Evolutionarily ancient BAH-PHD protein mediates Polycomb silencing

Wiles, Elizabeth T.; McNaught, Kevin J; Silva, Saumya M. De; Kaur, Gurmeet; Selker, Jeanne M. L.; Ormsby, Tereza; Aravind, L.; Musselman, Catherine A.; Selker, Eric U.

doi:10.1101/868117

Cited by 8 publications

(41 citation statements)

References 85 publications

(75 reference statements)

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“…We recently described a genetic scheme to select for mutants defective in Polycomb silencing in N. crassa (12). Briefly, a wild-type strain bearing two antibiotic-resistance genes repressed by H3K27 methylation, hph and nat-1 , is subjected to ultraviolet radiation and mutants resistant to both Hygromycin B and Nourseothricin are isolated.…”

Section: Resultsmentioning

confidence: 99%

“…5A) (10). We also immunopurified SUZ12-3xFLAG and a negative control (3xFLAG-EPR-1) (12), and analyzed their copurifying proteins by mass spectrometry. In addition, we re-examined previously collected mass spectrometry data from a 3xFLAG-EED purification (10).…”

Section: Resultsmentioning

confidence: 99%

“…All N. crassa strains used in this study are listed in Table S1 (supplemental material). Preparation of media and growth conditions for experiments were carried out as previously described (12).…”

Section: Methodsmentioning

confidence: 99%

“…Conidia from strain N6279 were mutagenized with ultraviolet light and challenged with Hygromycin B and Nourseothricin to select for antibiotic-resistant colonies as previously described (12). Primary mutants were rendered homokaryotic by crossing to strain N3756.…”

Section: Methodsmentioning

confidence: 99%

“…This was performed as previously described (12). Briefly, antibiotic-resistant, homokaryotic mutants were crossed to a “Mauriceville” wild-type strain (13) and antibiotic-resistant progeny were pooled for whole genome sequencing.…”

Section: Methodsmentioning

confidence: 99%

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Identification of a PRC2 accessory subunit required for subtelomeric H3K27 methylation in Neurospora

McNaught

Wiles

Selker

2020

Preprint

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Polycomb repressive complex 2 (PRC2) catalyzes methylation of histone H3 lysine 27 (H3K27) in genomic regions of most eukaryotes and is critical for maintenance of the associated transcriptional repression. However, the mechanisms that shape the distribution of H3K27 methylation, such as recruitment of PRC2 to chromatin and/or stimulation of PRC2 activity, are unclear. Here, using a forward genetic approach in the model organism Neurospora crassa, we identified two alleles of a gene, NCU04278, encoding an unknown PRC2 accessory subunit (PAS). Loss of PAS resulted in losses of H3K27 methylation concentrated near the chromosome ends and derepression of a subset of associated subtelomeric genes. Immunoprecipitation followed by mass spectrometry confirmed reciprocal interactions between PAS and known PRC2 subunits, and sequence similarity searches demonstrated that PAS is not unique to N. crassa. PAS homologs likely influence the distribution of H3K27 methylation, and underlying gene repression, in a variety of fungal lineages.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Identification of a PRC2 accessory subunit required for subtelomeric H3K27 methylation in Neurospora

McNaught

Wiles

Selker

2020

Preprint

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A conserved BAH module within mammalian BAHD1 connects H3K27me3 to Polycomb gene silencing

Fan

Guo

Tsai

et al. 2021

Preprint

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Trimethylation of histone H3 lysine 27 (H3K27me3) is important for gene silencing and imprinting, (epi)genome organization and organismal development. In a prevalent model, the functional readout of H3K27me3 in mammalian cells is achieved through the H3K27me3-recognizing chromodomain harbored within the chromobox (CBX) component of canonical Polycomb repressive complex 1 (cPRC1), which induces chromatin compaction and gene repression. Here, we report that binding of H3K27me3 by a Bromo Adjacent Homology (BAH) domain harbored within BAH domain-containing protein 1 (BAHD1) is required for overall BAHD1 targeting to chromatin and for optimal repression of the H3K27me3-demarcated genes in mammalian cells. Disruption of direct interaction between BAHD1BAH and H3K27me3 by point mutagenesis leads to chromatin remodeling, notably, increased histone acetylation, at its Polycomb gene targets. Mice carrying an H3K27me3-interaction-defective mutation of Bahd1BAH causes marked embryonic lethality, showing a requirement of this pathway for normal development. Altogether, this work demonstrates an H3K27me3-initiated signaling cascade that operates through a conserved BAH 'reader' module within BAHD1 in mammals.

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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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Evolutionarily ancient BAH-PHD protein mediates Polycomb silencing

Cited by 8 publications

References 85 publications

Identification of a PRC2 accessory subunit required for subtelomeric H3K27 methylation in Neurospora

Identification of a PRC2 accessory subunit required for subtelomeric H3K27 methylation in Neurospora

A conserved BAH module within mammalian BAHD1 connects H3K27me3 to Polycomb gene silencing

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

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