3D chromatin remodelling in the germ line modulates genome evolutionary plasticity

Lucía Álvarez-González, Frances Burden, Dadakhalandar Doddamani, Roberto Malinverni, Emma Leach, Cristina Marín-García, Laia Marín-Gual, Albert Gubern, Covadonga Vara, Andreu Paytuví-Gallart, Marcus Buschbeck, Peter J. I. Ellis (), Marta Farré () and Aurora Ruiz-Herrera ()
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Lucía Álvarez-González: Universitat Autònoma de Barcelona
Frances Burden: University of Kent
Dadakhalandar Doddamani: University of Kent
Roberto Malinverni: Josep Carreras Leukaemia Research Institute (IJC), Campus ICO-GTP-UAB
Emma Leach: University of Kent
Cristina Marín-García: Universitat Autònoma de Barcelona
Laia Marín-Gual: Universitat Autònoma de Barcelona
Albert Gubern: Universitat Autònoma de Barcelona
Covadonga Vara: Universitat Autònoma de Barcelona
Andreu Paytuví-Gallart: Universitat Autònoma de Barcelona
Marcus Buschbeck: Josep Carreras Leukaemia Research Institute (IJC), Campus ICO-GTP-UAB
Peter J. I. Ellis: University of Kent
Marta Farré: University of Kent
Aurora Ruiz-Herrera: Universitat Autònoma de Barcelona

Nature Communications, 2022, vol. 13, issue 1, 1-15

Abstract: Abstract Chromosome folding has profound impacts on gene regulation, whose evolutionary consequences are far from being understood. Here we explore the relationship between 3D chromatin remodelling in mouse germ cells and evolutionary changes in genome structure. Using a comprehensive integrative computational analysis, we (i) reconstruct seven ancestral rodent genomes analysing whole-genome sequences of 14 species representatives of the major phylogroups, (ii) detect lineage-specific chromosome rearrangements and (iii) identify the dynamics of the structural and epigenetic properties of evolutionary breakpoint regions (EBRs) throughout mouse spermatogenesis. Our results show that EBRs are devoid of programmed meiotic DNA double-strand breaks (DSBs) and meiotic cohesins in primary spermatocytes, but are associated in post-meiotic cells with sites of DNA damage and functional long-range interaction regions that recapitulate ancestral chromosomal configurations. Overall, we propose a model that integrates evolutionary genome reshuffling with DNA damage response mechanisms and the dynamic spatial genome organisation of germ cells.

Date: 2022
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DOI: 10.1038/s41467-022-30296-6

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