Dovetailing the Genetic, Developmental and Functional Bases of the Adaptation of Stomatal Traits to Climate.

Stomata, the micro-valves on leaves, regulate CO2 uptake and water loss. Thus, the anatomical maximum stomatal conductance, gmax, is a key influence on gas exchange, growth and productivity. For 145 geographically diverse ecotypes of Arabidopsis thaliana grown in a common garden we tested hypotheses for the drivers of variation in gmax and a stomatal size-density trade-off, considering epidermal optimization, epidermal development and climate adaptation. Ecotypes native to colder and drier macroclimates had higher gmax, consistent with leaf-scale stress-avoidance, despite having longer times to flowering. A high gmax was achieved through greater epidermal allocation to stomata, via both increased guard cell initiation and smaller epidermal pavement cells. Stomatal traits showed polygenic associations with climate. A weak stomatal size-density trade-off was observed for only the abaxial surface, consistent with flexible constraints on stomatal development and independent trait adaptation. Dovetailing mechanisms influence stomatal adaptation to climate across a wide-ranging species.