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.

Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant

“…Genes highly expressed during infection are often associated with heterochromatin during axenic culture (e.g., in Z. tritici or L. maculans [ 4 , 37 , 64 ]) and histone modifications (H3K9me3 and / or H3K27me3) have been shown to play a major role in regulating secondary metabolite gene clusters or effector genes (e.g., in F. graminearum , F. fujikuroi , Z. tritici , Epichloe festucae [ 65 – 69 ]). In the endophyte E. festucae and the pathogen Z. tritici , the derepression of putative effector genes or secondary metabolite gene clusters upon infection is associated with an underlying dynamic of histone modifications, which has been experimentally validated [ 65 , 68 , 70 ]. These data suggest that there is a generic chromatin-based control of plant infection mechanisms.…”

Genome-wide mapping of histone modifications during axenic growth in two species of Leptosphaeria maculans showing contrasting genomic organization

“…Typically, heterochromatin is enriched in the trimethylation of the lysine 9 of histone H3 (H3K9me3) and lysine 27 (H3K27me3) while euchromatin is enriched in the di-(or tri-) methylation of the lysine 4 of histone H3 (H3K4me2); (Mikkelsen et al 2007;Jamieson et al 2013). In fungal plant pathogens or endophytes, evidence is accumulating that transcriptional reprogramming of effector genes (either proteinaceous or metabolic) is tightly controlled by chromatinbased regulatory mechanisms (for example in Fusarium graminearum, Epichloe festucae, Lmb and Zymoseptoria tritici; Connolly et al 2013;Chujo and Scott 2014;Soyer et al 2014Soyer et al , 2015aSoyer et al , 2019Lukito et al 2020;Meile et al 2020). In Lmb, the location of avirulence genes in TE-rich regions has an influence on their evolution under selection pressure (Rouxel et al 2011;Daverdin et al 2012) and plays a role in regulating their expression during axenic culture via deposition of H3K9me3 (Soyer et al 2014).…”

Chromatin landscape dynamics in development of the plant parasitic nematode Meloidogyne incognita

“…H3K27ac is usually found on enhancers and can be used to distinguish between active and poised enhancers Leptosphaeria maculans, are the principal plant-parasitic organisms displaying chromatin-based control of concerted effector gene expression at specific times during infection [53,54]. In Zymoseptoria tritici, the H3K27me3 distribution dictates effector gene expression during host colonization, preventing the expression of these genes when not required [55].…”