Histone H3K4 methylation regulates hyphal growth, secondary metabolism and multiple stress responses in Fusarium graminearum

Abstract

Histone H3 lysine 4 methylation (H3K4me) is generally associated with actively transcribed genes in a variety of eukaryotes. The function of H3K4me in phytopathogenic fungi remains unclear. Here, we report that FgSet1 is predominantly responsible for mono-, di- and trimethylation of H3K4 in Fusarium graminearum. The FgSET1 deletion mutant (ΔFgSet1) was crippled in hyphal growth and virulence. H3K4me is required for the active transcription of genes involved in deoxynivalenol and aurofusarin biosyntheses. Unexpectedly, FgSet1 plays an important role in the response of F. graminearum to cell wall-damaging agents via negatively regulating phosphorylation of FgMgv1, a core kinase in the cell wall integrity pathway. In addition, ΔFgSet1 exhibited increased resistance to the transcription elongation inhibitor mycophenolic acid. Yeast two-hybrid assays showed that FgSet1 physically interacts with multiple proteins including FgBre2, FgSpp1 and FgSwd2. FgBre2 further interacts with FgSdc1. Western blotting analyses showed that FgBre2 and FgSdc1 are associated with H3K4me. Both proteins are also involved in regulating deoxynivalenol biosynthesis and in responses to mycophenolic acid and cell wall-damaging agents. Taken together, these data indicate that H3K4me plays critical roles not only in regulation of fungal growth and secondary metabolism but also in multiple stress responses in F. graminearum.

Lack of the COMPASS Component Ccl1 Reduces H3K4 Trimethylation Levels and Affects Transcription of Secondary Metabolite Genes in Two Plant–Pathogenic Fusarium Species

“…Cells of the rice pathogen M. oryzae lacking MoSet1 cannot develop proper infection and asexual reproduction structures (Pham et al, 2015). In contrast to the quite mild phenotypes of Set1 inactivation mutants in the species mentioned above, lack of this gene resulted in severe growth defects, increased stress sensitivity and reduced virulence in F. graminearum (Liu et al, 2015) as well as crippled growth and an almost abolished asexual reproduction in F. fujikuroi . Taken together, this indicates that H3K4 methylation is an essential chromatin modification in fusaria required for a number of cellular processes whereas in N. crassa and A. nidulans this histone mark seems to play only a role in some specialized processes.…”

“…The catalytic subunit, the methyltransferase Set1 (Kmt2), was first identified and co-purified in Saccharomyces cerevisiae together with a complex consisting of eight subunits, i.e., Set1, Bre2, Swd1, Spp1, Swd2, Swd3, Sdc1, and Shg1 (Nislow et al, 1997; Miller et al, 2001; Roguev et al, 2001). Set1 catalyzes mono-, di-, and trimethylation of the fourth lysine at histone 3 (H3K4me1/2/3) (Roguev et al, 2001; Krogan et al, 2002; Liu et al, 2015). However, Set1 alone is not functional as each of the subunits has a specific function in complex assembly and integrity, pattern of global H3K4 methylation and distribution of H3K4me along active genes (Dehé et al, 2006; Shilatifard, 2012).…”

KdmB, a Jumonji Histone H3 Demethylase, Regulates Genome-Wide H3K4 Trimethylation and Is Required for Normal Induction of Secondary Metabolism in Aspergillus nidulans

“…graminearum , a pathogen of wheat and maize, genes in the fusarin C or the carotenoid biosynthesis clusters carried only background levels of this mark [30]. It is still remarkable that Liu and colleagues found an essential function of the H3K4 methyltransferase Set1 for the expression of the TRI gene cluster coding for deoxynivalenol biosynthesis [80] and in this latter study, H3K4me2 was clearly enriched over the background level and positively correlated with active transcription. Additionally, in contrast to our study, Connolly et al [30] found H3K36me3 enrichment across the whole chromosome independent of transcriptional activity.…”

The b‐ZIP transcription factor FgTfmI is required for the fungicide phenamacril tolerance and pathogenecity in Fusarium graminearum

“…S3, Table S2). Additionally, two already identified virulence genes, FgCHS8 and FgSWD2, were also among the genes downregulated in the FgTFMI mutant. Reduction in the expression of these genes may be partially responsible for the defect of virulence in the ΔFgTfmI mutant.…”