H3K27me3 is vital for fungal development and secondary metabolite gene silencing, and substitutes for the loss of H3K9me3 in the plant pathogen Fusarium proliferatum
Facultative heterochromatin marked by histone H3 lysine 27 trimethylation (H3K27me3) is an important regulatory layer for secondary metabolite (SM) gene silencing and important for fungal development in the genus Fusarium. While this histone mark is essential in some (e.g., the rice pathogen Fusarium fujikuroi), it appears dispensable in other fusaria. Here, we show that deletion of FpKMT6 is detrimental but not lethal in the plant pathogen Fusarium proliferatum, a member of the Fusarium fujikuroi species complex (FFSC). Loss of FpKmt6 results in aberrant growth, and expression of a large set of previously H3K27me3-silenced genes is accompanied by increased H3K27 acetylation (H3K27ac) and an altered H3K36me3 pattern. Next, H3K9me3 patterns are affected in delta-fpkmt6, indicating a crosstalk between both heterochromatic marks that became even more obvious in a strain deleted for FpKMT1 encoding the H3K9-specific histone methyltransferase. In delta-fpkmt1, all H3K9me3 marks present in the wild-type strain are replaced by H3K27me3, a finding that possibly explains the subtle phenotype of delta-fpkmt1 strains which stands in marked contrast to other filamentous fungi. A large proportion of SM-encoding genes is allocated with H3K27me3 in the wild-type strain, and loss of H3K27me3 result in elevated expression of 49% of them. Interestingly, genes involved in the biosynthesis of the phytohormones gibberellins (GA) are among the most upregulated genes in delta-fpkmt6. Although several FFSC members harbor GA biosynthetic genes, its production in planta is largely restricted to F. fujikuroi with few exceptions. We show that GA gene silencing is mediated by H3K27me3 in F. proliferatum and in at least one additional FFSC member, possibly outlining the distinct lifestyles of these notorious plant pathogens.