NLRs guard metabolism to coordinate pattern- and effector-triggered immunity

Pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) in plants enable them to respond to pathogens by activating the production of defence metabolites that orchestrate immune responses(1-4). How the production of defence metabolites is promoted by immune receptors and coordinated with broad-spectrum resistance remains elusive. Here we identify the deubiquitinase PICI1 as an immunity hub for PTI and ETI in rice (Oryza sativa). PICI1 deubiquitinates and stabilizes methionine synthetasesto activate methionine-mediated immunity principally through biosynthesis ofthe phytohormone ethylene. PICI1 istargeted for degradation by blast fungal effectors, including AvrPi9, to dampen PTI. Nucleotide-binding domain, leucine-rich-repeat-containing receptors (NLRB) in the plant immune system, such as PigmR, protect PICI1 from effector-mediated degradation to reboot the methionine-ethylene cascade. Natural variation in the PICI1 gene contributes to divergence in basal blast resistance between the rice subspecies indica andjaponica. Thus, NLRs govern an arms race with effectors, using a competitive mode that hinges on a critical defence metabolic pathway to synchronize PTI with ETI and ensure broad-spectrum resistance.

Automated summary

This study identifies the deubiquitinase PICI1 as a key player in regulating PTI and ETI in rice, promoting the production of defense metabolites by activating methionine synthetase, and ensuring coordination between PTI and ETI. NLRB receptors such as PigmR protect PICI1 from effector-mediated degradation in the plant immune system, contributing to broad-spectrum resistance.