Nature Communications (Jan 2024)

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,
  • Daniel S. Rokhsar

DOI
https://doi.org/10.1038/s41467-023-43012-9
Journal volume & issue
Vol. 15, no. 1
pp. 1 – 18

Abstract

Read online

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.