The evolution of diffusive and biochemical capacities for photosynthesis was predominantly shaped by [CO2] with a smaller contribution from [O2

Abstract

The atmospheric concentration of carbon dioxide ([CO2]) and oxygen ([O2]) directly influence rates of photosynthesis (PN) and photorespiration (RPR) through the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO). Levels of [CO2] and [O2] have varied over Earth history affecting rates of both CO2 uptake and loss, alongside associated transpirative water-loss. The availability of CO2 has likely acted as a stronger selective pressure than [O2] due to the greater specificity of RubisCO for CO2. The role of [O2], and the interaction of [O2] and [CO2], in plant evolutionary history is less understood. We exposed twelve phylogenetically diverse species to combinations of sub-ambient, ambient and super-ambient [O2] and [CO2] to examine the biochemical and diffusive components of PN and the possible role of [O2] as a selective pressure. Photosynthesis, photosynthetic capacity and stomatal, mesophyll and total conductance to CO2 were higher in the derived eudicot and monocot angiosperms than the more basal ferns, gymnosperms and basal angiosperms which originated in atmospheres characterised by higher CO2:O2 ratios. The ratio of RPR:PN was lower in the monocots, consistent with greater carboxylation capacity and higher stomatal and mesophyll conductance making easier CO2 delivery to chloroplasts. The effect of [O2] and [CO2] on PN/RPR was less evident in more derived species with a higher conductance to CO2. The effect of [O2] was less apparent at high [CO2], suggesting that atmospheric [O2] may only have exerted a strong selective pressure on plant photosynthetic processes during periods characterised by low atmospheric CO2:O2 ratios. Current rising [CO2] will predominantly enhance PN rates in species with low diffusive conductance to CO2.