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Biophysical ordering transitions underlie genome 3D re-organization during cricket spermiogenesis

Author

Listed:
  • Guillermo A. Orsi

    (University Grenoble Alpes, Inserm U 1209, CNRS UMR 5309)

  • Maxime M. C. Tortora

    (Université Claude Bernard Lyon 1
    University of Southern California)

  • Béatrice Horard

    (Université Claude Bernard Lyon 1)

  • Dominique Baas

    (Université Claude Bernard Lyon 1)

  • Jean-Philippe Kleman

    (UMR5075, University Grenoble Alpes, CEA, CNRS)

  • Jonas Bucevičius

    (Max Planck Institute for Multidisciplinary Sciences)

  • Gražvydas Lukinavičius

    (Max Planck Institute for Multidisciplinary Sciences)

  • Daniel Jost

    (Université Claude Bernard Lyon 1)

  • Benjamin Loppin

    (Université Claude Bernard Lyon 1)

Abstract

Spermiogenesis is a radical process of differentiation whereby sperm cells acquire a compact and specialized morphology to cope with the constraints of sexual reproduction while preserving their main cargo, an intact copy of the paternal genome. In animals, this often involves the replacement of most histones by sperm-specific nuclear basic proteins (SNBPs). Yet, how the SNBP-structured genome achieves compaction and accommodates shaping remain largely unknown. Here, we exploit confocal, electron and super-resolution microscopy, coupled with polymer modeling to identify the higher-order architecture of sperm chromatin in the needle-shaped nucleus of the emerging model cricket Gryllus bimaculatus. Accompanying spermatid differentiation, the SNBP-based genome is strikingly reorganized as ~25nm-thick fibers orderly coiled along the elongated nucleus axis. This chromatin spool is further found to achieve large-scale helical twisting in the final stages of spermiogenesis, favoring its ultracompaction. We reveal that these dramatic transitions may be recapitulated by a surprisingly simple biophysical principle based on a nucleated rigidification of chromatin linked to the histone-to-SNBP transition within a confined nuclear space. Our work highlights a unique, liquid crystal-like mode of higher-order genome organization in ultracompact cricket sperm, and establishes a multidisciplinary methodological framework to explore the diversity of non-canonical modes of DNA organization.

Suggested Citation

  • Guillermo A. Orsi & Maxime M. C. Tortora & Béatrice Horard & Dominique Baas & Jean-Philippe Kleman & Jonas Bucevičius & Gražvydas Lukinavičius & Daniel Jost & Benjamin Loppin, 2023. "Biophysical ordering transitions underlie genome 3D re-organization during cricket spermiogenesis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39908-1
    DOI: 10.1038/s41467-023-39908-1
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    References listed on IDEAS

    as
    1. Livolant, Françoise, 1991. "Ordered phases of DNA in vivo and in vitro," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 176(1), pages 117-137.
    2. Samantha Tirmarche & Shuhei Kimura & Raphaëlle Dubruille & Béatrice Horard & Benjamin Loppin, 2016. "Unlocking sperm chromatin at fertilization requires a dedicated egg thioredoxin in Drosophila," Nature Communications, Nature, vol. 7(1), pages 1-11, December.
    3. Amy R. Strom & Alexander V. Emelyanov & Mustafa Mir & Dmitry V. Fyodorov & Xavier Darzacq & Gary H. Karpen, 2017. "Phase separation drives heterochromatin domain formation," Nature, Nature, vol. 547(7662), pages 241-245, July.
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