Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis

Abstract

Hydrogen peroxide (H₂O₂) is a major reactive oxygen species in unicellular and multicellular organisms, and is produced extracellularly in response to external stresses and internal cues^1-4. H₂O₂ enters cells through aquaporin membrane proteins and covalently modifies cytoplasmic proteins to regulate signalling and cellular processes. However, whether sensors for H₂O₂ also exist on the cell surface remains unknown. In plant cells, H₂O₂ triggers an influx of Ca²⁺ ions, which is thought to be involved in H₂O₂ sensing and signalling. Here, by using forward genetic screens based on Ca²⁺ imaging, we isolated hydrogen-peroxide-induced Ca²⁺ increases (hpca) mutants in Arabidopsis, and identified HPCA1 as a leucine-rich-repeat receptor kinase belonging to a previously uncharacterized subfamily that features two extra pairs of cysteine residues in the extracellular domain. HPCA1 is localized to the plasma membrane and is activated by H₂O₂ via covalent modification of extracellular cysteine residues, which leads to autophosphorylation of HPCA1. HPCA1 mediates H₂O₂-induced activation of Ca²⁺ channels in guard cells and is required for stomatal closure. Our findings help to identify how the perception of extracellular H₂O₂ is integrated with responses to various external stresses and internal cues in plants, and have implications for the design of crops with enhanced fitness.