Intra-population variability in genome-wide repressive histone marks underpins differential gene expression in a fungal wheat pathogen

Abstract

Epigenetic modifications influence the expression of phenotypic traits by modulating gene expression and responses to environmental cues. In plant pathogens, the expression of virulence-associated genes such as effectors and gene clusters encoding the production of secondary metabolites are known to be regulated by epigenetic modifications. Modulating epigenetic patterns of such genes is considered a key adaptation for pathogens to successfully attack hosts. Gene expression variation within pathogen species are regulated by extensive cis- regulatory polymorphism and insertion activities of transposable elements. However, whether pathogens vary in epigenetic profiles among members of the same species remains largely unexplored. Here, we focus on the major fungal wheat pathogen Zymoseptoria tritici and establish histone methylation profiles for 45 isolates of an extensively characterized wheat field population. We analyzed the facultative heterochromatin mark H3K27me3, a histone methylation that is thought to regulate effector and gene cluster loci in the genome. H3K27m3 coverage was increased in transposable element rich regions, with newly inserted long-terminal repeat retrotransposons contributing to epigenetic variation among pathogen genotypes. Overall, nearly 20% of all genes showed within-population variation in H3K27me3 marks, which likely contributes to the substantial within-population variation in gene expression. Effector candidate genes and members of gene clusters showed higher than average variation in repressive histone marks among isolates. Taken together, our study provides among the first insights into intra-species epigenetic variation of a fungal pathogen. Such population-level variation in histone methylation patterns opens avenues to recapitulate epigenetic mechanisms of pathogen adaptation.