Low relative air humidity leads to smaller, denser stomata and higher stomatal ratios in Arabidopsis

Atmospheric dryness is increasing, bringing about decreases in plant productivity. Stomatal pores mediate plant gas-exchange with the environment, balancing CO2 uptake with water loss. Stomatal anatomical and physiological traits respond to changes in environment, potentially affecting plant growth and yield under future environments. Designing stomatal patterns to suit future climate conditions has the potential to improve plant water use efficiency or productivity. By combining mutations in signaling pathways that control stomatal development and apertures, we designed plants that combine high stomatal densities with more open stomata and show that respective mutations independently affect stomatal conductance and density. Analyses of adaxial and abaxial stomatal conductances showed that in Arabidopsis, adaxial stomata are responsible for a significant proportion of leaf gas-exchange. Adaxial and abaxial stomatal physiology were largely similarly affected by mutations in stomatal regulation pathways but adaxial stomata tended to be relatively more closed than abaxial stomata. We show that growth under low relative air humidity leads to higher stomatal densities and smaller stomata. Stomatal development in the adaxial and abaxial leaf surface responded differently to dry air conditions: adaxial stomatal index increased, whereas abaxial stomatal index decreased. Stomatal ratio increased under dry air conditions, leading to a higher degree of amphistomaty. Plant growth was independently suppressed by dry air and high stomatal density and index. Our results suggest that acclimation to decreasing air humidity leads to stomatal anatomical adjustments that help to maximize plant gas-exchange potential under conditions where water supply may be limited and sporadic.