OsNUOR enhances disease susceptibility by interfering with reactive oxygen species homeostasis and ferroptosis-like cell death.

Abstract

Necrotrophic fungal pathogens such as Rhizoctonia solani, the causal agent of rice (Oryza sativa) sheath blight disease, enhance reactive oxygen species (ROS) production to induce necrosis in infected tissues. Here, we present evidence that the host alternative NADH:ubiquinone oxidoreductase (OsNUOR) facilitates R. solani infection by promoting an oxidative-stress-enriched environment and inducing iron-dependent ferroptosis-like cell death. OsNUOR overexpression (OE) lines exhibit enhanced disease susceptibility, whereas knock-out (KO) lines developed through genome editing demonstrate increased resistance. Infected OE lines have enhanced accumulation of ROS, lipid peroxides, and ferric ions (Fe3+); a significant reduction in antioxidative enzyme (including glutathione peroxidase) activity; and depletion of glutathione levels. In KO lines, the redox status of infected tissues is maintained, and the antioxidative defense is activated. Our data suggest that upregulation of OsNUOR induces mitochondrial ROS accumulation and modulates redox signalling, leading to Fe3+ accumulation and lipid peroxidation that promote necrosis in rice. KO lines are compromised in these processes and therefore exhibit disease resistance. We demonstrate that treatment with ferroptosis inhibitors prevents necrotic lesions, whereas ferroptosis inducers enhance disease severity. Overall, our study reveals the importance of ferroptosis-like cell death in promoting necrosis during R. solani infection in rice.