Rubisco is the primary carboxylating enzyme used by C3 plants during photosynthesis to incorporate CO2 into sugars needed for growth and development. Even C4 and CAM plants, which use PEP-carboxylase as their primary carboxylating enzyme, utilize rubisco during subsequent secondary CO2 assimilation events. Thus, rubisco is universally present in all of earth's vegetation and is, in fact, the most abundant plant enzyme on the planet, comprising up to 40 to 50% of total foliage protein. Hence, rubisco represents an enormous sink for nitrogen and other valuable resources within plants.
Rubisco, however, is a bifunctional enzyme that also possesses oxygenation activity; and when oxygenation reactions occur, photorespiration is enhanced, resulting in an increased loss of carbon from plant tissues. Thus, CO2 and O2 compete for active sites on rubisco to drive photosynthesis and photorespiration, respectively. How are these biochemical processes affected by the rising CO2 content of the air? And what are the implications of any potential changes in the content and/or activity of rubisco?
Voluminous experimental data demonstrate that atmospheric CO2 enrichment favors carboxylation over oxygenation, thereby increasing photosynthetic rates with concomitant reductions in photorespiratory rates. The rising CO2 content of the air thus invariably leads to greater rates of net photosynthesis and a more efficient process of carbon fixation. Hence, less rubisco is needed to obtain the carbon required for plant growth and development under CO2-enriched conditions.
As a consequence of these facts, plants grown in elevated CO2 environments often, but not always (Farage et al., 1998), exhibit some degree of photosynthetic acclimation or downregulation, which is typically characterized by reduced amounts of rubisco (Sims et al., 1998; Theobald et al., 1998) and/or decreases in its activation state (Pritchard et al., 2000; Reid et al., 1998). However, in nearly every reported case of CO2-induced photosynthetic acclimation, net photosynthetic rates displayed by CO2-enriched plants were still significantly greater than those exhibited by plants growing at ambient CO2 concentrations. In this summary, we thus review the photosynthetic acclimation of rubisco within agricultural species subjected to elevated CO2 concentrations.
In the study of Sicher and Bunce (1999), the authors grew potato plants at atmospheric CO2 concentrations of 350, 530 and 700 ppm over a three-year period and documented 13 and 21% CO2-induced reductions in rubisco concentrations at 530 and 700 ppm CO2, respectively. Nonetheless, rates of photosynthesis in the CO2-enriched plants were still 28 and 49% greater than those observed in control plants grown in ambient air. Similarly, Maroco et al. (1999) reported that a tripling of the ambient CO2 concentration increased photosynthetic rates in maize (a C4 plant) by about 15%, in spite of foliar reductions in both rubisco and PEP-carboxylase concentrations. In addition, Theobald et al. (1998) grew spring wheat at twice-ambient CO2 concentrations and determined that elevated CO2 reduced the amount of rubisco required to sustain enhanced rates of photosynthesis, which lead to a significant increase in plant nitrogen-use efficiency.
Interestingly, when elevated CO2 induces photosynthetic acclimation, the phenomenon generally does not occur in every leaf of the plant. Osborne et al. (1998), for example, grew wheat plants with an additional 200 ppm of CO2 and reported that CO2-induced reductions in foliar rubisco concentrations occurred in a depth-dependent manner, with the reductions increasing with depth in the canopy. Likewise, Sims et al. (1999) documented similar canopy-depth-dependent reductions in rubisco content in sunflowers. Thus, because CO2-induced reductions in rubisco typically occur for only a portion of a plant's total leaf area, most plants still exhibit biomass increases in response to elevated CO2 exposure in spite of 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 that reduces foliar rubisco concentrations. Gesch et al. (1998), for example, 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 leaf rubisco protein contents.
In another experiment, Gesch et al. (2000) took rice plants growing in ambient air and placed them in an atmospheric CO2 concentration of 175 ppm, which reduced their rates of photosynthesis by 45%. However, after five days of exposure to this sub-ambient CO2 concentration, the plants manifested an upregulation of rubisco, which stimulated photosynthetic rates by 35%. Thus, plant acclimation responses can involve both increases and decreases in specific enzymes, depending on the nature of the change in atmospheric CO2 concentration.
These several observations demonstrate the reduced need for nitrogen investment in leaf rubisco in plants growing in CO2-enriched environments. Under such conditions, plants are able to reallocate some of their "surplus" nitrogen to other processes that are essential to optimal growth and development without compromising enhanced carbon gains via photosynthesis. The end result, as almost always observed in well-run experiments, is increased biomass production in CO2-enriched air [see our Plant Growth Data section].
References
Farage, P.K., McKee, I.F. and Long, S.P. 1998. Does a low nitrogen supply necessarily lead to acclimation of photosynthesis to elevated CO2? Plant Physiology 118: 573-580.
Gesch, R.W., Boote, K.J., Vu, J.C.V., Allen, L.H., Jr. and Bowes, G. 1998. Changes in growth CO2 result in rapid adjustments of ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit gene expression in expanding and mature leaves of rice. Plant Physiology 118: 521-529.
Gesch, R.W., Vu, J.C.V., Boote, K.J., Allen, L.H., Jr. and Bowes, G. 2000. Subambient growth CO2 leads to increased Rubisco small subunit gene expression in developing rice leaves. Journal of Plant Physiology 157: 235-238.
Maroco, J.P., Edwards, G.E. and Ku, M.S.B. 1999. Photosynthetic acclimation of maize to growth under elevated levels of carbon dioxide. Planta 210: 115-125.
Osborne, C.P., LaRoche, J., Garcia, R.L., Kimball, B.A., Wall, G.W., Pinter, P.J., Jr., LaMorte, R.L., Hendrey, G.R. and Long, S.P. 1998. Does leaf position within a canopy affect acclimation of photosynthesis to elevated CO2? Plant Physiology 117: 1037-1045.
Pritchard, S.G., Ju, Z., van Santen, E., Qiu, J., Weaver, D.B., Prior, S.A. and Rogers, H.H. 2000. The influence of elevated CO2 on the activities of antioxidative enzymes in two soybean genotypes. Australian Journal of Plant Physiology 27: 1061-1068.
Reid, C.D., Fiscus, E.L. and Burkey, K.O. 1998. Combined effects of chronic ozone and elevated CO2 on rubisco activity and leaf components in soybean (Glycine max). Journal of Experimental Botany 49: 1999-2011.
Sicher, R.C. and Bunce, J.A. 1999. Photosynthetic enhancement and conductance to water vapor of field-grown Solanum tuberosum (L.) in response to CO2 enrichment. Photosynthesis Research 62: 155-163.
Sims, D.A., Cheng, W., Luo, Y. and Seeman, J.R. 1999. Photosynthetic acclimation to elevated CO2 in a sunflower canopy. Journal of Experimental Botany 50: 645-653.
Sims, D.A., Luo, Y. and Seeman, J.R. 1998. Comparison of photosynthetic acclimation to elevated CO2 and limited nitrogen supply in soybean. Plant, Cell and Environment 21: 945-952.
Theobald, J.C., Mitchell, R.A.C., Parry, M.A.J. and Lawlor, D.W. 1998. Estimating the excess investment in ribulose-1,5-bisphosphate carboxylase/oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiology 118: 945-955.