Antagonistic systemin receptors integrate the activation and attenuation of systemic wound signaling in tomato

Pattern recognition receptor (PRR)-mediated perception of damage-associated molecular patterns (DAMPs) triggers the first line of inducible defenses in both plants and animals. Compared with animals, plants are sessile and regularly encounter physical damage by biotic and abiotic factors. A longstanding problem concerns how plants achieve a balance between wound defense response and normal growth, avoiding overcommitment to catastrophic defense. Here, we report that two antagonistic systemin receptors, SYR1 and SYR2, of the wound peptide hormone systemin in tomato act in a ligand-concentration-dependent manner to regulate immune homeostasis. Whereas SYR1 acts as a high-affinity receptor to initiate systemin signaling, SYR2 functions as a low-affinity receptor to attenuate systemin signaling. The expression of systemin and SYR2, but not SYR1, is upregulated upon SYR1 activation. Our findings provide a mechanistic explanation for how plants appropriately respond to tissue damage based on PRR-mediated perception of DAMP concentrations and have implications for uncoupling defense-growth trade-offs.