The Transcription Factor FgAtrR Regulates Asexual and Sexual Development, Virulence, and DON Production and Contributes to Intrinsic Resistance to Azole Fungicides in Fusarium graminearum

SIMPLE SUMMARY: Fusarium graminearum is a devastating plant pathogen that can cause wheat head blight. Azole fungicides are commonly used chemicals for control of this disease. However, F. graminearum strains resistant to these fungicides have emerged. To better understand the azole resistance mechanism of F. graminearum, we identified and characterized the Zn(II)2-Cys6 transcription factor FgAtrR in F. graminearum. We found that FgAtrR played critical roles in vegetative growth, conidia production, perithecium formation, and virulence on wheat heads and corn silks. FgAtrR was also involved in the resistance to azole antifungals by regulating the expression of the drug target FgCYP51s and efflux pump transporters. These results broadened our understanding of the azole resistance mechanisms of F. graminearum. ABSTRACT: Fusarium graminearum is the predominant causal agent of cereal Fusarium head blight disease (FHB) worldwide. The application of chemical fungicides such as azole antifungals is still the primary method for FHB control. However, to date, our knowledge of transcriptional regulation in the azole resistance of F. graminearum is quite limited. In this study, we identified and functionally characterized a Zn(II)2-Cys6 transcription factor FgAtrR in F. graminearum. We constructed a FgAtrR deletion mutant and found that deletion of FgAtrR resulted in faster radial growth with serious pigmentation defects, significantly reduced conidial production, and an inability to form perithecia. The pathogenicity of the ΔFgAtrR mutant on wheat spikes and corn silks was severely impaired with reduced deoxynivalenol production, while the tolerance to prochloraz and propiconazole of the deletion mutant was also significantly decreased. RNA-seq indicated that many metabolic pathways were affected by the deletion of FgAtrR. Importantly, FgAtrR could regulate the expression of the FgCYP51A and ABC transporters, which are the main contributors to azole resistance. These results demonstrated that FgAtrR played essential roles in asexual and sexual development, DON production, and pathogenicity, and contributed to intrinsic resistance to azole fungicides in F. graminearum. This study will help us improve the understanding of the azole resistance mechanism in F. graminearum.