Enhanced production of OsRACK1A, an effector-targeted scaffold protein that promotes OsRBOHB-mediated ROS production, confers rice floral resistance to false smut disease without yield penalty.

Grain formation is fundamental for crop yield but is vulnerable to abiotic and biotic stresses. Rice grain production is threatened by the false smut fungus, Ustilaginoidea virens, that specifically infects rice floral organs to intercept fertilization and seed formation. However, little is known on molecular mechanisms of U. virens-rice interaction and genetic basis of floral resistance. Here, we report that U. virens secretes a cytoplasmic effector UvCBP1 for facilitating infection in rice flowers. Mechanistically, UvCBP1 interacts with rice scaffold protein OsRACK1A and competes its interaction with NADPH oxidase OsRBOHB, leading to inhibition of reactive oxygen species (ROS) production. Although natural variation analysis identifies no OsRACK1A variants that avoid being targeted by UvCBP1, OsRACK1A expression levels appear correlated with field resistance against U. virens in rice germplasms. Importantly, overproducing OsRACK1A restores OsRACK1A-OsRBOHB association and promotes OsRBOHB phosphorylation to enhance ROS production, conferring resistance to U. virens while not penalizing rice yield. Our findings thus reveal a new pathogenic mechanism mediated by an essential effector of a flower-specific pathogen and provide a valuable genetic resource for equilibrating disease resistance and crop yield.