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

Author

Listed:
  • Lucía Álvarez-González

    (Universitat Autònoma de Barcelona
    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
    Universitat Autònoma de Barcelona)

  • Laia Marín-Gual

    (Universitat Autònoma de Barcelona
    Universitat Autònoma de Barcelona)

  • Albert Gubern

    (Universitat Autònoma de Barcelona)

  • Covadonga Vara

    (Universitat Autònoma de Barcelona
    Universitat Autònoma de Barcelona)

  • Andreu Paytuví-Gallart

    (Universitat Autònoma de Barcelona
    Universitat Autònoma de Barcelona
    Sequentia Biotech)

  • Marcus Buschbeck

    (Josep Carreras Leukaemia Research Institute (IJC), Campus ICO-GTP-UAB
    Germans Trias i Pujol Research Institute (PMPPC-IGTP))

  • Peter J. I. Ellis

    (University of Kent)

  • Marta Farré

    (University of Kent)

  • Aurora Ruiz-Herrera

    (Universitat Autònoma de Barcelona
    Universitat Autònoma de Barcelona)

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.

Suggested Citation

  • Lucía Álvarez-González & Frances Burden & Dadakhalandar Doddamani & Roberto Malinverni & Emma Leach & Cristina Marín-García & Laia Marín-Gual & Albert Gubern & Covadonga Vara & Andreu Paytuví-Gallart , 2022. "3D chromatin remodelling in the germ line modulates genome evolutionary plasticity," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30296-6
    DOI: 10.1038/s41467-022-30296-6
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    References listed on IDEAS

    as
    1. Jacob T. Sanders & Trevor F. Freeman & Yang Xu & Rosela Golloshi & Mary A. Stallard & Ashtyn M. Hill & Rebeca San Martin & Adayabalam S. Balajee & Rachel Patton McCord, 2020. "Radiation-induced DNA damage and repair effects on 3D genome organization," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    2. Covadonga Vara & Andreu Paytuví-Gallart & Yasmina Cuartero & Lucía Álvarez-González & Laia Marín-Gual & Francisca Garcia & Beatriu Florit-Sabater & Laia Capilla & Rosa Ana Sanchéz-Guillén & Zaida Sarr, 2021. "The impact of chromosomal fusions on 3D genome folding and recombination in the germ line," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Kevin Brick & Sarah Thibault-Sennett & Fatima Smagulova & Kwan-Wood G. Lam & Yongmei Pu & Florencia Pratto & R. Daniel Camerini-Otero & Galina V. Petukhova, 2018. "Extensive sex differences at the initiation of genetic recombination," Nature, Nature, vol. 561(7723), pages 338-342, September.
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