Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs

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 Plott, Jane Grimwood, Jeremy Schmutz, Guadalupe Aguirre-Figueroa, Mustafa K. Khokha, Maura Lane, Isabelle Philipp, Mara Laslo, James Hanken, Gwenneg Kerdivel, Nicolas Buisine, Laurent M. Sachs, Daniel R. Buchholz, Taejoon Kwon, Heidi Smith-Parker, Marcos Gridi-Papp, Michael J. Ryan, Robert D. Denton, John H. Malone, John B. Wallingford, Aaron F. Straight, Rebecca Heald, Dirk Hockemeyer, Richard M. Harland and Daniel S. Rokhsar ()
Additional contact information
Jessen V. Bredeson: University of California
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
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
Richard M. Harland: University of California
Daniel S. Rokhsar: University of California

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-023-43012-9

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