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Polycomb-dependent differential chromatin compartmentalization determines gene coregulation in Arabidopsis.

ABSTRACT: In animals, distant H3K27me3-marked Polycomb targets can establish physical interactions forming repressive chromatin hubs. In plants, growing evidence suggests that H3K27me3 acts directly or indirectly to regulate chromatin interactions, although how this histone modification modulates 3D chromatin architecture remains elusive. To decipher the impact of the dynamic deposition of H3K27me3 on the Arabidopsis thaliana nuclear interactome, we combined genetics, transcriptomics, and several 3D epigenomic approaches. By analyzing mutants defective for histone H3K27 methylation or demethylation, we uncovered the crucial role of this chromatin mark in short- and previously unnoticed long-range chromatin loop formation. We found that a reduction in H3K27me3 levels led to a decrease in the interactions within Polycomb-associated repressive domains. Regions with lower H3K27me3 levels in the H3K27 methyltransferase clf mutant established new interactions with regions marked with H3K9ac, a histone modification associated with active transcription, indicating that a reduction in H3K27me3 levels induces a global reconfiguration of chromatin architecture. Altogether, our results reveal that the 3D genome organization is tightly linked to reversible histone modifications that govern chromatin interactions. Consequently, nuclear organization dynamics shapes the transcriptional reprogramming during plant development and places H3K27me3 as a key feature in the coregulation of distant genes.

SUBMITTER: Huang Y

PROVIDER: S-EPMC8256866 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Polycomb-dependent differential chromatin compartmentalization determines gene co-regulation in Arabidopsis

Project description:Previous studies in animals have shown that polycomb targets marked with H3K27me3 can establish interactions between them, forming a repressive chromatin hub (Lanzuolo et al., 2007; Cheutin and Cavalli, 2014). In plants few studies suggested that H3K27me3 may act directly or indirectly to regulate the interactivity of polycomb marked genes. However, several aspects of the molecular function of the H3K27me3 histone modification on the 3D chromatin architecture remained obscure. To decipher the impact of H3K27me3 levels on loop formation, we combined genetics, 3D epigenomics and transcriptomic approaches. By using the ref6 mutant, defective for a histone demethylase, that displays ectopic accumulation of H3K27me3, we demonstrated that H3K27me3 is important to trigger chromatin loop formation. Reciprocally, using clf mutant, a histone methyltransferase mutant that displays a strong reduction of H3K27me3 we found that a reduction of the H3K27me3 leads to the decrease of interactions inside the polycomb repressive domain. Surprisingly, we observed that regions losing H3K27me3 in clf establish new interactions with regions marked with the H3K9ac active histone modification, showing that a reduction in H3K27me3 levels induces a global reconfiguration of chromatin architecture. Altogether our results demonstrate that the 3D organization of the genome is tightly linked to histone modifications that trigger the formation of chromatin domains associated with gene co-regulation, thereby allowing proper plant development and in which H3K27me3 is a key regulator of chromatin topology at global and local scales.

2021-04-29 | GSE155502 | GEO

Polycomb-dependent differential chromatin compartmentalization determines gene co-regulation in Arabidopsis

Project description:Polycomb-dependent differential chromatin compartmentalization determines gene co-regulation in Arabidopsis

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Polycomb-mediated gene silencing in Arabidopsis thaliana.

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The Arabidopsis SWI2/SNF2 chromatin Remodeler BRAHMA regulates polycomb function during vegetative development and directly activates the flowering repressor gene SVP.

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Chromatin localization of nucleophosmin determines the sorting and compartmentalization of ribosome biogenesis

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2023-03-01 | GSE156203 | GEO

Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics.

Project description:Transcription factor cistromes are highly cell-type specific. Chromatin accessibility, histone modifications, and nucleosome occupancy have all been found to play a role in defining these binding locations. Here, we show that hormone-induced DNase I hypersensitivity changes (?DHS) are highly predictive of androgen receptor (AR) and estrogen receptor 1 (ESR1) binding in prostate cancer and breast cancer cells, respectively. While chromatin structure prior to receptor binding and nucleosome occupancy after binding are strikingly different for ESR1 and AR, ?DHS is highly predictive for both. AR binding is associated with changes in both local nucleosome occupancy and DNase I hypersensitivity. In contrast, while global ESR1 binding is unrelated to changes in nucleosome occupancy, DNase I hypersensitivity dynamics are also predictive of the ESR1 cistrome. These findings suggest that AR and ESR1 have distinct modes of interaction with chromatin and that DNase I hypersensitivity dynamics provides a general approach for predicting cell-type specific cistromes.

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Overexpression of AtBMI1C, a polycomb group protein gene, accelerates flowering in Arabidopsis.

Project description:Polycomb group protein (PcG)-mediated gene silencing is emerging as an essential developmental regulatory mechanism in eukaryotic organisms. PcGs inactivate or maintain the silenced state of their target chromatin by forming complexes, including Polycomb Repressive Complex 1 (PRC1) and 2 (PRC2). Three PRC2 complexes have been identified and characterized in Arabidopsis; of these, the EMF and VRN complexes suppress flowering by catalyzing the trimethylation of lysine 27 on histone H3 of FLOWER LOCUS T (FT) and FLOWER LOCUS C (FLC). However, little is known about the role of PRC1 in regulating the floral transition, although AtRING1A, AtRING1B, AtBMI1A, and AtBMI1B are believed to regulate shoot apical meristem and embryonic development as components of PRC1. Moreover, among the five RING finger PcGs in the Arabidopsis genome, four have been characterized. Here, we report that the fifth, AtBMI1C, is a novel, ubiquitously expressed nuclear PcG protein and part of PRC1, which is evolutionarily conserved with Psc and BMI1. Overexpression of AtBMI1C caused increased H2A monoubiquitination and flowering defects in Arabidopsis. Both the suppression of FLC and activation of FT were observed in AtBMI1C-overexpressing lines, resulting in early flowering. No change in the H3K27me3 level in FLC chromatin was detected in an AtBMI1C-overexpressing line. Our results suggest that AtBMI1C participates in flowering time control by regulating the expression of FLC; moreover, the repression of FLC by AtBMI1C is not due to the activity of PRC2. Instead, it is likely the result of PRC1 activity, into which AtBMI1C is integrated.

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Project description:Patterned expression of many developmental genes is specified by transcription factor gene expression, but is thought to be refined by chromatin-mediated repression. Regulatory DNA sequences called Polycomb Response Elements (PREs) are required to repress some developmental target genes, and are widespread in genomes, suggesting that they broadly affect developmental programs. While PREs in transgenes can nucleate trimethylation on lysine 27 of the histone H3 tail (H3K27me3), none have been demonstrated to be necessary at endogenous chromatin domains. This failure is thought to be due to the fact that most endogenous H3K27me3 domains contain many PREs, and individual PREs may be redundant. In contrast to these ideas, we show here that PREs near the wing selector gene vestigial have distinctive roles at their endogenous locus, even though both PREs are repressors in transgenes. First, a PRE near the promoter is required for vestigial activation and not for repression. Second, only the distal PRE contributes to H3K27me3, but even removal of both PREs does not eliminate H3K27me3 across the vestigial domain. Thus, endogenous chromatin domains appear to be intrinsically marked by H3K27me3, and PREs appear required to enhance this chromatin modification to high levels at inactive genes.

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