Regulation and Virulence Function of Fusarium graminearum Secondary Metabolites During Arabidopsis thaliana Infection

Abstract

During plant infection, Fusarium graminearum induces secondary metabolite production, which include mycotoxins and virulence factors, to overcome host defenses. Different hosts can elicit expression of distinct secondary metabolite biosynthetic genes through unknown host-derived signals. Here, we investigate how the Arabidopsis thaliana NADPH oxidase gene RbohD, which contributes to stress-induced reactive oxygen species (ROS) bursts, influences fungal secondary metabolite gene expression during seedling infection. F. graminearum infection induces progressive accumulation of ROS in Arabidopsis cotyledons which accompanied by tissue whitening. In the fungus, 650 genes are differentially expressed during infection including 51 secondary metabolite biosynthetic genes from the trichothecene, culmorin, fusaoctaxin, butenolide and fungal decalin-containing diterpenoid pyrone clusters (FDDP). In F. graminearum-infected rbohD knockout plants, cotyledon ROS accumulation was attenuated and fungal expression of genes from the trichothecene, fusaoctaxin, butenolide, and FDDP clusters were reduced. Knocking out other host susceptibility genes, including RLK7, ILK1, and APEX, had no effect on ROS accumulation and impacted expression of fewer fungal secondary metabolite genes. Abolishment of fungal production of deoxynivalenol, fusaoctaxin, and FDDP reduced F. graminearum virulence and resulted in increased callose production in the host during infection. Together, these findings indicate that the Arabidopsis RbohD gene influences F. graminearum pathogenesis and expression of secondary metabolite virulence factors during infection.