Antagonistic systemin receptors integrate the activation and attenuation of systemic wound signaling in tomato
Ke Zhou, Fangming Wu, Lei Deng, Yu Xiao, Wentao Yang, Jiuhai Zhao, Qinyang Wang, Zeqian Chang, Huawei Zhai, Chuanlong Sun, Hongyu Han, Minmin Du, Qian Chen, Jijun Yan, Peiyong Xin, Jinfang Chu, Zhifu Han, Jijie Chai, Gregg A. Howe, Changbao Li, Chuanyou Li
Abstract
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. • SYR1 is a high-affinity systemin receptor and positively regulates SWR • SYR2 is a low-affinity systemin receptor and negatively regulates SWR • SYR2 attenuates SWR by outcompeting SYR1 for binding with the co-receptor SERK3a • The SYR1-SYR2 module opens up avenues for uncoupling growth-defense trade-offs Zhou et al. report that two antagonistic wound peptide hormone systemin receptors (SYR1 and SYR2) enable plants to integrate the attenuation of wound signaling with its activation. Whereas SYR1 acts as a high-affinity receptor to initiate systemin signaling, SYR2 functions as a low-affinity receptor in signaling attenuation in tomato.