Photorespiration in Phase III of Crassulacean Acid Metabolism: Evolutionary and Ecophysiological Implications

Abstract

Ribulose-bis-phosphate carboxylase/oxygenase (RubisCO), the enzyme of primary CO₂-fixation in photosynthesis, from its early evolution in a high CO₂ and low O₂ atmosphere has inherited a dual affinity for both CO₂ and O₂. The reaction with O₂ makes photorespiration an unavoidable affix of photosynthesis. The relative CO₂/O₂ specificity of RubisCO has improved during evolution. However, O₂ affinity has been conserved to date and CO₂ affinity has remained rather low. Hence, various inorganic carbon concentrating mechanisms have evolved. Among them, the CO₂-concentrating mechanism of plants with crassulacean acid metabolism (CAM) achieves the strongest increase in CO₂ concentration within the photosynthesizing organs. In the so-called Phase III of CAM, CO₂ fixed via phosphoenolpyruvate carboxylase in the dark period (Phase I of CAM) and stored nocturnally in the form of malate in the vacuoles is remobilized behind closed stomata, and this leads to a 2-fold up to 60-fold increase of CO₂ partial pressures in the leaf air spaces as compared with atmospheric partial pressure. However, this does not eliminate photorespiration because with vigorous CO₂ assimilation at high concentration behind closed stomata, photosynthetic oxygen evolution simultaneously also leads to O₂ concentrating of up to 40% within the leaves. Hence, photorespiration in CAM plants is not only active in Phase IV of CAM when the store of malate is exhausted and stomata open for CO₂ uptake and standard C₃-photosynthesis, but also in Phase III where CO₂ concentrating is counterbalanced by O₂ concentrating. The question arises whether in Phase III photorespiration is quantitatively similar to that in C₃-photosynthesis or suppressed at least to some extent. The particular question asked in this essay is if the ratio of the reaction rates of RubisCO with O₂ and CO₂, ${{{{v^{{{\rm{O}}_{_2}}}}}} \left/ {{{v^{{\rm{C}}{{\rm{O}}_{_2}}}}}} \right.}$, can be calculated using enzyme kinetics formalism with data given in the literature for partial pressures of O₂ and CO₂ in the leaves during Phase III of CAM. Depending on assumptions inherent in kinetic formalisms, the calculations yield different conclusions. According to one approach photorespiration is strongly suppressed in Phase III of CAM. Another assessment suggests that under physiological conditions of C₃-photosynthesis and Phase III of CAM, oxygenase activity in relation to carboxylase activity of RubisCO is not fundamentally different. At the very most in Phase III of CAM, ${{{{v^{{{\rm{O}}_{_2}}}}}} \left/ {{{v^{{\rm{C}}{{\rm{O}}_{_2}}}}}} \right.}$ is about half of that in C₃ photosynthesis but mostly it is much less reduced than that. The result of the second approach currently appears to be more likely in comparison with experimental findings of gas exchange measurements. However, more experimental data are needed for comparison with the theoretical evaluations.