The Impact of Atmospheric Composition on the Evolutionary Development of Stomatal Control and Biochemistry of Photosynthesis over the Past 450 Ma

Abstract

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.