Polycomb-dependent differential chromatin compartmentalization determines gene coregulation in Arabidopsis
- Ying Huang1,
- Sanchari Sircar1,
- Juan Sebastian Ramirez-Prado1,
- Deborah Manza-Mianza1,
- Javier Antunez-Sanchez2,
- Rim brik-chaouche1,
- Natalia Rodriguez-Granados1,
- Jing An1,
- Catherine Bergounioux1,
- Magdy Mahfouz3,
- Heribert Hirt3,
- Martin Crespi1,
- Lorenzo Concia1,
- Fredy Barnech4,
- Simon Amiard5,
- Aline V Probst5,
- Jose Gutierrez-Marcos2,
- Federico Ariel6,
- Cecile Raynaud1,
- David Latrasse1 and
- Moussa Benhamed7,8
- 1 Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2);
- 2 University of Warwick;
- 3 King Abdullah University of Science and Technology;
- 4 Institut de Biologie de l'Ecole Normale Supérieure (IBENS), ENS, CNRS;
- 5 GReD, Université Clermont Auvergne, CNRS, INSERM;
- 6 Instituto de Agrobiotecnología del Litoral, CONICET, Universidad Nacional del Litoral;
- 7 Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Institut Universitaire de France
Abstract
In animals, distant H3K27me3-marked Polycomb targets can establish physical interactions forming repressive chromatin hubs. In plants, growing evidence suggests that H3K27me3 act 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 alternative 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 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, thus 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.
- Received November 6, 2020.
- Accepted May 20, 2021.
- Published by Cold Spring Harbor Laboratory Press
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