Optimal coordination and reorganization of photosynthetic properties in C4 grasses

Each of >20 independent evolutions of C-4 photosynthesis in grasses required reorganization of the Calvin-Benson-cycle (CB-cycle) within the leaf, along with coordination of C-4-cycle enzymes with the CB-cycle to maximize CO2 assimilation. Considering the vast amount of time over which C-4 evolved, we hypothesized (i) trait divergences exist within and across lineages with both C-4 and closely related C-3 grasses, (ii) trends in traits after C-4 evolution yield the optimization of C-4 through time, and (iii) the presence/absence of trends in coordination between the CB-cycle and C-4-cycle provides information on the strength of selection. To address these hypotheses, we used a combination of optimality modelling, physiological measurements and phylogenetic-comparative-analysis. Photosynthesis was optimized after the evolution of C-4 causing diversification in maximal assimilation, electron transport, Rubisco carboxylation, phosphoenolpyruvate carboxylase and chlorophyll within C-4 lineages. Both theory and measurements indicated a higher light-reaction to CB-cycle ratio (J(atpmax)/V-cmax) in C-4 than C-3. There were no evolutionary trends with photosynthetic coordination between the CB-cycle, light reactions and the C-4-cycle, suggesting strong initial selection for coordination. The coordination of CB-C-4-cycles (V-pmax/V-cmax) was optimal for CO2 of 200 ppm, not to current conditions. Our model indicated that a higher than optimal V-pmax/V-cmax affects assimilation minimally, thus lessening recent selection to decrease V-pmax/V-cmax.