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Extensive DNA methylome rearrangement during early lamprey embryogenesis

Author

Listed:
  • Allegra Angeloni

    (Garvan Institute of Medical Research
    University of New South Wales)

  • Skye Fissette

    (Michigan State University)

  • Deniz Kaya

    (University of Oxford)

  • Jillian M. Hammond

    (Garvan Institute of Medical Research
    Garvan Institute of Medical Research and Murdoch Children’s Research Institute)

  • Hasindu Gamaarachchi

    (Garvan Institute of Medical Research
    Garvan Institute of Medical Research and Murdoch Children’s Research Institute
    University of New South Wales)

  • Ira W. Deveson

    (Garvan Institute of Medical Research
    Garvan Institute of Medical Research and Murdoch Children’s Research Institute
    University of New South Wales)

  • Robert J. Klose

    (University of Oxford)

  • Weiming Li

    (Michigan State University)

  • Xiaotian Zhang

    (Van Andel Research Institute
    University of Texas Health Science Center)

  • Ozren Bogdanovic

    (Garvan Institute of Medical Research
    University of New South Wales
    CSIC-Universidad Pablo de Olavide-Junta de Andalucía)

Abstract

DNA methylation (5mC) is a repressive gene regulatory mark widespread in vertebrate genomes, yet the developmental dynamics in which 5mC patterns are established vary across species. While mammals undergo two rounds of global 5mC erasure, teleosts, for example, exhibit localized maternal-to-paternal 5mC remodeling. Here, we studied 5mC dynamics during the embryonic development of sea lamprey, a jawless vertebrate which occupies a critical phylogenetic position as the sister group of the jawed vertebrates. We employed 5mC quantification in lamprey embryos and tissues, and discovered large-scale maternal-to-paternal epigenome remodeling that affects ~30% of the embryonic genome and is predominantly associated with partially methylated domains. We further demonstrate that sequences eliminated during programmed genome rearrangement (PGR), are hypermethylated in sperm prior to the onset of PGR. Our study thus unveils important insights into the evolutionary origins of vertebrate 5mC reprogramming, and how this process might participate in diverse developmental strategies.

Suggested Citation

  • Allegra Angeloni & Skye Fissette & Deniz Kaya & Jillian M. Hammond & Hasindu Gamaarachchi & Ira W. Deveson & Robert J. Klose & Weiming Li & Xiaotian Zhang & Ozren Bogdanovic, 2024. "Extensive DNA methylome rearrangement during early lamprey embryogenesis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46085-2
    DOI: 10.1038/s41467-024-46085-2
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    References listed on IDEAS

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    1. Zachary D. Smith & Michelle M. Chan & Tarjei S. Mikkelsen & Hongcang Gu & Andreas Gnirke & Aviv Regev & Alexander Meissner, 2012. "A unique regulatory phase of DNA methylation in the early mammalian embryo," Nature, Nature, vol. 484(7394), pages 339-344, April.
    2. Ryan Lister & Mattia Pelizzola & Robert H. Dowen & R. David Hawkins & Gary Hon & Julian Tonti-Filippini & Joseph R. Nery & Leonard Lee & Zhen Ye & Que-Minh Ngo & Lee Edsall & Jessica Antosiewicz-Bourg, 2009. "Human DNA methylomes at base resolution show widespread epigenomic differences," Nature, Nature, vol. 462(7271), pages 315-322, November.
    3. Grégoire Vernaz & Milan Malinsky & Hannes Svardal & Mingliu Du & Alexandra M. Tyers & M. Emília Santos & Richard Durbin & Martin J. Genner & George F. Turner & Eric A. Miska, 2021. "Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Rahul M. Kohli & Yi Zhang, 2013. "TET enzymes, TDG and the dynamics of DNA demethylation," Nature, Nature, vol. 502(7472), pages 472-479, October.
    5. Raphaël Margueron & Danny Reinberg, 2011. "The Polycomb complex PRC2 and its mark in life," Nature, Nature, vol. 469(7330), pages 343-349, January.
    6. Dorit Hockman & Vanessa Chong-Morrison & Stephen A. Green & Daria Gavriouchkina & Ivan Candido-Ferreira & Irving T. C. Ling & Ruth M. Williams & Chris T. Amemiya & Jeramiah J. Smith & Marianne E. Bron, 2019. "A genome-wide assessment of the ancestral neural crest gene regulatory network," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    7. Ksenia Skvortsova & Katsiaryna Tarbashevich & Martin Stehling & Ryan Lister & Manuel Irimia & Erez Raz & Ozren Bogdanovic, 2019. "Retention of paternal DNA methylome in the developing zebrafish germline," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    8. Kentaro Mochizuki & Jafar Sharif & Kenjiro Shirane & Kousuke Uranishi & Aaron B. Bogutz & Sanne M. Janssen & Ayumu Suzuki & Akihiko Okuda & Haruhiko Koseki & Matthew C. Lorincz, 2021. "Repression of germline genes by PRC1.6 and SETDB1 in the early embryo precedes DNA methylation-mediated silencing," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    9. Yoichiro Nakatani & Prashant Shingate & Vydianathan Ravi & Nisha E. Pillai & Aravind Prasad & Aoife McLysaght & Byrappa Venkatesh, 2021. "Publisher Correction: Reconstruction of proto-vertebrate, protocyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    10. Christian Popp & Wendy Dean & Suhua Feng & Shawn J. Cokus & Simon Andrews & Matteo Pellegrini & Steven E. Jacobsen & Wolf Reik, 2010. "Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency," Nature, Nature, vol. 463(7284), pages 1101-1105, February.
    11. Zohar Shipony & Zohar Mukamel & Netta Mendelson Cohen & Gilad Landan & Elad Chomsky & Shlomit Reich Zeliger & Yael Chagit Fried & Elena Ainbinder & Nir Friedman & Amos Tanay, 2014. "Dynamic and static maintenance of epigenetic memory in pluripotent and somatic cells," Nature, Nature, vol. 513(7516), pages 115-119, September.
    12. Wolfgang Mayer & Alain Niveleau & Jörn Walter & Reinald Fundele & Thomas Haaf, 2000. "Demethylation of the zygotic paternal genome," Nature, Nature, vol. 403(6769), pages 501-502, February.
    13. Silvia Domcke & Anaïs Flore Bardet & Paul Adrian Ginno & Dominik Hartl & Lukas Burger & Dirk Schübeler, 2015. "Competition between DNA methylation and transcription factors determines binding of NRF1," Nature, Nature, vol. 528(7583), pages 575-579, December.
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