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Set2 and Ash1 are histone methyltransferases (KMTs) in the KMT3 family normally used to catalyze methylation of histone H3K36 (H3K36me) but remain unexplored in fungal insect pathogens. Here, we report broader/greater roles of Set2 and Ash1 in mono-/di-/trimethylation (me1/me2/me3) of H3K4 than of H3K36 in  Beauveria bassiana  and function similarly to Set1/KMT2, which has been reported to catalyze H3K4me3 as an epigenetic mark of  cre1  (carbon catabolite repressor) to upregulate the classes I and II hydrophobin genes  hyd1  and  hyd2  required for conidial hydrophobicity and adherence to insect cuticle. H3K4me3 was more attenuated than H3K36me3 in the absence of  set2  (72% versus 67%) or  ash1  (92% versus 12%), leading to sharply repressed or nearly abolished expression of  cre1 ,  hyd1  and  hyd2 , as well as reduced hydrophobicity. Consequently, the delta- set2  and delta- ash1  mutants were differentially compromised in radial growth on various media or under different stresses, aerial conidiation under normal culture conditions, virulence, and cellular events crucial for normal cuticle infection and hemocoel colonization, accompanied by transcriptional repression of subsets of genes involved in or required for asexual development and multiple stress responses. These findings unravel novel roles of Set2 and Ash1 in the co-catalysis of usually Set1-reliant H3K4me3 required for fungal insect-pathogenic lifestyle.

Conserved and Noncanonical Activities of Two Histone H3K36 Methyltransferases Required for Insect-Pathogenic Lifestyle of Beauveria bassiana