IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39908-1.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39908-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39908-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yifeng Qi & Bin Zhang, 2021. "Chromatin network retards nucleoli coalescence," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. Ting Peng & Yingping Hou & Haowei Meng & Yong Cao & Xiaotian Wang & Lumeng Jia & Qing Chen & Yang Zheng & Yujie Sun & Hebing Chen & Tingting Li & Cheng Li, 2023. "Mapping nucleolus-associated chromatin interactions using nucleolus Hi-C reveals pattern of heterochromatin interactions," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Akiko Doi & Gianmarco D. Suarez & Rita Droste & H. Robert Horvitz, 2023. "A DEAD-box helicase drives the partitioning of a pro-differentiation NAB protein into nuclear foci," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Jorine M. Eeftens & Manya Kapoor & Davide Michieletto & Clifford P. Brangwynne, 2021. "Polycomb condensates can promote epigenetic marks but are not required for sustained chromatin compaction," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    5. Wenqi Sun & Qianhua Dong & Xueqing Li & Jinxin Gao & Xianwen Ye & Chunyi Hu & Fei Li & Yong Chen, 2024. "The SUN-family protein Sad1 mediates heterochromatin spatial organization through interaction with histone H2A-H2B," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Hye Ji Cha & Özgün Uyan & Yan Kai & Tianxin Liu & Qian Zhu & Zuzana Tothova & Giovanni A. Botten & Jian Xu & Guo-Cheng Yuan & Job Dekker & Stuart H. Orkin, 2021. "Inner nuclear protein Matrin-3 coordinates cell differentiation by stabilizing chromatin architecture," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    7. Taehyun Kim & Jaeyoon Yoo & Sungho Do & Dong Soo Hwang & YongKeun Park & Yongdae Shin, 2023. "RNA-mediated demixing transition of low-density condensates," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Catherine Naughton & Covadonga Huidobro & Claudia R. Catacchio & Adam Buckle & Graeme R. Grimes & Ryu-Suke Nozawa & Stefania Purgato & Mariano Rocchi & Nick Gilbert, 2022. "Human centromere repositioning activates transcription and opens chromatin fibre structure," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Hyun-Soo Kim & Benjamin Roche & Sonali Bhattacharjee & Leila Todeschini & An-Yun Chang & Christopher Hammell & André Verdel & Robert A. Martienssen, 2024. "Clr4SUV39H1 ubiquitination and non-coding RNA mediate transcriptional silencing of heterochromatin via Swi6 phase separation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Naohiro Kuwayama & Tomoya Kujirai & Yusuke Kishi & Rina Hirano & Kenta Echigoya & Lingyan Fang & Sugiko Watanabe & Mitsuyoshi Nakao & Yutaka Suzuki & Kei-ichiro Ishiguro & Hitoshi Kurumizaka & Yukiko , 2023. "HMGA2 directly mediates chromatin condensation in association with neuronal fate regulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Ellen H. Brumbaugh-Reed & Yang Gao & Kazuhiro Aoki & Jared E. Toettcher, 2024. "Rapid and reversible dissolution of biomolecular condensates using light-controlled recruitment of a solubility tag," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    12. Yohan Lee & Sujin Park & Feng Yuan & Carl C. Hayden & Liping Wang & Eileen M. Lafer & Siyoung Q. Choi & Jeanne C. Stachowiak, 2023. "Transmembrane coupling of liquid-like protein condensates," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Zhaowei Yu & Qi Wang & Qichen Zhang & Yawen Tian & Guo Yan & Jidong Zhu & Guangya Zhu & Yong Zhang, 2024. "Decoding the genomic landscape of chromatin-associated biomolecular condensates," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Pan Jia & Xiang Li & Xuelei Wang & Liangjiao Yao & Yingying Xu & Yu Hu & Wenwen Xu & Zhe He & Qifan Zhao & Yicong Deng & Yi Zang & Meiyu Zhang & Yan Zhang & Jun Qin & Wei Lu, 2021. "ZMYND8 mediated liquid condensates spatiotemporally decommission the latent super-enhancers during macrophage polarization," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    15. Lidice González & Daniel Kolbin & Christian Trahan & Célia Jeronimo & François Robert & Marlene Oeffinger & Kerry Bloom & Stephen W. Michnick, 2023. "Adaptive partitioning of a gene locus to the nuclear envelope in Saccharomyces cerevisiae is driven by polymer-polymer phase separation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Lennart Enders & Marton Siklos & Jan Borggräfe & Stefan Gaussmann & Anna Koren & Monika Malik & Tatjana Tomek & Michael Schuster & Jiří Reiniš & Elisa Hahn & Andrea Rukavina & Andreas Reicher & Tamara, 2023. "Pharmacological perturbation of the phase-separating protein SMNDC1," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Meng Zhang & César Díaz-Celis & Jianfang Liu & Jinhui Tao & Paul D. Ashby & Carlos Bustamante & Gang Ren, 2024. "Angle between DNA linker and nucleosome core particle regulates array compaction revealed by individual-particle cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Buer Sen & Zhihui Xie & Michelle D. Thomas & Samantha G. Pattenden & Sean Howard & Cody McGrath & Maya Styner & Gunes Uzer & Terrence S. Furey & Janet Rubin, 2024. "Nuclear actin structure regulates chromatin accessibility," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Adel Al Jord & Gaëlle Letort & Soline Chanet & Feng-Ching Tsai & Christophe Antoniewski & Adrien Eichmuller & Christelle Da Silva & Jean-René Huynh & Nir S. Gov & Raphaël Voituriez & Marie-Émilie Terr, 2022. "Cytoplasmic forces functionally reorganize nuclear condensates in oocytes," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    20. Simon M Lichtinger & Adiran Garaizar & Rosana Collepardo-Guevara & Aleks Reinhardt, 2021. "Targeted modulation of protein liquid–liquid phase separation by evolution of amino-acid sequence," PLOS Computational Biology, Public Library of Science, vol. 17(8), pages 1-28, August.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39908-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.