Polycomb Repression without Bristles: Facultative Heterochromatin and Genome Stability in Fungi

Ridenour, John B.; Möller, Mareike; Freitag, Michael

doi:10.3390/genes11060638

Cited by 30 publications

(33 citation statements)

References 173 publications

(304 reference statements)

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“…The H3K27me3 mark is catalyzed and maintained by Polycomb group proteins, termed Polycomb Repressive Complex 1 and 2 (PRC1 and PRC2). While PRC1 appears to be absent in fungi, PRC2, first identified in Drosophila as an important developmental regulator, is present in many eukaryotes [2,[15][16][17]. In the model filamentous fungus Neurospora crassa, three core components of PRC2 (NcSet7, NcSu(z) 12 and NcEed) are required for normal H3K27me3 deposition, and 130 genes of total 774 H3K27me3-marked genes are upregulated~7.5-fold in the absence of H3K27me3 [18].…”

Section: Introductionmentioning

confidence: 99%

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

2021

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Transcriptional dynamic in response to environmental and developmental cues are fundamental to biology, yet many mechanistic aspects are poorly understood. One such example is fungal plant pathogens, which use secreted proteins and small molecules, termed effectors, to suppress host immunity and promote colonization. Effectors are highly expressed in planta but remain transcriptionally repressed ex planta, but our mechanistic understanding of these transcriptional dynamics remains limited. We tested the hypothesis that repressive histone modification at H3-Lys27 underlies transcriptional silencing ex planta, and that exchange for an active chemical modification contributes to transcription of in planta induced genes. Using genetics, chromatin immunoprecipitation and sequencing and RNA-sequencing, we determined that H3K27me3 provides significant local transcriptional repression. We detail how regions that lose H3K27me3 gain H3K27ac, and these changes are associated with increased transcription. Importantly, we observed that many in planta induced genes were marked by H3K27me3 during axenic growth, and detail how altered H3K27 modification influences transcription. ChIP-qPCR during in planta growth suggests that H3K27 modifications are generally stable, but can undergo dynamics at specific genomic locations. Our results support the hypothesis that dynamic histone modifications at H3K27 contributes to fungal genome regulation and specifically contributes to regulation of genes important during host infection.

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Section: Introductionmentioning

confidence: 99%

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

2021

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“…Polycomb silencing has been extensively studied in multicellular organisms, which is conserved from Drosophila to mammals and higher plants, as well as in the fungi kingdom (Margueron and Reinberg, 2011, Ridenour et al, 2020, Wiles and Selker, 2017, Schuettengruber et al, 2017. The core subunits Kmt6, Suz12 and Eed are necessary for H3K27me3 modification and transcriptional silencing (Wiles and Selker, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…However, the role of P55, the additional subunit of PRC2, remains obscure in fungi. In F. graminearum, the homolog of subunit p55 is not involved in H3K27me3 modification (Ridenour et al, 2020). In N. crassa, P55 (NPF) is critical for H3K27me3 in a region-dependent manner (Jamieson et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Polycomb-group genes were first identified in Hox regulation in Drosohpila and are usually assembled with Polycomb repressive complex 1(PRC1) and PRC2 (Blackledge et al, 2015, Ridenour et al, 2020. To identify the candidate PRC1 and other PRC2 subunits in M. oryzae, BLASTp was used to search for the orthologs from M. oryzae 70-15 genomes (taxid: 242507) with the query sequences from Neurospora crassa, Arabidopsis thaliana, and Drosophila melanogaster (Table S1).…”

Section: Kmt6 As Well As Other Prc2 Subunits Is Indispensable For H3k27me3 Modification In M Oryzaementioning

confidence: 99%

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Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression ofeffectorsand regulate pathogenicity inMagnaporthe oryzae

Qiu

Shi

et al. 2021

Preprint

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The strict suppression and reprogramming of gene expression are necessary at different development stages and/or in response to environment stimuli in eukaryotes. In Rice Magnaporthe oryzae pathosystem, effectors from pathogen are kept transcriptionally silenced in the vegetative growth stage and are highly expressed during invasive growth stage to adapt to the host environment. However, the mechanism of how such effectors are stably repressed in the vegetative stage and its roles during rice blast infection remain unclear so far. Here, we showed that all subunits of Polycomb Repressive Complex 2 are required for such repression by direct H3K27me3 occupancy and pathogenic process in M. oryzae. Suppression of polycomb-mediated H3K27me3 causes an improper induction of effectors during vegetative growth thus simulating a host environment. Notably, the addition subunit P55 not only acts as the bridge to connect with core subunits to form a complex in M. oryzae, but also recruits Sin3 histone deacetylase complex to prompt H3K27me3 occupancy for stable maintenance of transcriptional silencing of the target genes in the absence of PRC1. In contrast, during invasive growth stage, the repressed state of effectors chromatin can be partially erased during pathogenic development resulting in transcriptional activation of effectors therein. Overall, Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression of effectors, which act as molecular switch to memorize the host environment from vegetative to invasive growth, thus contributing to the infection of rice blast.

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“…However, as global depletion of a histone modification can result in pleiotropic effects, such as improper localization of other histone modifications or altered development (Tian & Chen, 2001; Fan et al ., 2017), it is difficult to infer transcriptional control mechanisms used for natural gene regulation from these genetic perturbation experiments. Therefore, additional research is needed to directly test the hypothesis that heterochromatin-associated histone modifications directly regulate transcription either through their dynamics, or their action to form or recruit transcriptional complexes (Galazka & Freitag, 2014; Seidl et al ., 2016; Ridenour et al ., 2020).…”

Section: Introductionmentioning

confidence: 99%

Local rather than global H3K27me3 dynamics associates with differential gene expression inVerticillium dahliae

Kramer

Seidl

Thomma

et al. 2021

Preprint

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Differential growth conditions typically trigger global transcriptional responses in filamentous fungi. Such fungal responses to environmental cues involve epigenetic regulation, including chemical histone modifications. It has been proposed that conditionally expressed genes, such as those that encode secondary metabolites but also effectors in pathogenic species, are often associated with a specific histone modification, lysine27 methylation of H3 (H3K27me3). However, thus far no analyses on the global H3K27me3 profiles have been reported under differential growth conditions in order to assess if H3K27me3 dynamics governs differential transcriptional. Using ChIP- and RNA-sequencing data from the plant pathogenic fungus Verticillium dahliae grown on three in vitro cultivation media, we now show that a substantial number of the identified H3K27me3 domains globally display stable profiles among these growth conditions. However, we do observe local quantitative differences in H3K27me3 ChIP-seq signal that associate with differentially transcribed genes between media. Comparing the in vitro results to expression during plant infection suggests that in planta induced genes require chromatin remodelling to achieve expression. Overall, our results demonstrate that although some loci display H3K27me3 dynamics that can contribute to transcriptional variation, other loci do not show such dependence. Thus, we conclude that while H3K27me3 is required for transcriptional repression, it is not a conditionally responsive global regulator of differential transcription. We propose that the H3K27me3 domains that do not undergo dynamic methylation may contribute to transcription through other mechanisms or may serve additional genomic regulatory functions.IMPORTANCEIn many organisms, including filamentous fungi, epigenetic mechanisms that involve chemical and physical modifications of DNA without changing the genetic sequence have been implicated in transcriptional responses upon developmental or environmental cues. In fungi, facultative heterochromatin that can de-condense to allow transcription in response to developmental changes or to environmental stimuli is characterized by tri-methylation of lysine 27 on histone H3 (H3K27me3), and H3K27me3 has been implicated in transcriptional regulation although precise mechanisms and functions remain enigmatic. Based on ChIP- and RNA-sequencing data, we show for the soil-borne broad host range vascular wilt plant pathogenic fungus Verticillium dahliae that although some loci display H3K27me3 dynamics that can contribute to transcriptional variation, other loci do not show such dependence. Thus, although we recognize that H3K27me3 is required for transcriptional repression, we also conclude that this mark is not a conditionally responsive global regulator of differential transcription upon responses to environmental cues.

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Polycomb Repression without Bristles: Facultative Heterochromatin and Genome Stability in Fungi

Cited by 30 publications

References 173 publications

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression ofeffectorsand regulate pathogenicity inMagnaporthe oryzae

Local rather than global H3K27me3 dynamics associates with differential gene expression inVerticillium dahliae

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