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 () and C.-ting Wu ()
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Jelena Erceg: Harvard Medical School
Jumana AlHaj Abed: Harvard Medical School
Anton Goloborodko: Massachusetts Institute of Technology (MIT)
Bryan R. Lajoie: University of Massachusetts Medical School
Geoffrey Fudenberg: Massachusetts Institute of Technology (MIT)
Nezar Abdennur: Massachusetts Institute of Technology (MIT)
Maxim Imakaev: Massachusetts Institute of Technology (MIT)
Ruth B. McCole: Harvard Medical School
Son C. Nguyen: Harvard Medical School
Wren Saylor: Harvard Medical School
Eric F. Joyce: Harvard Medical School
T. Niroshini Senaratne: Harvard Medical School
Mohammed A. Hannan: Harvard Medical School
Guy Nir: Harvard Medical School
Job Dekker: University of Massachusetts Medical School
Leonid A. Mirny: Massachusetts Institute of Technology (MIT)
C.-ting Wu: Harvard Medical School

Nature Communications, 2019, vol. 10, issue 1, 1-13

Abstract: Abstract Genome organization involves cis and trans chromosomal interactions, both implicated in gene regulation, development, and disease. Here, we focus on trans interactions in Drosophila, where homologous chromosomes are paired in somatic cells from embryogenesis through adulthood. We first address long-standing questions regarding the structure of embryonic homolog pairing and, to this end, develop a haplotype-resolved Hi-C approach to minimize homolog misassignment and thus robustly distinguish trans-homolog from cis contacts. This computational approach, which we call Ohm, reveals pairing to be surprisingly structured genome-wide, with trans-homolog domains, compartments, and interaction peaks, many coinciding with analogous cis features. We also find a significant genome-wide correlation between pairing, transcription during zygotic genome activation, and binding of the pioneer factor Zelda. Our findings reveal a complex, highly structured organization underlying homolog pairing, first discovered a century ago in Drosophila. Finally, we demonstrate the versatility of our haplotype-resolved approach by applying it to mammalian embryos.

Date: 2019
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DOI: 10.1038/s41467-019-12211-8

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