A phosphorelay circuit drives extracellular alkalinization in receptor kinase-mediated immune and cell-wall damage signaling.

Extracellular alkalinization has long been recognized as a hallmark of plant cell-surface receptor activation, including during pattern-triggered immunity (PTI), yet the mechanisms driving elicitor-induced alkalinization and its role in plant signaling remain unclear. Here, we demonstrate that inhibition of autoinhibited H+-ATPases (AHAs) is required for elicitor-induced extracellular alkalinization. This alkalinization is essential for immune and cell-wall damage signaling mediated by diverse plasma membrane-localized receptor kinases (RKs), likely through modulation of ligand-receptor interactions. Mechanistically, RKs transduce elicitor-triggered signaling via the receptor-like cytoplasmic kinase BOTRYTIS-INDUCED KINASE 1 (BIK1), which inhibits AHA activity by disrupting AHA-GENERAL REGULATORY FACTOR (GRF) interactions through a conserved phosphorylation event. This phosphorylation-driven extracellular alkalinization module is required for disease resistance and cell-wall damage responses initiated by ligand-RK pairs. Our findings uncover a conserved phosphorelay circuit that broadly regulates extracellular alkalinization to coordinate RK signaling, illuminating a general mechanism for RK activation and stress resilience.