Stomatal-To-Epidermal Cell Size Ratio and Physiological Coordination Influence Stomatal Response Speed to Leaf Water Disruption in Tomato Plants.

The rapidity with which stomata respond to environmental stresses, such as water shortages or changes in atmospheric demand, is crucial for plant survival and increased water use efficiency. We still have limited information on how the anatomy of stomatal complexes relates to physiological variables, such as transpiration or leaf turgor pressure, and thus to their overall response kinetics. We hypothesize that the coordination between the anatomy of the stomatal complex and transpiration influences the speed of stomatal response to environmental stress by affecting turgor pressure dynamics. To test this, we grew tomato plants under different levels of atmospheric demand, or water vapour pressure deficit (VPD), to generate different leaf anatomies in terms of stomatal complexes, as well as to assess their physiological behaviour. We found that plants grown under high evaporative demand developed leaves with smaller stomatal size: epidermal cell size ratio (SS:ECS), higher steady state leaf turgor pressure (Ψ_p-st), and transpiration rates (E_st) than those grown at low VPD, leading to faster stomatal responses to leaf excision, as well as shorter response durations, which were found to be correlated with an increase in the cumulative water use efficiency during the response. We attribute this stomatal kinetics to a fine coordination between these anatomical changes in the stomatal complex and specific physiological traits (E_st, Ψ_p-st), needed for the plants to exhibit such a faster stomatal response. These results highlight the significance of effective coordination between the anatomy of the stomatal complex and associated physiological parameters in optimising stomatal regulation.