The impact of atmospheric composition on the evolutionary development of stomatal control and biochemistry of photosynthesis over the past 450 Ma

The conversion of carbon dioxide (CO2) and water into glucose and oxygen (O2) by photosynthesis has been a central component of the atmosphere and climate system over Earth history. The diffusive uptake of CO2 and its biochemical assimilation have in turn been strongly affected by atmospheric composition. Here, we illustrate how declining [CO2] and rising [O2] have exerted selective pressures to reduce the uptake of O2 (photorespiration) in favor of CO2 (photosynthesis) by the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco). In the last 10 Myr when [CO2] fell to less than 300 ppm, C3 photosynthesis became less efficient and mechanisms concentrating CO2 at the rubisco active site were favored leading to the expansion of C4 photosynthesis. The need to optimize carbon gain relative to water-loss has acted as a key selective pressure in the evolutionary development of stomatal function and epidermal patterning, to not only maximize diffusion of CO2 into the leaf but also regulate excessive transpirative water-loss. This stomatal control of photosynthesis generally allows angiosperms to sustain greater levels of stomatal conductance and CO2-uptake than species with more ancient evolutionary origins. This is particularly evident in the grasses, where dumb-bell stomata and the allocation of a higher percentage of the epidermis to gas exchange permit greater rates of stomatal conductance and photosynthesis than species with kidney-shaped stomata. The diffusive and biochemical components of photosynthesis have been strongly influenced by declining CO2:O2 over the past 100 Myr. However, current rising [CO2] may affect these selective pressures, having implications for future plant growth.