Alternative NADH:ubiquinone oxidoreductase modulates disease susceptibility in rice by interfering ROS homeostasis and ferroptosis

Necrotrophic fungal pathogens, such as Rhizoctonia solani, the causal agent of sheath blight disease (SBD) in rice, enhance the production of reactive oxygen species (ROS) to induce necrosis and infect a broad range of plant species. Here, we present evidence that the upregulation of host alternative NADH:ubiquinone oxidoreductase (OsNUOR) is important for R. solani to induce ROS production and cause SBD in rice. The knock-out lines developed through genome editing are defective in ROS accumulation and demonstrate SBD resistance, whereas the overexpression lines exhibit enhanced disease susceptibility. We emphasize that the cross-talk between OsNUOR and ROS signaling is important for the suppression of antioxidant defense, followed by enhancement of lipid peroxidation and accumulation of ferric ions in rice under R. solani-infected conditions. Considering that treatment with deferoxamine, an iron chelator, and ferrostatin-1, a lipid peroxidation inhibitor, prevents SBD disease, whereas FeCl3 enhances disease severity, we propose that R. solani induces iron-dependent cell death, referred to as ferroptosis, in rice. As agronomic traits of OsNUOR-edited lines are comparable to wild-type lines, we emphasize that editing of OsNUOR and additional genes in ferroptotic pathway can be utilized as biotechnological interventions for control of SBD, for which effective control measures remain a challenge.