Updated project metadata. The decision of whether to grow or to divert energy to stress response is a major physiological trade-off for plants in surviving under fluctuating environments. Here we show that three leucine-rich repeat receptor kinases (LRR-RKs) act as direct ligand-perceiving receptors for PLANT PEPTIDE CONTAINING SULFATED TYROSINE (PSY) -family peptides and mediate local switching between two opposing pathways. In contrast to the known LRR-RKs, PSY receptors (PSYRs) activate the expression of various genes encoding stress response transcription factors upon depletion of the ligands. Loss of PSYRs resulted in defects in the plant’s tolerance to both biotic and abiotic stresses. This ligand-deprivation-dependent activation system enables plants to exert tuned regulation of stress responses in the tissues proximal to metabolically dysfunctional damaged sites where ligand production is impaired.