Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis

Nature. 2020 Feb;578(7796):577-581. doi: 10.1038/s41586-020-2032-3. Epub 2020 Feb 19.

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 cues1-4. 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.

MeSH terms

  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Calcium / metabolism
  • Calcium Channels / metabolism
  • Calcium Signaling
  • Cysteine / chemistry
  • Cysteine / metabolism
  • Enzyme Activation
  • Hydrogen Peroxide / metabolism*
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mutation
  • Oxidation-Reduction
  • Plant Cells / metabolism
  • Protein Domains
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*

Substances

  • Arabidopsis Proteins
  • Calcium Channels
  • Membrane Proteins
  • Hydrogen Peroxide
  • At5g49760 protein, Arabidopsis
  • Protein Serine-Threonine Kinases
  • Cysteine
  • Calcium