A Dual‐Role Transcription Factor FpCys3 Couples Glucose Sensing to Methionine Biosynthesis and Virulence in <i>Fusarium pseudograminearum</i>

Fusarium pseudograminearum is a soil-borne phytopathogen that causes Fusarium crown rot (FCR) in wheat and barley, posing a severe threat to global grain yield and quality. A deeper understanding of its pathogenicity is essential for developing effective control strategies. Methionine (Met) has been reported that involved in plant-pathogen interactions at multiple levels, regulating both plant immunity and fungal pathogenicity. Here, we identified a conserved bZIP transcription factor, FpCys3, which is a key mediator of methionine biosynthesis in F. pseudograminearum. The FpCys3 mutant exhibited a series of defects, including reduced tolerance to abiotic stress, decreased conidiation, shortened conidia, reduced septa, and slowed germination rate. Specifically, deletion of FpCys3 led to a significant reduction in the pathogenicity and induced the accumulation of ROS in wheat, and exogenous application of methionine could fully restore the pathogenicity of the ΔFpcys3 mutant. We further demonstrated that FpCys3 binds to the promotors of FpMet16 and FpMet5. In vegetative hyphae, FpCys3 acts as a positive regulator of these genes, and deletion of either FpMet16 or FpMet5 phenocopied the ΔFpcys3 mutant, showing methionine-dependent growth and reduced virulence. Despite containing a C-terminus nuclear localisation signal, FpCys3 did not accumulate in the nucleus under normal conditions. However, during the early infection of F. pseudograminearum on wheat coleoptiles or under glucose treatment, FpCys3 accumulated significantly in the nucleus, where it negatively regulated the expression of FpMet16 and FpMet5, and methionine synthesis. Exogenous glucose treatment markedly alleviated the necrotic lesions of wheat coleoptiles caused by F. pseudograminearum. Collectively, these findings uncover a dual role for FpCys3 in regulating methionine biosynthesis during both fungal development and host-pathogen interactions, providing new insights for exploring pathogen infection mechanisms and plant disease resistance strategies.