Genome-Wide Characterization of the RNA Exosome Complex in Relation to Growth, Development, and Pathogenicity of Fusarium graminearum

The RNA exosome complex is a conserved, multisubunit RNase complex that contributes to the processing and degradation of RNAs in mammalian cells. However, the roles of the RNA exosome in phytopathogenic fungi and how it relates to fungal development and pathogenicity remain unclear. Herein, we identified 12 components of the RNA exosome in the wheat fungal pathogen Fusarium graminearum. Live-cell imaging showed that all the components of the RNA exosome complex are localized in the nucleus. FgEXOSC1 and FgEXOSCA were successfully knocked out; they are both involved in the vegetative growth, sexual reproduction, and pathogenicity of F. graminearum. Moreover, deletion of FgEXOSC1 resulted in abnormal toxisomes, decreased deoxynivalenol (DON) production, and downregulation of the expression levels of DON biosynthesis genes. The RNA-binding domain and N-terminal region of FgExosc1 are required for its normal localization and functions. Transcriptome sequencing (RNA-seq) showed that the disruption of FgEXOSC1 resulted in differential expression of 3,439 genes. Genes involved in processing of noncoding RNA (ncRNA), rRNA and ncRNA metabolism, ribosome biogenesis, and ribonucleoprotein complex biogenesis were significantly upregulated. Furthermore, subcellular localization, green fluorescent protein (GFP) pulldown, and coimmunoprecipitation (co-IP) assays demonstrated that FgExosc1 associates with the other components of the RNA exosome to form the RNA exosome complex in F. graminearum. Deletion of FgEXOSC1 and FgEXOSCA reduced the relative expression of some of the other subunits of the RNA exosome. Deletion of FgEXOSC1 affected the localization of FgExosc4, FgExosc6, and FgExosc7. In summary, our study reveals that the RNA exosome is involved in vegetative growth, sexual reproduction, DON production, and pathogenicity of F. graminearum. IMPORTANCE The RNA exosome complex is the most versatile RNA degradation machinery in eukaryotes. However, little is known about how this complex regulates the development and pathogenicity of plant-pathogenic fungi. In this study, we systematically identified 12 components of the RNA exosome complex in Fusarium head blight fungus Fusarium graminearum and first unveiled their subcellular localizations and established their biological functions in relation to the fungal development and pathogenesis. All the RNA exosome components are localized in the nucleus. FgExosc1 and FgExoscA are both required for the vegetative growth, sexual reproduction, DON production and pathogenicity in F. graminearum. FgExosc1 is involved in ncRNA processing, rRNA and ncRNA metabolism process, ribosome biogenesis and ribonucleoprotein complex biogenesis. FgExosc1 associates with the other components of RNA exosome complex and form the exosome complex in F. graminearum. Our study provides new insights into the role of the RNA exosome in regulating RNA metabolism, which is associated with fungal development and pathogenicity.