Agricultural species grown in elevated CO2 environments often, but not always (Gavito et al., 2000), exhibit some degree of photosynthetic acclimation or down regulation, which is typically characterized by reduced rates of photosynthesis resulting from decreased activity and/or amount of the primary plant carboxylating enzyme rubisco (Ulman et al., 2000; Sims et al., 1999). However, in nearly every reported case of CO2-induced photosynthetic acclimation, the reduced rates of photosynthesis displayed by CO2-enriched plants are typically greater than those exhibited by plants growing at ambient CO2 concentrations. Ziska (1998), for example, reported that soybeans grown at an atmospheric CO2 concentration of 720 ppm initially exhibited photosynthetic rates that were 50% 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% greater than their ambiently-grown counterparts.
Several studies have examined the effects of elevated CO2 on acclimation in wheat. Theobald et al. (1998), for example, 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 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 ultimately 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% 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% 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%. 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%. 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; for if a plant can maintain a balance between its sources and sinks for carbohydrates at the whole-plant level, acclimation should not be necessary. In addition, 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. However, in the event that 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.
References
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