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 CO₂ into organic matter. Globally, photosynthetic efficiency in terrestrial plants has become increasingly challenged in recent decades due to a rapid increase in atmospheric CO₂ and associated changes toward warmer and dryer environments. Well adapted for these new climatic conditions, the C₄ photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO₂ concentrations surrounding RuBisCO, suppressing photorespiration from the oxygenase catalyzed reaction with O₂. The energy efficiency of C₃ photosynthesis, from which the C₄ pathway evolved, is thought to rely critically on an uninterrupted supply of chloroplast CO₂. Part of the homeostatic mechanism that maintains this constancy of supply involves the CO₂ 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 C₃ and C₄ examples are available, the C₄ pathway evolved only from C₃ 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 CO₂ levels required for development of the photorespiratory CO₂ pump (C₂ photosynthesis) essential in the initial stages of C₄ evolution, while in the later stage (final optimization phase in the Flaveria model) increased CO₂ turnover may have occurred, which would have been supported by the higher CO₂ levels. Otherwise, C₄ RuBisCO kinetic traits remain little changed from the ancestral C₃ species. At the opposite end of the spectrum, C₃ plants (from Limonium) with higher than average S_C/O, which may be associated with the ability of increased CO₂, relative to O₂, affinity to offset reduced photorespiration and chloroplast CO₂ 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 CO₂ supply under a broad range of abiotic environmental conditions.