Selective pressures on C4 photosynthesis evolution in grasses through the lens of optimality

Background/Question/Methods CO₂, temperature, water availability and light intensity were potential selective pressures to propel the initial evolution (25-32 MYA) and global expansion of C₄photosynthesis in grasses (5-10 MYA). We teased apart the primary selective pressures along the evolutionary trajectory through the lens of an optimality model. We coupled photosynthesis and hydraulics models and optimized photosynthesis over stomatal resistance and leaf/fine-root allocation. We also examined the importance of nitrogen reallocation from the dark to the light reactions.

Results/Conclusions At CO₂ concentration above 400 ppm, water limitation was the primary selective factor for C₄ evolution, and even at 600 ppm there is room for C₄ evolution under the driest conditions. Furthermore, we find that the carbon concentration mechanism in C₄ (CCM) alone leads to enough of a reduction in water use that there would have been little selection for increased hydraulic conductance within C₄ grasses. When CO₂ decreased below 300 ppm, high light intensity provided an enhanced advantage for C₄. Low CO₂, together with light intensity, were the primary drivers during the global radiation of C₄ 5-10 MYA, occurring hand-in-hand with grassland expansion. Subsequent to the evolution of CCM, selection could favor the reallocation of nitrogen from dark to light reactions. the selection pressure to reallocate would have been strongest when CO₂ was high, i.e., during the initial evolutionary events, when the CCM alone does not give C₄ a large advantage. As CO₂ decreased during the C₄ radiation 5-10 MYA to Pleistocene glacial periods, the CCM alone would give C₄ an advantage and selection of reallocation would lessen. However, as CO₂ increased again from Pleistocene, our modeling results show the N reallocation may play a major role in maintaining the high productivity of C₄ species in current CO₂ concentration.