The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants

Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO) is the carbon-fixing enzyme present in most photosynthetic organisms, converting CO(2) into organic matter. Globally, photosynthetic efficiency in terrestrial plants has become increasingly challenged in recent decades due to a rapid increase in atmospheric CO(2) and associated changes toward warmer and dryer environments. Well adapted for these new climatic conditions, the C(4) photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO(2) concentrations surrounding RuBisCO, suppressing photorespiration from the oxygenase catalyzed reaction with O(2). The energy efficiency of C(3) photosynthesis, from which the C(4) pathway evolved, is thought to rely critically on an uninterrupted supply of chloroplast CO(2). Part of the homeostatic mechanism that maintains this constancy of supply involves the CO(2) produced as a byproduct of photorespiration in a negative feedback loop. Analyzing the database of RuBisCO kinetic parameters, we suggest that in genera (Flaveria and Panicum) for which both C(3) and C(4) examples are available, the C(4) pathway evolved only from C(3) ancestors possessing much lower than the average carboxylase specificity relative to that of the oxygenase reaction (S(C/O)=S(C)/S(O)), and hence, the higher CO(2) levels required for development of the photorespiratory CO(2) pump (C(2) photosynthesis) essential in the initial stages of C(4) evolution, while in the later stage (final optimization phase in the Flaveria model) increased CO(2) turnover may have occurred, which would have been supported by the higher CO(2) levels. Otherwise, C(4) RuBisCO kinetic traits remain little changed from the ancestral C(3) species. At the opposite end of the spectrum, C(3) plants (from Limonium) with higher than average S(C/O), which may be associated with the ability of increased CO(2), relative to O(2), affinity to offset reduced photorespiration and chloroplast CO(2) levels, can tolerate high stress environments. It is suggested that, instead of inherently constrained by its kinetic mechanism, RuBisCO possesses the extensive kinetic plasticity necessary for adaptation to changes in photorespiration that occur in the homeostatic regulation of CO(2) supply under a broad range of abiotic environmental conditions.