Source  NATURE BIOTECHNOLOGY

Published  SEP 1 2025

DOI: 10.1016/j.molp.2025.07.006

IF  24.1

Abstract

ROPGTPases regulate various cellular processes, including plantimmunity. While ROP GTPase activation has been reported during plant immune responses, the mechanisms underlying the dynamic deactivation of ROP GTPases remain unclear. In this study, we identified the autophagy kinase OsATG1 as a key regu- lator that interacts with , phosphorylates SPIN6, a plant-specific ROP GTPase-activating protein (Rho- GAP), which in turn deactivates the ROPGTPase OsRac1. OsATG1-mediated multi-site phosphorylation is necessary for the GAP activity of SPIN6 to hydrolyze OsRac1-GTP , overexpression of a phosphomimic form of SPIN6 attenuates riceimmunity. We showed that two isoforms of OsATG1, OsATG1a and OsATG1b, operate redundantly in riceimmunity to the fungal pathogen Magnaporthe oryzae. . Double mutants of OsATG1a and OsATG1b exhibit stronger resistance as well as developmental defects and complete steril- ity. Moreover, OsATG1 interacts with OsATG8. Phenotypic analyses of OsATG8 transgenic plants reveal that OsATG8 positively regulates riceimmunity, but OsATG8 activates immunity partially indepen- dent of its function in autophagy, because overexpressing the lipidation-defective OsATG8G117A G117A or accu- mulating non-lipidated OsATG8 in the osatg7 mutant enhances rice disease resistance. Mechanistically, OsATG8 promotes OsATG1 turnover, whereas OsATG8G117A G117A is sufficient to deplete OsATG1, leading to SPIN6 dissociation and degradation. As autophagy is essential in nutrient recycling, we found that nutrient limitations induce OsATG8 expression and riceimmunity while suppressing SPIN6. However, SPIN6 phos- phorylation inhibits this nutrient-limitation-induced immunity. Taken together, our results suggest that OsATG1 and OsATG8 possess autophagy-independentfunctions to transform nutrient limitation into im- munity via plant-specific ROP GTPase signaling.