation in that species. Also, in the study of Wiemken and Ineichen (2000), a 300-ppm increase in the air’s CO2 concentration induced seasonal acclimation in young spruce trees, where late-summer, fall and winter rates of net photosynthesis declined in conjunction with 40 to 50 percent increases in foliar glucose levels.
In some cases, trees can effectively increase their sink strength, and thus reduce the magnitude of CO2-induced photosynthetic acclimation, by forming symbiotic relationships with certain species of soil fungi. Under such conditions, photosynthetic down regulation is not triggered as rapidly, or as frequently, by end-product feedback inhibition, as excess carbohydrates are mobilized out of the trees’ source leaves and sent belowground to support the growth of symbiotic fungi. Jifon et al. (2002), for example, reported that the degree of CO2-induced photosynthetic acclimation in sour orange tree seedlings was significantly reduced by the presence of mycorrhizal fungi, which served as sinks for excess carbohydrates synthesized by the CO2-enriched seedlings.
During acclimation to elevated CO2, the amounts and activities of rubisco and/or other photosynthetic proteins are often reduced, which effectively increases the amount of nitrogen available for enhancing sink development or stimulating other nutrient-limited processes. As an example of this phenomenon operating in trees, in the study of Blaschke et al. (2001), the authors reported that a doubling of the atmospheric CO2 concentration reduced foliar rubisco concentrations by 15 and 30 percent in two mature oak species growing near CO2-emitting springs. Similarly, a 200-ppm increase in the air’s CO2 content reduced foliar rubisco concentrations in young aspen and birch seedlings by 39 percent (Takeuchi et al., 2001) and 24 percent (Tjoelker et al., 1998), respectively. Also, in two Pinus radiata studies, seedlings fumigated with air containing 650 ppm CO2 displayed 30 to 40 percent reductions in rubisco concentration and rubisco activity relative to measurements made on seedlings grown in ambient air (Griffin et al., 2000; Turnbull et al., 1998). Other studies of CO2-enriched Norway spruce and Scots pines have documented CO2-induced reductions in foliar chlorophyll contents of 17 percent (Spunda et al., 1998) and 26 percent (Gielen et al., 2000), respectively. And in the study of Gleadow et al. (1998), elevated CO2 led to acclimation in eucalyptus seedlings, which mobilized nitrogen away from rubisco and into prunasin, a sugar-based defense compound that deters herbivory.
In another interesting experiment, Polle et al. (2001) germinated acorns from oak trees exposed to ambient and CO2-enriched air and subsequently grew them at ambient and twice-ambient atmospheric CO2 concentrations. They discovered that seedlings derived from acorns produced on CO2-enriched trees exhibited less-pronounced photosynthetic acclimation to elevated CO2 than did seedlings derived from acorns produced on ambiently grown trees, suggesting the possibility of generational adaptation to higher atmospheric CO2 concentrations over even longer periods of time.
In summary, these many peer-reviewed scientific studies suggest that as the air’s CO2 content slowly but steadily rises, trees may be able to avoid photosynthetic acclimation if they maintain a proper balance between carbohydrate sources and sinks at the whole-tree level, which they may well be able to do in response to the current rate of rise of the air’s CO2 concentration (a mere 1.5 ppm per year). If a tree cannot initially balance its sources and sinks of carbohydrates, however, acclimation is an important and effective means of achieving that balance through redistributing essential resources away from the tree’s photosynthetic machinery in an effort to strengthen sink development, enhance various nutrient-limited processes, and increase nutrient acquisition by, for example, stimulating the development of roots and their symbiotic fungal partners. And if those adjustments are not entirely successful, it is still the case that the acclimation process is hardly ever 100 percent complete (in the studies reviewed here it was on the order of 20 percent), so that tree growth is almost always significantly enhanced in CO2-enriched air in nearly every real-world setting.
Climate Change Reconsidered: Website of the Nongovernmental International Panel on Climate Change. http://www.nipccreport.org/archive/archive.html
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Huxman, T.E. and Smith, S.D. 2001. Photosynthesis in an invasive grass and native forb at elevated CO2 during an El Niño year in the Mojave Desert. Oecologia 128: 193-201.
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Roumet, C., Garnier, E., Suzor, H., Salager, J.-L. and Roy, J. 2000. Short and long-term responses of whole-plant gas exchange to elevated CO2 in four herbaceous species. Environmental and Experimental Botany 43: 155-169.
Staddon, P.L., Fitter, A.H. and Robinson, D. 1999. Effects of mycorrhizal colonization and elevated atmospheric carbon dioxide on carbon fixation and below-ground carbon partitioning in Plantago lanceolata. Journal of Experimental Botany 50: 853-860.
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Blaschke, L., Schulte, M., Raschi, A., Slee, N., Rennenberg, H. and Polle, A. 2001. Photosynthesis, soluble and structural carbon compounds in two Mediterranean oak species (Quercus pubescens and Q. ilex) after lifetime growth at naturally elevated CO2 concentrations. Plant Biology 3: 288-297.
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Gleadow, R.M., Foley, W.J. and Woodrow, I.E. 1998. Enhanced CO2 alters the relationship between photosynthesis and defense in cyanogenic Eucalyptus cladocalyx F. Muell. Plant, Cell and Environment 21: 12-22.
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Tjoelker, M.G., Oleksyn, J. and Reich, P.B. 1998. Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature. Tree Physiology 18: 715-726.
Turnbull, M.H., Tissue, D.T., Griffin, K.L., Rogers, G.N.D. and Whitehead, D. 1998. Photosynthetic acclimation to long-term exposure to elevated CO2 concentration in Pinus radiata D. Don. is related to age of needles. Plant, Cell and Environment 21: 1019-1028.
Wiemken, V. and Ineichen, K. 2000. Seasonal fluctuations of the levels of soluble carbohydrates in spruce needles exposed to elevated CO2 and nitrogen fertilization and glucose as a potential mediator of acclimation to elevated CO2. Journal of Plant Physiology 156: 746-750.