Chloroplast-derived hydrogen peroxide coordinates photosynthesis with stomatal opening

Abstract

Stomatal pores on plant leaves control the entry point of carbon into the terrestrial biosphere and concomitant release of water vapour into the atmosphere. Stomatal aperture changes need to be coordinated with photosynthesis to balance carbon gain against water loss. Despite this importance, molecular signals underpinning this coordination, and the cell types from which such signals originate, remain poorly understood. Here we show that chloroplast-derived H2O2 coordinates stomatal movements with photosynthesis. Specifically, when H2O2 scavenging is compromised in the cytosolic ascorbate peroxidase1 (apx1) mutant, stomatal opening is increased. This is rescued when photosynthetic H2O2 production derived from plastoquinol is reduced either genetically or pharmacologically. Furthermore, cell-specific complementation of APX1 in the apx1 mutant demonstrated that H2O2 signals from both guard cells and mesophyll cells contribute significantly to stomatal movements. Altogether, our findings identify H2O2 as a key photosynthesis-derived signal underpinning effective coordination between stomatal conductance and photosynthesis, a key prerequisite for terrestrial plant life, and may inspire new strategies to enhance photosynthetic water use efficiency in crop species.