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 C-4 photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO2 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 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 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 CO2 levels required for development of the photorespiratory CO2 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 CO2 turnover may have occurred, which would have been supported by the higher CO2 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 CO2, relative to O-2, 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.

Automated summary

RuBisCO is the carbon-fixing enzyme in most photosynthetic organisms, with the C4 pathway utilizing carbon concentrating mechanisms to increase CO2 levels, while the energy efficiency of C3 photosynthesis relies on chloroplast CO2 supply. RuBisCO possesses extensive kinetic plasticity for adaptation to changes in photorespiration under various environmental conditions.