Guard cell endomembrane Ca2+-ATPases underpin a 'carbon memory' of photosynthetic assimilation that impacts on water-use efficiency

Abstract

Stomata of most plants close to preserve water when the demand for CO₂ by photosynthesis is reduced. Stomatal responses are slow compared with photosynthesis, and this kinetic difference erodes assimilation and water-use efficiency under fluctuating light. Despite a deep knowledge of guard cells that regulate the stoma, efforts to enhance stomatal kinetics are limited by our understanding of its control by foliar CO₂. Guided by mechanistic modelling that incorporates foliar CO₂ diffusion and mesophyll photosynthesis, here we uncover a central role for endomembrane Ca²⁺ stores in guard cell responsiveness to fluctuating light and CO₂. Modelling predicted and experiments demonstrated a delay in Ca²⁺ cycling that was enhanced by endomembrane Ca²⁺-ATPase mutants, altering stomatal conductance and reducing assimilation and water-use efficiency. Our findings illustrate the power of modelling to bridge the gap from the guard cell to whole-plant photosynthesis, and they demonstrate an unforeseen latency, or 'carbon memory', of guard cells that affects stomatal dynamics, photosynthesis and water-use efficiency.