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Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs

Author

Listed:
  • Jessen V. Bredeson

    (University of California
    DOE-Joint Genome Institute)

  • Austin B. Mudd

    (University of California)

  • Sofia Medina-Ruiz

    (University of California)

  • Therese Mitros

    (University of California)

  • Owen Kabnick Smith

    (Stanford University School of Medicine)

  • Kelly E. Miller

    (University of California)

  • Jessica B. Lyons

    (University of California)

  • Sanjit S. Batra

    (University of California Berkeley)

  • Joseph Park

    (University of California)

  • Kodiak C. Berkoff

    (University of California)

  • Christopher Plott

    (HudsonAlpha Institute for Biotechnology)

  • Jane Grimwood

    (HudsonAlpha Institute for Biotechnology)

  • Jeremy Schmutz

    (HudsonAlpha Institute for Biotechnology)

  • Guadalupe Aguirre-Figueroa

    (Stanford University School of Medicine)

  • Mustafa K. Khokha

    (Yale University School of Medicine)

  • Maura Lane

    (Yale University School of Medicine)

  • Isabelle Philipp

    (University of California)

  • Mara Laslo

    (Harvard University)

  • James Hanken

    (Harvard University)

  • Gwenneg Kerdivel

    (UMR 7221 CNRS, Muséum National d’Histoire Naturelle)

  • Nicolas Buisine

    (UMR 7221 CNRS, Muséum National d’Histoire Naturelle)

  • Laurent M. Sachs

    (UMR 7221 CNRS, Muséum National d’Histoire Naturelle)

  • Daniel R. Buchholz

    (University of Cincinnati)

  • Taejoon Kwon

    (Ulsan National Institute of Science and Technology
    Institute for Basic Science (IBS))

  • Heidi Smith-Parker

    (University of Texas)

  • Marcos Gridi-Papp

    (University of the Pacific)

  • Michael J. Ryan

    (University of Texas)

  • Robert D. Denton

    (University of Connecticut)

  • John H. Malone

    (University of Connecticut)

  • John B. Wallingford

    (The University of Texas at Austin)

  • Aaron F. Straight

    (Stanford University School of Medicine)

  • Rebecca Heald

    (University of California)

  • Dirk Hockemeyer

    (University of California
    University of California
    Chan-Zuckerberg BioHub)

  • Richard M. Harland

    (University of California)

  • Daniel S. Rokhsar

    (University of California
    DOE-Joint Genome Institute
    University of California
    Chan-Zuckerberg BioHub)

Abstract

Frogs are an ecologically diverse and phylogenetically ancient group of anuran amphibians that include important vertebrate cell and developmental model systems, notably the genus Xenopus. Here we report a high-quality reference genome sequence for the western clawed frog, Xenopus tropicalis, along with draft chromosome-scale sequences of three distantly related emerging model frog species, Eleutherodactylus coqui, Engystomops pustulosus, and Hymenochirus boettgeri. Frog chromosomes have remained remarkably stable since the Mesozoic Era, with limited Robertsonian (i.e., arm-preserving) translocations and end-to-end fusions found among the smaller chromosomes. Conservation of synteny includes conservation of centromere locations, marked by centromeric tandem repeats associated with Cenp-a binding surrounded by pericentromeric LINE/L1 elements. This work explores the structure of chromosomes across frogs, using a dense meiotic linkage map for X. tropicalis and chromatin conformation capture (Hi-C) data for all species. Abundant satellite repeats occupy the unusually long (~20 megabase) terminal regions of each chromosome that coincide with high rates of recombination. Both embryonic and differentiated cells show reproducible associations of centromeric chromatin and of telomeres, reflecting a Rabl-like configuration. Our comparative analyses reveal 13 conserved ancestral anuran chromosomes from which contemporary frog genomes were constructed.

Suggested Citation

  • Jessen V. Bredeson & Austin B. Mudd & Sofia Medina-Ruiz & Therese Mitros & Owen Kabnick Smith & Kelly E. Miller & Jessica B. Lyons & Sanjit S. Batra & Joseph Park & Kodiak C. Berkoff & Christopher Plo, 2024. "Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-43012-9
    DOI: 10.1038/s41467-023-43012-9
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    as
    1. Martin Mascher & Heidrun Gundlach & Axel Himmelbach & Sebastian Beier & Sven O. Twardziok & Thomas Wicker & Volodymyr Radchuk & Christoph Dockter & Pete E. Hedley & Joanne Russell & Micha Bayer & Luke, 2017. "A chromosome conformation capture ordered sequence of the barley genome," Nature, Nature, vol. 544(7651), pages 427-433, April.
    2. Andreea Dréau & Vrinda Venu & Elena Avdievich & Ludmila Gaspar & Felicity C. Jones, 2019. "Genome-wide recombination map construction from single individuals using linked-read sequencing," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    3. Tim J. Stevens & David Lando & Srinjan Basu & Liam P. Atkinson & Yang Cao & Steven F. Lee & Martin Leeb & Kai J. Wohlfahrt & Wayne Boucher & Aoife O’Shaughnessy-Kirwan & Julie Cramard & Andre J. Faure, 2017. "3D structures of individual mammalian genomes studied by single-cell Hi-C," Nature, Nature, vol. 544(7648), pages 59-64, April.
    4. Sergej Nowoshilow & Siegfried Schloissnig & Ji-Feng Fei & Andreas Dahl & Andy W. C. Pang & Martin Pippel & Sylke Winkler & Alex R. Hastie & George Young & Juliana G. Roscito & Francisco Falcon & Dunja, 2018. "Author Correction: The axolotl genome and the evolution of key tissue formation regulators," Nature, Nature, vol. 559(7712), pages 2-2, July.
    5. Andrew R. Blaustein & Andy Dobson, 2006. "A message from the frogs," Nature, Nature, vol. 439(7073), pages 143-144, January.
    6. Brian Leung & Anna L. Hargreaves & Dan A. Greenberg & Brian McGill & Maria Dornelas & Robin Freeman, 2020. "Clustered versus catastrophic global vertebrate declines," Nature, Nature, vol. 588(7837), pages 267-271, December.
    7. Adam M. Session & Yoshinobu Uno & Taejoon Kwon & Jarrod A. Chapman & Atsushi Toyoda & Shuji Takahashi & Akimasa Fukui & Akira Hikosaka & Atsushi Suzuki & Mariko Kondo & Simon J. van Heeringen & Ian Qu, 2016. "Genome evolution in the allotetraploid frog Xenopus laevis," Nature, Nature, vol. 538(7625), pages 336-343, October.
    8. Sergej Nowoshilow & Siegfried Schloissnig & Ji-Feng Fei & Andreas Dahl & Andy W. C. Pang & Martin Pippel & Sylke Winkler & Alex R. Hastie & George Young & Juliana G. Roscito & Francisco Falcon & Dunja, 2018. "The axolotl genome and the evolution of key tissue formation regulators," Nature, Nature, vol. 554(7690), pages 50-55, February.
    9. Zhijun Duan & Mirela Andronescu & Kevin Schutz & Sean McIlwain & Yoo Jung Kim & Choli Lee & Jay Shendure & Stanley Fields & C. Anthony Blau & William S. Noble, 2010. "A three-dimensional model of the yeast genome," Nature, Nature, vol. 465(7296), pages 363-367, May.
    10. Ross A. Alford & Philip M. Dixon & Joseph H. K. Pechmann, 2001. "Global amphibian population declines," Nature, Nature, vol. 412(6846), pages 499-500, August.
    11. Jun Li & Haiyan Yu & Wenxia Wang & Chao Fu & Wei Zhang & Fengming Han & Hua Wu, 2019. "Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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