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The genome-wide, multi-layered architecture of chromosome pairing in early Drosophila embryos

Jelena Erceg, Jumana AlHaj Abed, Anton Goloborodko, Bryan R. Lajoie, Geoffrey Fudenberg, Nezar Abdennur, Maxim Imakaev, Ruth B. McCole, Son C. Nguyen, Wren Saylor, Eric F. Joyce, T. Niroshini Senaratne, Mohammed A. Hannan, Guy Nir, Job Dekker, Leonid A. Mirny, Chao-ting Wu
doi: https://doi.org/10.1101/443028
Jelena Erceg
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
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Jumana AlHaj Abed
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
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Anton Goloborodko
2Department of Physics, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA
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Bryan R. Lajoie
3Howard Hughes Medical Institute and Program in Systems Biology, Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605-0103, USA
4Illumina, San Diego, CA, USA
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Geoffrey Fudenberg
2Department of Physics, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA
5Gladstone Institutes of Data Science and Biotechnology, San Francisco, CA 94158, USA
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Nezar Abdennur
2Department of Physics, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA
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Maxim Imakaev
2Department of Physics, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA
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Ruth B. McCole
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
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Son C. Nguyen
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
6Department of Genetics, Penn Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6145, USA
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Wren Saylor
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
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Eric F. Joyce
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
6Department of Genetics, Penn Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6145, USA
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T. Niroshini Senaratne
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
7Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA
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Mohammed A. Hannan
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
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Guy Nir
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
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Job Dekker
3Howard Hughes Medical Institute and Program in Systems Biology, Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605-0103, USA
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Leonid A. Mirny
2Department of Physics, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA
8Institute for Medical Engineering and Science, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA
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  • For correspondence: leonid@mit.edu twu@genetics.med.harvard.edu
Chao-ting Wu
1Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
9Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA
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  • For correspondence: leonid@mit.edu twu@genetics.med.harvard.edu
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Abstract

Genome organization involves cis and trans chromosomal interactions, both implicated in gene regulation, development, and disease. Here, we focused on trans interactions in Drosophila, where homologous chromosomes are paired in somatic cells from embryogenesis through adulthood. We first addressed the long-standing question of whether pairing extends genome-wide and, to this end, developed a haplotype-resolved Hi-C approach that uses a new strategy to minimize homolog misassignment and thus robustly distinguish trans-homolog from cis contacts. This approach revealed striking genome-wide pairing in Drosophila embryos. Moreover, we discovered pairing to be surprisingly structured, with trans-homolog domains and interaction peaks, many coinciding with the positions of analogous cis features. We also found a significant correlation between pairing and the chromatin accessibility mediated by the pioneer factor Zelda. Our findings reveal a complex, highly structured organization underlying homolog pairing, first discovered more than a century ago.

One Sentence Summary A robust approach for haplotype-resolved Hi-C reveals highly-structured homolog pairing in early stage Drosophila embryos.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted October 17, 2018.
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The genome-wide, multi-layered architecture of chromosome pairing in early Drosophila embryos
Jelena Erceg, Jumana AlHaj Abed, Anton Goloborodko, Bryan R. Lajoie, Geoffrey Fudenberg, Nezar Abdennur, Maxim Imakaev, Ruth B. McCole, Son C. Nguyen, Wren Saylor, Eric F. Joyce, T. Niroshini Senaratne, Mohammed A. Hannan, Guy Nir, Job Dekker, Leonid A. Mirny, Chao-ting Wu
bioRxiv 443028; doi: https://doi.org/10.1101/443028
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The genome-wide, multi-layered architecture of chromosome pairing in early Drosophila embryos
Jelena Erceg, Jumana AlHaj Abed, Anton Goloborodko, Bryan R. Lajoie, Geoffrey Fudenberg, Nezar Abdennur, Maxim Imakaev, Ruth B. McCole, Son C. Nguyen, Wren Saylor, Eric F. Joyce, T. Niroshini Senaratne, Mohammed A. Hannan, Guy Nir, Job Dekker, Leonid A. Mirny, Chao-ting Wu
bioRxiv 443028; doi: https://doi.org/10.1101/443028

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