Genetic Differentiation in the S dh C Subunit Confers Intrinsic Resistance to SDHI Fungicides in Fusarium asiaticum

Fusarium head blight (FHB), caused by Fusarium asiaticum, is a significant wheat disease in China, reducing yields and contaminating grain with deoxynivalenol (DON). Due to the absence of highly resistant wheat varieties, chemical control remains the primary method for managing FHB. This study identified two homologous SDHC genes in F. asiaticum, namely FaSDHC1 and FaSDHC2. Deletion of FaSDHC2 impaired fungal sporulation, virulence and DON production, whereas the loss of FaSDHC1 increased DON production. Both genes were found to regulate sensitivity to SDHI fungicides-ΔFaSDHC1 showed decreased sensitivity, while ΔFaSDHC2 exhibited increased sensitivity. To explore the regulatory role of the SdhC subunit in SDHI fungicides sensitivity in F. asiaticum, this study obtained 11 boscalid-resistant mutants from ΔFaSDHC2 through chemical taming. Genetic analysis identified six mutation genotypes, including two previously reported in Fusarium species (FaSdhB-H248Y and FaSdhD-E166K) and four novel mutations in the Fusarium genus (FaSdhC1-H144Y, FaSdhC1-H144N, FaSdhD-H122Y and FaSdhD-D133N). The site-directed mutation verification and sensitivity assays revealed that mutants harbouring FaSdhC1-H144Y/N, FaSdhD-H122Y, FaSdhD-D133N or FaSdhD-E166K exhibited resistance to multiple SDHI fungicides (boscalid, fluopyram, pydiflumetofen, isopyrazam and benzovindiflupyr). In contrast, FaSdhB-H248Y mutants remained sensitive to fluopyram while showing resistance to other SDHI fungicides. This study elucidates the important regulatory role of SdhC genetic differentiation to SDHI fungicide sensitivity in F. asiaticum. Furthermore, it confirms that specific variations within distinct subunits of the SDH complex endow F. asiaticum with resistance to SDHI fungicides. The findings advance understanding of SDHI fungicides resistance mechanisms and provide a basis for developing FaSdhC-specific inhibitors and resistance management strategies.