Rapid stomatal closure contributes to higher water use efficiency in major C4 compared to C3 Poaceae crops

Understanding water use characteristics of C3 and C4 crops is important for food security under climate change. Here, we aimed to clarify how stomatal dynamics and water use efficiency (WUE) differ in fluctuating environments in major C3 and C4 crops. Under high and low nitrogen conditions, we evaluated stomatal morphology and kinetics of stomatal conductance (gs) at leaf and whole-plant levels in controlled fluctuating light environments in four C3 and five C4 Poaceae species. We developed a dynamic photosynthesis model, which incorporates C3 and C4 photosynthesis models that consider stomatal dynamics, to evaluate the contribution of rapid stomatal opening and closing to photosynthesis and WUE. C4 crops showed more rapid stomatal opening and closure than C3 crops, which could be explained by smaller stomatal size and higher stomatal density in plants grown at high nitrogen conditions. Our model analysis indicated that accelerating the speed of stomatal closure in C3 crops to the level of C4 crops could enhance WUE up to 16% by reducing unnecessary water loss during low light periods, whereas accelerating stomatal opening only minimally enhanced photosynthesis. The present results suggest that accelerating the speed of stomatal closure in major C3 crops to the level of major C4 crops is a potential breeding target for the realization of water-saving agriculture.