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Polycomb-dependent differential chromatin compartmentalization determines gene coregulation in Arabidopsis
Genome Research ( IF 6.2 ) Pub Date : 2021-07-01 , DOI: 10.1101/gr.273771.120
Ying Huang 1 , Sanchari Sicar 1 , Juan S Ramirez-Prado 1 , Deborah Manza-Mianza 1 , Javier Antunez-Sanchez 2 , Rim Brik-Chaouche 1 , Natalia Y Rodriguez-Granados 1 , Jing An 1 , Catherine Bergounioux 1 , Magdy M Mahfouz 3 , Heribert Hirt 1, 3 , Martin Crespi 1 , Lorenzo Concia 1, 4 , Fredy Barneche 4 , Simon Amiard 5 , Aline V Probst 5 , Jose Gutierrez-Marcos 2 , Federico Ariel 6 , Cécile Raynaud 1 , David Latrasse 1 , Moussa Benhamed 1, 7, 8
Affiliation  

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.

中文翻译:

多梳依赖的差异染色质区室化决定拟南芥中的基因共调控

在动物中,远处 H3K27me3 标记的 Polycomb 靶标可以建立物理相互作用,形成抑制性染色质中心。在植物中,越来越多的证据表明 H3K27me3 直接或间接调节染色质相互作用,尽管这种组蛋白修饰如何调节 3D 染色质结构仍然难以捉摸。为了破译 H3K27me3 动态沉积对拟南芥核相互作用组的影响,我们结合了遗传学、转录组学和几种 3D 表观基因组方法。通过分析组蛋白 H3K27 甲基化或去甲基化缺陷的突变体,我们发现了这种染色质标记在短程和以前未被注意到的长程染色质环形成中的关键作用。我们发现 H3K27me3 水平的降低导致 Polycomb 相关抑制域内相互作用的减少。H3K27 甲基转移酶clf突变体中 H3K27me3 水平较低的区域与 H3K9ac 标记的区域建立了新的相互作用,H3K9ac 是一种与活性转录相关的组蛋白修饰,表明 H3K27me3 水平的降低会诱导染色质结构的整体重新配置。总而言之,我们的结果表明,3D 基因组组织与控制染色质相互作用的可逆组蛋白修饰紧密相关。因此,核组织动力学决定了植物发育过程中的转录重编程,并将 H3K27me3 作为远距离基因共调控的关键特征。
更新日期:2021-07-01
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