An uORF-encoded mobile peptide sparks systemic stomatal immunity.

Abstract

Higher organisms spread external stimuli from the perceptive tissues to the whole body to achieve systemic responses. In plants, guard cells sense pathogens and close stomata to prevent their entry. We observed that pathogen-infected local leaves transmit the danger status to uninfected distal systemic leaves and trigger their stomatal closure as a global defense termed systemic stomatal immunity (SSIM). The underlying mobile signals remain unknown. Here, we report that an upstream open reading frame (uORF)-encoded systemic stomatal immune conductor (USIC) acts as a long-distance mobile peptide inducing SSIM. In local leaves, USIC increases upon pathogen/pattern signals and is secreted into the apoplast for long-distance transport. In systemic leaves, USIC is perceived by the cell surface SUCROSE-INDUCED RECEPTOR KINASE 1 (SIRK1)-KINASE 7 (KIN7) receptor complex and induces METACASPASE 4 (MC4)-mediated KIN7 cleavage. KIN7 associates with proton pumps/aquaporins to regulate stomatal closure. This study reveals a systemic signaling mechanism whereby an uORF-encoded mobile signal and its receptor pathway activate SSIM.