Chromatin Dynamics Contribute to the Spatiotemporal Expression Pattern of Virulence Genes in a Fungal Plant Pathogen

ABSTRACT Dynamic changes in transcription profiles are key for the success of pathogens in colonizing their hosts. In many pathogens, genes associated with virulence, such as effector genes, are located in regions of the genome that are rich in transposable elements and heterochromatin. The contribution of chromatin modifications to gene expression in pathogens remains largely unknown. Using a combination of a reporter gene-based approach and chromatin immunoprecipitation, we show that the heterochromatic environment of effector genes in the fungal plant pathogen Zymoseptoria tritici is a key regulator of their specific spatiotemporal expression patterns. Enrichment in trimethylated lysine 27 of histone H3 dictates the repression of effector genes in the absence of the host. Chromatin decondensation during host colonization, featuring a reduction in this repressive modification, indicates a major role for epigenetics in effector gene induction. Our results illustrate that chromatin modifications triggered during host colonization determine the specific expression profile of effector genes at the cellular level and, hence, provide new insights into the regulation of virulence in fungal plant pathogens. IMPORTANCE Fungal plant pathogens possess a large repertoire of genes encoding putative effectors, which are crucial for infection. Many of these genes are expressed at low levels in the absence of the host but are strongly induced at specific stages of the infection. The mechanisms underlying this transcriptional reprogramming remain largely unknown. We investigated the role of the genomic environment and associated chromatin modifications of effector genes in controlling their expression pattern in the fungal wheat pathogen Zymoseptoria tritici. Depending on their genomic location, effector genes are epigenetically repressed in the absence of the host and during the initial stages of infection. Derepression of effector genes occurs mainly during and after penetration of plant leaves and is associated with changes in histone modifications. Our work demonstrates the role of chromatin in shaping the expression of virulence components and, thereby, the interaction between fungal pathogens and their plant hosts.