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The regulation of virulence in plant-pathogenic fungi has emerged as a key area of importance underlying host infections. Recent work has highlighted the role of transcription factors (TFs) that mediate the expression of virulence-associated genes. A prominent example is Pf2, a member of the Zn2Cys6 family of fungal TFs, where orthologues regulate the expression of genes linked to parasitism in several plant-pathogen lineages. These include PnPf2 which controls effector-gene expression in Parastagonospora nodorum, thereby determining the outcome of effector-triggered susceptibility on its host, wheat. PnPf2 is a promising target for disease suppression but the genomic targets, or whether other are regulators involved, remain unknown. This study used chromatin immunoprecipitation (ChIP-seq) and a mutagenesis analysis to investigate these components. Two distinct binding motifs connected to positive gene-regulation were characterised and genes directly targeted by PnPf2 were identified. These included genes encoding major effectors and other components associated with the P. nodorum pathogenic lifestyle, such as carbohydrate-active enzymes and nutrient assimilators. This supports a direct involvement of PnPf2 in coordinating virulence on wheat. Other TFs were also prominent PnPf2 targets, suggesting it also operates within a transcriptional network. Several TFs were therefore functionally investigated in connection to fungal virulence. Distinct metabolic and developmental roles were evident for the newly characterised PnPro1, PnAda1, PnEbr1 and the carbon-catabolite repressor PnCreA. Overall, the results uphold PnPf2 as the central transcriptional regulator orchestrating genes that contribute to virulence on wheat and provide mechanistic insight into how this occurs.ImportanceFungal pathogens cause large crop losses worldwide and consequently much attention has focused on improving host genetic resistance to diseases. These pathogens use effectors, which require coordinated expression at specific stages of the pathogenic lifecycle, to manipulate the host plant metabolism in favour of infection. However, our understanding of the underlying regulatory network in coordination with other genes involved in fungal pathogenicity is lacking. The Pf2 TF orthologues are key players underpinning virulence and effector gene expression in several fungal phytopathogens, including P. nodorum. This study provided significant insight into the DNA-binding regulatory mechanisms of P. nodorum PnPf2, as well as further evidence that it is central to the coordination of virulence. In the context of crop protection, the Pf2 taxonomic orthologues present opportune targets in major fungal pathogens that can be perturbed to reduce the impact of effector triggered-susceptibility and improve disease resistance.

Fungal pathogens represent a serious threat towards agriculture, health, and environment. Control of fungal diseases on crops necessitates a global understanding of fungal pathogenicity determinants and their expression during infection. Genomes of phytopathogenic fungi are often compartmentalized: the core genome contains housekeeping genes whereas the fast-evolving genome mainly contains transposable elements and species-specific genes. In this study, we analysed nucleosome landscapes of four phytopathogenic fungi with contrasted genome organizations to describe and compare nucleosome repartition patterns in relation with genome structure and gene expression level. We combined MNase-seq and RNA-seq analyses to concomitantly map nucleosome-rich and transcriptionally active regions during fungal growth in axenic culture; we developed the MNase-seq Tool Suite (MSTS) to analyse and visualise data obtained from MNase-seq experiments in combination with other genomic data and notably RNA-seq expression data. We observed different characteristics of nucleosome profiles between species, as well as between genomic regions within the same species. We further linked nucleosome repartition and gene expression. Our findings support that nucleosome positioning and occupancies are subjected to evolution, in relation with underlying genome sequence modifications. Understanding genomic organization and its role in expression regulation is the next gear to understand complex cellular mechanisms and their evolution.

Leptosphaeria maculans ‘brassicae’ (Lmb) and Leptosphaeria maculans ‘lepidii’ (Lml) are closely related phytopathogenic species that exhibit a large macrosynteny but contrasting genome structure. Lmb has more than 30% of repeats clustered in large repeat-rich regions, while the Lml genome has only a small amount of evenly distributed repeats. Repeat-rich regions of Lmb are enriched in effector genes, expressed during plant infection. The distinct genome structures of Lmb and Lml provide an excellent model for comparing the organization of pathogenicity genes in relation to the chromatin landscape in two closely related phytopathogenic fungi. Here, we performed chromatin immunoprecipitation (ChIP) during axenic culture, targeting histone modifications typical for heterochromatin or euchromatin, combined with transcriptomic analysis to analyze the influence of chromatin organization on gene expression. In both species, we found that facultative heterochromatin is enriched with genes lacking functional annotation, including numerous effector and species-specific genes. Notably, orthologous genes located in H3K27me3 domains are enriched with effector genes. Compared to other fungal species, including Lml, Lmb is distinct in having large H3K9me3 domains associated with repeat-rich regions that contain numerous species-specific effector genes. Discovery of these two distinctive heterochromatin landscapes now raises questions about their involvement in the regulation of pathogenicity, the dynamics of these domains during plant infection and the selective advantage to the fungus to host effector genes in H3K9me3 or H3K27me3 domains. Supplementary Information The online version contains supplementary material available at 10.1007/s10577-021-09658-1.

The fungus Leptosphaeria maculans has an exceptionally long and complex relationship with its host plant, Brassica napus, during which it switches between different lifestyles, including asymptomatic, biotrophic, necrotrophic, and saprotrophic stages. The fungus is also exemplary of “two-speed” genome organisms in which gene-rich and repeat-rich regions alternate. Except for a few stages of plant infection under controlled conditions, nothing is known about the genes mobilized by the fungus throughout its life cycle, which may last several years in the field. We show here that about 9% of the genes of this fungus are highly expressed during its interactions with its host plant. These genes are distributed into eight well-defined expression clusters, corresponding to specific infection lifestyles or to tissue-specific genes. All expression clusters are enriched in effector genes, and one cluster is specific to the saprophytic lifestyle on plant residues. One cluster, including genes known to be involved in the first phase of asymptomatic fungal growth in leaves, is re-used at each asymptomatic growth stage, regardless of the type of organ infected. The expression of the genes of this cluster is repeatedly turned on and off during infection. Whatever their expression profile, the genes of these clusters are located in regions enriched in heterochromatin, either constitutive or facultative. These findings provide support for the hypothesis that fungal genes involved in niche adaptation are located in heterochromatic regions of the genome, conferring an extreme plasticity of expression. This work opens up new avenues for plant disease control, by identifying stage-specific effectors that could be used as targets for the identification of novel durable disease resistance genes, or for the in-depth analysis of chromatin remodeling during plant infection, which could be manipulated to interfere with the global expression of effector genes at crucial stages of plant infection.Author SummaryFungi are extremely important organisms in the global ecosystem. Some are damaging plant pathogens that threaten global food security. A knowledge of their biology and pathogenic cycle is vital for the design of environmentally-friendly control strategies. Unfortunately, many parts of their life cycle remain unknown, due to the complexity of their life-cycles and technical limitations. Here, we use a rapeseed pathogen, Leptosphaeria maculans, which has a particularly complex life-cycle, to show that large-scale RNA-Seq analyses of fungal gene expression can decipher all stages of the fungal cycle over two years of interaction with living or dead hosts, in laboratory and agricultural conditions. We found that the fungus uses about 9% of the genes of its genome specifically during interactions with the plant, and observed waves of extremely tight, complex regulation during the colonization of specific tissues and specific parts of the life-cycle. Our findings highlight the importance of genes encoding effectors, small secreted proteins manipulating the host. This work opens up new avenues for plant disease control through the identification of stage-specific effectors leading to the discovery of novel durable disease resistance genes, or the analysis of epigenetic regulation, which could be manipulated to interfere with effector gene expression.

International audience; A central feature of meiosis is pairing of homologous chromosomes , which occurs in two stages: coalignment of axes followed by installation of the synaptonemal complex (SC). Concomitantly, recombination complexes reposition from on-axis association to the SC central region. We show here that, in the fungus $Sordaria\ macrospora$, this critical transition is mediated by robust interaxis bridges that contain an axis component (Spo76/Pds5), DNA, plus colocalizing Mer3/Msh4 recombination proteins and the Zip2-Zip4 mediator complex. Mer3-Msh4-Zip2-Zip4 colocalizing foci are first released from their tight axis association, dependent on the SC transverse-filament protein Sme4/Zip1, before moving to bridges and thus to a between-axis position. Ensuing shortening of bridges and accompanying juxtaposition of axes to 100 nm enables installation of SC central elements at sites of between-axis Mer3-Msh4-Zip2-Zip4 complexes. We show also that the Zip2-Zip4 complex has an intrinsic affinity for chromosome axes at early leptotene, where it localizes independently of recombination, but is dependent on Mer3. Then, later, Zip2-Zip4 has an intrinsic affinity for the SC central element, where it ultimately localizes to sites of crossover complexes at the end of pachytene. These and other findings suggest that the fundamental role of Zip2-Zip4 is to mediate the recombina-tion/structure interface at all post-double-strand break stages. We propose that Zip2-Zip4 directly mediates a molecular handoff of Mer3-Msh4 complexes, from association with axis components to association with SC central components, at the bridge stage, and then directly mediates central region installation during SC nucleation. meiotic recombination | synaptonemal complex | Zip2-Zip4 | chromosome structure | interaxis bridges T he central feature of meiotic prophase, which distinguishes it from the mitotic cell cycle, is a complex program of interactions between homologous maternal and paternal chromosomes ("homologs"). A major event of this program is the coming-together of homologous axes, first via coalignment and then via synapsis mediated by the tripartite protein structure called synaptonemal complex (SC). In most organisms, coalignment and SC formation are directly mediated by recombination. Recombination initiates through DNA double-strand breaks (DSBs) that occur within axis-associated recombination complexes (reviewed in ref. 1). For coalignment, a consensus hypothesis is that one DSB end searches for a DNA partner on the homologous chromosome. A resultant nascent D-loop between the DSB end and its homologous DNA region nucleates development of a partner recombination complex, which then becomes associated with the underlying partner axis, where it mediates spatial juxtaposition of the linked two chromosome axes (reviewed in ref. 2). Occurrence of such events at many positions along the chromosomes results in coalignment of axes all along their lengths. Following coalignment, formation of the SC at some of the coalignment-mediated recombination sites brings homologous axes together by installation of SC central elements (reviewed in refs. 3-5). The transition from coalignment to synapsis is a major event of meiotic prophase. One of the most interesting features of this transition is the fact that recombination complexes must undergo a major change in localization: from the on-axis position that occurs before and during coalignment (above) to a between-axis position on the central region of the SC. Once the SC has formed, recombination complexes are associated with the SC central element, and crossover (CO)-fated recombination complexes retain this association throughout ensuing recombination events, with mature COs finally emerging shortly before the SC is disassembled (reviewed in refs. 2 and 6). Existing information provides some clues about the nature of this transition. i) First, EM images in Allium cepa have defined the existence of bridges between coaligned axes, including bridges with centrally localized nodules (7). Although the involved proteins remain unknown, these bridges/nodules likely represent the sites of recombinational interactions. Accordingly, in human and mouse spermatocytes, RPA (Replication Protein A) and BLM (Bloom Syndrome Protein) proteins are visible either as matching foci still attached to their coaligned axis or as coalescent foci now forming a bridge linking the two axes before onset of SC formation (8-10). ii) Second, studies in budding yeast have identified a set of molecules that coordinately mediate both SC nucleation and progression of CO-designated recombination interactions (11-13). This group, referred to as "ZMM" proteins, includes SC transverse-filament protein Zip1, the SUMO Significance The central feature of meiosis is pairing and recombination of homologous maternal and paternal chromosomes (homologs). Homolog axes become first coaligned at a certain distance; they then synapse by synaptonemal complex (SC) formation. We show that the structural and molecular pathway by which chromosomes transit from coalignment to the SC state in the fungus Sordaria macrospora involves the formation of robust interaxis bridges comprising axis component Spo76/Pds5, re-combination proteins, and the evolutionary-conserved Zip2-Zip4 complex. Zip2-Zip4 mediates the recombination complex/ structure interface from coalignment onward. These findings solve the conundrum of how recombination complexes move from on-axis localization at coalignment to between-axis lo-calization on SC central regions and provoke new ideas about the molecular and mechanistic nature of SC nucleation.

Chromosome and genome stability are important for normal cell function as instability often correlates with disease and dysfunction of DNA repair mechanisms. Many organisms maintain supernumerary or accessory chromosomes that deviate from standard chromosomes. The pathogenic fungus Zymoseptoria tritici has as many as eight accessory chromosomes, which are highly unstable during meiosis and mitosis, transcriptionally repressed, show enrichment of repetitive elements, and enrichment with heterochromatic histone methylation marks, e.g., trimethylation of H3 lysine 9 or lysine 27 (H3K9me3, H3K27me3). To elucidate the role of heterochromatin on genome stability in Z. tritici, we deleted the genes encoding the methyltransferases responsible for H3K9me3 and H3K27me3, kmt1 and kmt6, respectively, and generated a double mutant. We combined experimental evolution and genomic analyses to determine the impact of these deletions on chromosome and genome stability, both in vitro and in planta. We used whole genome sequencing, ChIP-seq, and RNA-seq to compare changes in genome and chromatin structure, and differences in gene expression between mutant and wildtype strains. Analyses of genome and ChIP-seq data in H3K9me3-deficient strains revealed dramatic chromatin reorganization, where H3K27me3 is mostly relocalized into regions that are enriched with H3K9me3 in wild type. Many genome rearrangements and formation of new chromosomes were found in the absence of H3K9me3, accompanied by activation of transposable elements. In stark contrast, loss of H3K27me3 actually increased the stability of accessory chromosomes under normal growth conditions in vitro, even without large scale changes in gene activity. We conclude that H3K9me3 is important for the maintenance of genome stability because it disallows H3K27me3 in regions considered constitutive heterochromatin. In this system, H3K27me3 reduces the overall stability of accessory chromosomes, generating a “metastable” state for these quasi-essential regions of the genome., Author summary Genome and chromosome stability are essential to maintain normal cell function and viability. However, differences in genome and chromosome structure are frequently found in organisms that undergo rapid adaptation to changing environmental conditions, and in humans are often found in cancer cells. We study genome instability in a fungal pathogen that exhibits a high degree of genetic diversity. Regions that show extraordinary diversity in this pathogen are the transposon-rich accessory chromosomes, which contain few genes that are of unknown benefit to the organism but maintained in the population and thus considered “quasi-essential”. Accessory chromosomes in all fungi studied so far are enriched with markers for heterochromatin, namely trimethylation of H3 lysine 9 and 27 (H3K9me3, H3K27me3). We show that loss of these heterochromatin marks has strong but opposing effects on genome stability. While loss of the transposon-associated mark H3K9me3 destabilizes the entire genome, presence of H3K27me3 favors instability of accessory chromosomes. Our study provides insight into the relationship between chromatin and genome stability and why some regions are more susceptible to genetic diversity than others.

SummaryDuring infection, pathogens secrete effectors, key elements of pathogenesis. In several phytopathogenic fungi, synchronous waves of effector genes are expressed during plant infection to manipulate and silence plant defenses. In Zymoseptoria tritici, causing septoria leaf blotch of wheat, at least two waves of effector genes are expressed, during the asymptomatic phase and at the switch to necrotrophy. The underlying factors responsible for the fine-tuned regulation of effector gene expression in this pathogen are unknown. Previously, a detailed map of the chromatin structure in vitro of Z. tritici was generated by chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq) targeting histone modifications typical for euchromatin (di-methylation of the lysine 4 of the histone H3, H3K4me2) or heterochromatin (tri-methylation of the lysine 9 and 27 of the histone H3, H3K9me3 and H3K27me3). Based on the hypothesis that changes in the histone modifications contribute to the transcriptional control of pathogenicity-related genes, we tested whether different sets of genes are associated with different histone modifications in vitro. We correlated the in vitro histone maps with in planta transcriptome data and show that genes located in heterochromatic domains in vitro are highly up-regulated at the switch toward necrotrophy. We combined our integrated analyses of genomic, transcriptomic and epigenomic data with ChIP-qPCR in planta and thereby provide further evidence for the involvement of histone modifications in the transcriptional dynamic of putative pathogenicity-related genes of Z. tritici.

first posted online on May 16, 2018; International audience; Filamentous pathogens, including fungi and oomycetes, pose major threats to global food security. Crop pathogens cause damage by secreting effectors that manipulate the host to the pathogen’s advantage. Genes encoding such effectors are among the most rapidly evolving genes in pathogen genomes. Here, we review how the major characteristics of the emergence, function, and regulation of effector genes are tightly linked to the genomic compartments where these genes are located in pathogen genomes. The presence of repetitive elements in these compartments is associated with elevated rates of point mutations and sequence rearrangements with a major impact on effector diversification. The expression of many effectors converges on an epigenetic control mediated by the presence of repetitive elements. Population genomics analyses showed that rapidly evolving pathogens show high rates of turnover at effector loci and display a mosaic in effector presence-absence polymorphism among strains. We conclude that effective pathogen containment strategies require a thorough understanding of the effector genome biology and the pathogen’s potential for rapid adaptation.

International audience; Plant-associated fungi often present in their genome areas enriched in repeat sequences and effector genes, the latter being specifically induced in planta. The location of effector genes in regions enriched in repeats has been shown to have an impact on adaptability of fungi but could also provide for tight control of effector gene expression through chromatin-based regulation. The distribution of two repressive histone marks was shown to be an important regulatory layer in two fungal species with different lifestyles. Chromatin-based control of effector gene expression is likely to provide an evolutionary advantage by preventing the expression of genes not needed during vegetative growth and allow for a massive concerted expression at particular time-points of plant infection.

Summary Leptosphaeria maculans causes stem canker of oilseed rape (Brassica napus). The APSES transcription factor StuA is a key developmental regulator of fungi, involved in morphogenesis, conidia production and also more recently described as required for secondary metabolite production and for effector gene expression in phytopathogenic fungi. We investigated the involvement of the orthologue of StuA in L. maculans, LmStuA, in morphogenesis, pathogenicity and effector gene expression. LmStuA is induced during mycelial growth and at 14 days after infection, corresponding to the development of pycnidia on oilseed rape leaves, consistent with the function of StuA described so far. We set up the functional characterization of LmStuA using an RNA interference approach. Silenced LmStuA transformants showed typical phenotypic defects of StuA mutants with altered growth in axenic culture and impaired conidia production and perithecia formation. Silencing of LmStuA abolished the pathogenicity of L. maculans on oilseed rape leaves and also resulted in a drastic decrease in expression of at least three effector genes during in planta infection, suggesting either that LmStuA regulates, directly or indirectly, the expression of several effector genes in L. maculans or that the infection stage in which effectors are expressed is not reached when LmStuA expression is silenced.

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Background Supernumerary chromosomes have been found in many organisms. In fungi, these “accessory” or “dispensable” chromosomes are present at different frequencies in populations and are usually characterized by higher repetitive DNA content and lower gene density when compared to the core chromosomes. In the reference strain of the wheat pathogen, Zymoseptoria tritici, eight discrete accessory chromosomes have been found. So far, no functional role has been assigned to these chromosomes; however, they have existed as separate entities in the karyotypes of Zymoseptoria species over evolutionary time. In this study, we addressed what—if anything—distinguishes the chromatin of accessory chromosomes from core chromosomes. We used chromatin immunoprecipitation combined with high-throughput sequencing (“ChIP-seq”) of DNA associated with the centromere-specific histone H3, CENP-A (CenH3), to identify centromeric DNA, and ChIP-seq with antibodies against dimethylated H3K4, trimethylated H3K9 and trimethylated H3K27 to determine the relative distribution and proportion of euchromatin, obligate and facultative heterochromatin, respectively. Results Centromeres of the eight accessory chromosomes have the same sequence composition and structure as centromeres of the 13 core chromosomes and they are of similar length. Unlike those of most other fungi, Z. tritici centromeres are not composed entirely of repetitive DNA; some centromeres contain only unique DNA sequences, and bona fide expressed genes are located in regions enriched with CenH3. By fluorescence microscopy, we showed that centromeres of Z. tritici do not cluster into a single chromocenter during interphase. We found dramatically higher enrichment of H3K9me3 and H3K27me3 on the accessory chromosomes, consistent with the twofold higher proportion of repetitive DNA and poorly transcribed genes. In contrast, no single histone modification tested here correlated with the distribution of centromeric nucleosomes. Conclusions All centromeres are similar in length and composed of a mixture of unique and repeat DNA, and most contain actively transcribed genes. Centromeres, subtelomeric regions or telomere repeat length cannot account for the differences in transfer fidelity between core and accessory chromosomes, but accessory chromosomes are greatly enriched in nucleosomes with H3K27 trimethylation. Genes on accessory chromosomes appear to be silenced by trimethylation of H3K9 and H3K27. Electronic supplementary material The online version of this article (doi:10.1186/s13072-015-0033-5) contains supplementary material, which is available to authorized users.

The presence or absence of specific transcription factors, chromatin remodeling machineries, chromatin modification enzymes, post-translational histone modifications and histone variants all play crucial roles in the regulation of pathogenicity genes. Chromatin immunoprecipitation (ChIP) followed by high-throughput sequencing (ChIP-seq) provides an important tool to study genome-wide protein–DNA interactions to help understand gene regulation in the context of native chromatin. ChIP-seq is a convenient in vivo technique to identify, map and characterize occupancy of specific DNA fragments with proteins against which specific antibodies exist or which can be epitope-tagged in vivo. We optimized existing ChIP protocols for use in the wheat pathogen Zymoseptoria tritici and closely related sister species. Here, we provide a detailed method, underscoring which aspects of the technique are organism-specific. Library preparation for Illumina sequencing is described, as this is currently the most widely used ChIP-seq method. One approach for the analysis and visualization of representative sequence is described; improved tools for these analyses are constantly being developed. Using ChIP-seq with antibodies against H3K4me2, which is considered a mark for euchromatin or H3K9me3 and H3K27me3, which are considered marks for heterochromatin, the overall distribution of euchromatin and heterochromatin in the genome of Z. tritici can be determined. Our ChIP-seq protocol was also successfully applied to Z. tritici strains with high levels of melanization or aberrant colony morphology, and to different species of the genus (Z. ardabiliae and Z. pseudotritici), suggesting that our technique is robust. The methods described here provide a powerful framework to study new aspects of chromatin biology and gene regulation in this prominent wheat pathogen.

Background Many plant-pathogenic fungi have a tendency towards genome size expansion, mostly driven by increasing content of transposable elements (TEs). Through comparative and evolutionary genomics, five members of the Leptosphaeria maculans-Leptosphaeria biglobosa species complex (class Dothideomycetes, order Pleosporales), having different host ranges and pathogenic abilities towards cruciferous plants, were studied to infer the role of TEs on genome shaping, speciation, and on the rise of better adapted pathogens. Results L. maculans ‘brassicae’, the most damaging species on oilseed rape, is the only member of the species complex to have a TE-invaded genome (32.5%) compared to the other members genomes (

Plant pathogens secrete an arsenal of small secreted proteins (SSPs) acting as effectors that modulate host immunity to facilitate infection. SSP-encoding genes are often located in particular genomic environments and show waves of concerted expression at diverse stages of plant infection. To date, little is known about the regulation of their expression. The genome of the Ascomycete Leptosphaeria maculans comprises alternating gene-rich GC-isochores and gene-poor AT-isochores. The AT-isochores harbor mosaics of transposable elements, encompassing one-third of the genome, and are enriched in putative effector genes that present similar expression patterns, namely no expression or low-level expression during axenic cultures compared to strong induction of expression during primary infection of oilseed rape (Brassica napus). Here, we investigated the involvement of one specific histone modification, histone H3 lysine 9 methylation (H3K9me3), in epigenetic regulation of concerted effector gene expression in L. maculans. For this purpose, we silenced the expression of two key players in heterochromatin assembly and maintenance, HP1 and DIM-5 by RNAi. By using HP1-GFP as a heterochromatin marker, we observed that almost no chromatin condensation is visible in strains in which LmDIM5 was silenced by RNAi. By whole genome oligoarrays we observed overexpression of 369 or 390 genes, respectively, in the silenced-LmHP1 and -LmDIM5 transformants during growth in axenic culture, clearly favouring expression of SSP-encoding genes within AT-isochores. The ectopic integration of four effector genes in GC-isochores led to their overexpression during growth in axenic culture. These data strongly suggest that epigenetic control, mediated by HP1 and DIM-5, represses the expression of at least part of the effector genes located in AT-isochores during growth in axenic culture. Our hypothesis is that changes of lifestyle and a switch toward pathogenesis lift chromatin-mediated repression, allowing a rapid response to new environmental conditions., Author Summary Effectors are key players in pathogenicity of microbes toward plants. Effector genes usually show concerted expression during plant infection but how this concerted expression is generated remains a largely unexplored research topic. Epigenetic mechanisms are involved in genome maintenance and integrity but are increasingly considered as important for regulation of gene expression in numerous and diverse organisms. Here we show that the genomic environment has impact on expression of Leptosphaeria maculans effector genes, and that an epigenetic mechanism that relies on two proteins involved in heterochromatin formation and maintenance, HP1 and DIM-5, modulates this expression, leading to repression during growth in axenic culture. Chromatin decondensation by removal of histone H3 lysine 9 methylation and/or HP1 is presumably a prerequisite for effector gene expression during primary infection of oilseed rape. Thus we show chromatin-based transcriptional regulation that can act on effector gene expression in fungi. Our study highlights the importance of heterochromatic landscapes, not only for genome maintenance but also in rapid and efficient adaptation of organisms to changing environmental situations.