De novo genome assemblies of two cryptodiran turtles with ZZ/ZW and XX/XY sex chromosomes provide insights into patterns of genome reshuffling and uncover novel 3D genome folding in amniotes

Basanta Bista, Laura González-Rodelas, Lucía Álvarez-González, Zhi Qiang Wu, Eugenia E. Montiel, Ling Sze Lee, Daleen B. Badenhorst, Srihari Radhakrishnan, Robert Literman, Beatriz Navarro-Dominguez, John B. Iverson, Simon Orozco-Arias, Josefa González, Aurora Ruiz-Herrera*, Nicole Valenzuela*

*Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Understanding the evolution of chromatin conformation among species is fundamental to elucidate the architecture and plasticity of genomes. Nonrandom interactions of linearly distant loci regulate gene function in species-specific patterns, affecting genome function, evolution, and, ultimately, speciation. Yet, data from nonmodel organisms are scarce. To capture the macroevolutionary diversity of vertebrate chromatin conformation, here we generate de novo genome assemblies for two cryptodiran (hidden-neck) turtles via Illumina sequencing, chromosome conformation capture, and RNA-seq: Apalone spinifera (ZZ/ZW, 2n = 66) and Staurotypus triporcatus (XX/XY, 2n = 54). We detected differences in the three-dimensional (3D) chromatin structure in turtles compared to other amniotes beyond the fusion/fission events detected in the linear genomes. Namely, whole-genome comparisons revealed distinct trends of chromosome rearrangements in turtles: (1) a low rate of genome reshuffling in Apalone (Trionychidae) whose karyotype is highly conserved when compared to chicken (likely ancestral for turtles), and (2) a moderate rate of fusions/fissions in Staurotypus (Kinosternidae) and Trachemys scripta (Emydidae). Furthermore, we identified a chromosome folding pattern that enables “centromere–telomere interactions” previously undetected in turtles. The combined turtle pattern of “centromere–telomere interactions” (discovered here) plus “centromere clustering” (previously reported in sauropsids) is novel for amniotes and it counters previous hypotheses about amniote 3D chromatin structure. We hypothesize that the divergent pattern found in turtles originated from an amniote ancestral state defined by a nuclear configuration with extensive associations among microchromosomes that were preserved upon the reshuffling of the linear genome.

Original languageEnglish
Pages (from-to)1553-1569
Number of pages17
JournalGenome research
Volume34
Issue number10
DOIs
Publication statusPublished - 16 Oct 2024

Keywords

  • Animals
  • Turtles/genetics
  • Genome
  • Sex Chromosomes/genetics
  • Male
  • Female
  • Chromatin/genetics
  • Evolution, Molecular

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