Higher adaxial-to-abaxial stomatal density ratio in C3 cereals than dicots facilitates stomatal kinetics and water use efficiency

Abstract

Stomatal anatomical traits are known to influence stomatal movements and water use efficiency (WUE). However, it is unclear how strongly stomatal distribution regulates stomatal kinetics and WUE. In this study, we examined gas exchange parameters and stomatal traits in five cereal and five dicotyledonous C3 crops to study the relationship between stomatal distribution and stomatal kinetics. Using modeling and experimental validation, we further assessed the impacts of stomatal distribution on WUE in cereals and dicots, represented by rye and cotton, respectively. Results showed that stomatal kinetics were specifically correlated with the ratio of adaxial to abaxial stomatal density (SR) across these C3 crops. Moreover, increased SR could reduce water loss by accelerating stomatal closure when transitioning from light to darkness, thereby significantly improving leaf intrinsic WUE and reducing whole-plant water consumption under well-watered and drought conditions. In addition, the higher SR observed in cereals than dicots contributed to the former’s faster stomatal kinetics and enhanced WUE. These findings highlight the critical function of stomatal distribution on stomatal kinetics and WUE in C3 crops, and its differential regulation between cereals and dicots, providing a feasible approach for breeding drought-tolerant crops in future water-saving agriculture.