Allocation of the epidermis to stomata relates to stomatal physiological control: Stomatal factors involved in the evolutionary diversification of the angiosperms and development of amphistomaty

•The number and size of stomata over a leaf surface determines potential gas exchange.•Optimal allocation of the epidermis to stomata (EP%) has influenced plant evolution.•The velocity of stomatal conductance (Gs) adjustment was positively related to EP%.•Velocity of Gs adjustment also correlated to occurrence of hypostomaty/amphistomaty.•Low [CO2] favours angiosperms with increased EP% and velocity of Gs adjustment. The proportion of the leaf epidermis allocated to stomata (EP%) and stomatal function (the capacity to adjust stomatal pore area to regulate stomatal conductance: Gs) are key components in leaf gas exchange, and have likely played a major role in plant evolution. We examined the velocity of change in Gs (Gs50%) during a transition from steady state conditions in the light to darkness and EP% in 31 vascular plants with diverse evolutionary origins. Across all species, EP% correlated to Gs50% and the magnitude of Gs reduction (GsLIGHT-GsDARK) after the cessation of illumination. Those species with higher absolute and relative Gs50% values tended to distribute stomata more evenly over the abaxial and adaxial leaf surfaces, whereas species with lower Gs50% utilised only one leaf surface for gas exchange. Groups that diverged at relatively early stages in plant phylogeny, including ferns, gymnosperms and basal angiosperms, exhibited lower EP% and Gs50%, and took longer to achieve the initial 50% reduction in Gs (T50%) than the more recently diverging angiosperms; in particular, the amphistomatous monocot grasses, which also showed higher absolute rates of photosynthesis and Gs. We propose that selective pressures induced by declining [CO2] over the past 100 Myr have favoured greater allocation of the epidermis to stomata, increased amphistomaty (the presence of stomata on the abaxial and adaxial surfaces) and faster control of Gs in the more recently derived angiosperm groups. Modification of photosynthesis to enhance the carbon and water use efficiencies of C3 crops may therefore require concurrent increases in stomatal density and in the capacity of stomata to react quickly to environmental pressures.