GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis

Recognition of extracellular peptides by plasma membrane‐localized receptor proteins is commonly used in signal transduction. In plants, very little is known about how extracellular peptides are processed and activated in order to allow recognition by receptors. Here, we show that induction of cell death in planta by a secreted plant protein GRIM REAPER (GRI) is dependent on the activity of the type II metacaspase METACASPASE‐9. GRI is cleaved by METACASPASE‐9 in vitro resulting in the release of an 11 amino acid peptide. This peptide bound in vivo to the extracellular domain of the plasma membrane‐localized, atypical leucine‐rich repeat receptor‐like kinase POLLEN‐SPECIFIC RECEPTOR‐LIKE KINASE 5 (PRK5) and was sufficient to induce oxidative stress/ROS‐dependent cell death. This shows a signaling pathway in plants from processing and activation of an extracellular protein to recognition by its receptor. Synopsis In plants, ROS‐induced cell death requires Metacaspase‐9‐mediated processing of secreted protein GRIM REAPER to produce the peptide ligand for PRK5. Secreted protein GRIM REAPER is processed by Metacaspase‐9, resulting in a small peptide. The peptide binds to the extracellular domain of the leucine‐rich repeat receptor‐like protein kinase PRK5. PRK5 has no kinase activity, but acts as a peptide receptor in vivo . Metacaspase‐9 and PRK5 are required for cell death induction by GRIM REAPER. Graphical Abstract In plants, ROS‐induced cell death requires Metacaspase‐9‐mediated processing of secreted protein GRIM REAPER to produce the peptide ligand for PRK5.