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Pericentromeric heterochromatin is hierarchically organized and spatially contacts H3K9me2/3 islands located in euchromatic genome

Yuh Chwen G. Lee, Yuki Ogiyama, Nuno M. C. Martins, Brian J. Beliveau, David Acevedo, C.-ting Wu, Giacomo Cavalli, Gary H. Karpen
doi: https://doi.org/10.1101/525873
Yuh Chwen G. Lee
1Department of Molecular and Cell Biology, UC Berkeley and BSE Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Yuki Ogiyama
2Institute of Human Genetics, CNRS, Montpellier, France
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Nuno M. C. Martins
3Department of Genetics, Harvard Medical School, Boston, MA, USA
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Brian J. Beliveau
4Department of Genome Sciences, University of Washington, Seattle, WA, USA
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David Acevedo
1Department of Molecular and Cell Biology, UC Berkeley and BSE Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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C.-ting Wu
3Department of Genetics, Harvard Medical School, Boston, MA, USA
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Giacomo Cavalli
2Institute of Human Genetics, CNRS, Montpellier, France
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Gary H. Karpen
1Department of Molecular and Cell Biology, UC Berkeley and BSE Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Abstract

Membraneless pericentromeric heterochromatin (PCH) domains play vital roles in chromosome dynamics and genome stability. However, our current understanding of 3D genome organization does not include PCH domains because of technical challenges associated with repetitive sequences enriched in PCH genomic regions. We investigated the 3D architecture of Drosophila melanogaster PCH domains and their spatial associations with euchromatic genome by developing a novel analysis method that incorporates genome-wide Hi-C reads originating from PCH DNA. Combined with cytogenetic analysis, we reveal a hierarchical organization of the PCH domains into distinct “territories,” in which “intra-arm” interactions are the most prevalent, followed by 3D contacts between specific PCH regions on different chromosomes. Strikingly, H3K9me2/3-enriched regions embedded in euchromatic genome show prevalent 3D interactions with the PCH domain. These spatial contacts require H3K9me2/3 enrichment, are likely mediated by liquid-liquid phase separation, and influence organismal fitness. Our findings have important implications for how PCH architecture influences the function and evolution of both repetitive heterochromatin and the gene-rich euchromatin.

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Posted January 21, 2019.
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Pericentromeric heterochromatin is hierarchically organized and spatially contacts H3K9me2/3 islands located in euchromatic genome
Yuh Chwen G. Lee, Yuki Ogiyama, Nuno M. C. Martins, Brian J. Beliveau, David Acevedo, C.-ting Wu, Giacomo Cavalli, Gary H. Karpen
bioRxiv 525873; doi: https://doi.org/10.1101/525873
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Pericentromeric heterochromatin is hierarchically organized and spatially contacts H3K9me2/3 islands located in euchromatic genome
Yuh Chwen G. Lee, Yuki Ogiyama, Nuno M. C. Martins, Brian J. Beliveau, David Acevedo, C.-ting Wu, Giacomo Cavalli, Gary H. Karpen
bioRxiv 525873; doi: https://doi.org/10.1101/525873

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