Identifying transcription factors associated with Fusarium graminearum virus 2 accumulation in Fusarium graminearum by phenome-based investigation

•FgV2 was transferred to F. graminearum transcription factor deletion mutant library.•Defective RNAs adversely affected FgV2 accumulation and vertical transmission.•Some TFs were involved in the transcription of FgDICER-2 and FgAGO-1 against FgV2.•FgV2 infection depressed the resistance to hydroxyurea of TF mutant.•FgV2 accumulation was lower in ROS-excessive TF mutants compared to WT. Fusarium graminearum virus 2 (FgV2) infection induces phenotypic changes like reduction of growth rate and virulence with an alteration of the transcriptome, including various transcription factor (TFs) gene transcripts in Fusarium graminearum. Transcription factors are the primary regulator in many cellular processes and are significant in virus-host interactions. However, a detailed study about specific TFs to understand interactions between FgV2 and F. graminearum has yet to be conducted. We transferred FgV2 to a F. graminearum TF gene deletion mutant library to identify host TFs related to FgV2 infection. FgV2-infected TF mutants were classified into three groups depending on colony growth. The FgV2 accumulation level was generally higher in TF mutants showing more reduced growth. Among these FgV2-infected TF mutants, we found several possible TFs that might be involved in FgV2 accumulation, generation of defective interfering RNAs, and transcriptional regulation of FgDICER-2 and FgAGO-1 in response to virus infection. We also investigated the relation between FgV2 accumulation and production of reactive oxygen species (ROS) and DNA damage in fungal host cells by using DNA damage- or ROS-responsive TF deletion mutants. Our studies provide insights into the host factors related to FgV2 infection and bases for further investigation to understand interactions between FgV2 and F. graminearum.