C4 photosynthesis and climate through the lens of optimality

CO2, temperature, water availability and light intensity were all potential selective pressures to propel the initial evolution and global expansion of C4 photosynthesis over the last 30 million years. To tease apart how the primary selective pressures varied along this evolutionary trajectory, we coupled photosynthesis and hydraulics models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of resource (e.g. nitrogen) reallocation from the dark to the light reactions during and after the initial formation of C4 syndrome. We show here that the primary selective pressures—all acting upon photorespiration in C3 progenitors—changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root allocation ratio enabled by the C4 carbon-concentrating mechanism led to a C4 advantage without any change in hydraulic properties, but selection on nitrogen reallocation varied. Water limitation was the primary driver for the initial evolution of C4 25-32 million years ago, and could positively select for C4 evolution with atmospheric CO2 as high as 600 ppm. Under these high CO2 conditions, nitrogen reallocation was necessary. Low CO2 and light intensity, but not nitrogen reallocation, were the primary drivers during the global radiation of C4 5-10 MYA. Finally, our results suggest that identifying the predominate selective pressures at the time C4 first evolved within a lineage should help explain current biogeographical distributions.Statement of authorship:HZ, BH and EA conceptualized the study. HZ and EA built the model, HZ and BH put the idea in a general evolutionary context, HZ performed the modeling work and analyzed output data. HZ wrote the first draft, BH and EA contributed substantially to revisions.Significance StatementC4 photosynthesis pathway had evolved more than 60 times independently across the terrestrial plants through mid-Oligocene (~30 MYA) and diversified at late Miocene (5 to 10 MYA). We use an optimal physiology model to examine the primary selective pressures along the evolutionary history. Water limitation was the primary driver for C4 evolution from the initial evolutionary events 25-32 MYA until CO2 became low enough to, along with light intensity, drive the global radiation of C4 5-10 MYA. This modeling framework can be used to investigate evolution of other physiological traits (e.g. N reallocation, hydraulics) after the initial formation of C4 syndrome, which contributed to further increasing productivity of C4 in historical and current environmental conditions.