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Cited by 151Chromosomal and Genetic VariationsGenomics and Phylogenetic StudiesGenome Rearrangement Algorithms

Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution

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Nakatani, Yoichiro, Shingate, Prashant, Ravi, Vydianathan, Pillai, Nisha E., Prasad, Aravind, McLysaght, Aoife, Venkatesh, Byrappa·2021·Nature Communications
DOI 10.1038/s41467-021-24573-zPMC PMC8302630
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Abstract

Ancient polyploidization events have had a lasting impact on vertebrate genome structure, organization and function. Some key questions regarding the number of ancient polyploidization events and their timing in relation to the cyclostome-gnathostome divergence have remained contentious. Here we generate de novo long-read-based chromosome-scale genome assemblies for the Japanese lamprey and elephant shark. Using these and other representative genomes and developing algorithms for the probabilistic macrosynteny model, we reconstruct high-resolution proto-vertebrate, proto-cyclostome and proto-gnathostome genomes. Our reconstructions resolve key questions regarding the early evolutionary history of vertebrates. First, cyclostomes diverged from the lineage leading to gnathostomes after a shared tetraploidization (1R) but before a gnathostome-specific tetraploidization (2R). Second, the cyclostome lineage experienced an additional hexaploidization. Third, 2R in the gnathostome lineage was an allotetraploidization event, and biased gene loss from one of the subgenomes shaped the gnathostome genome by giving rise to remarkably conserved microchromosomes. Thus, our reconstructions reveal the major evolutionary events and offer new insights into the origin and evolution of vertebrate genomes.

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  • These patterns of conservation hold largely for smaller chromosomes across vertebrates, including mammals.

    “These patterns of conservation hold largely for smaller chromosomes across vertebrates, including mammals (65, 67, 100)”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [65]

    The Results section on the origin of microchromosomes reports that smaller ancestral chromosomes tend to have higher gene densities across the species studied, including human-derived segments (Fig. 5). But it says intact microchromosomes persist in some gnathostomes, such as chicken, spotted gar and elephant shark, and explicitly states that humans have no microchromosomes. It therefore supports conservation of some features in mammalian chromosomal regions, not conservation of the small chromosomes themselves in mammals; page numbers were not available in our copy. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Comparison of chromosome-scale genomes across vertebrates has clarified the timing and consequences of ancient whole-genome duplications that led to extant vertebrate genomes, supporting Ohno's hypothesis.

    “Comparison of chromosome-scale genomes across vertebrates has clarified the timing and consequences of the ancient whole-genome duplications (WGDs) that led to extant vertebrate genomes (59–65), supporting Ohno's (66) hypothesis.”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [65]

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Authors
Nakatani, Y., Shingate, P., Ravi, V., Pillai, N. E., Prasad, A., McLysaght, A., & Venkatesh, B.
Affiliations
  • Trinity College Dublin (IE)
  • Agency for Science, Technology and Research (SG)
Corresponding author
  • McLysaght, Aoife
  • Venkatesh, Byrappa
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2021-07-23
Volume
12
Issue
1
Pages
4489-4489
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-021-24573-z
PMC
PMC8302630
OpenAlex
W3184440907
Cited by
151
References
2
Citations by year
2026: 31 · 2025: 25 · 2024: 20 · 2023: 36 · 2022: 28 · 2021: 11
FWCI
13.85
Type
journal article
Language
en
Update notices
correction (2021-07-29)
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion, cc-by-nc-sa)
Funders
Biomedical Research Council of A*STAR, Singapore
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
Keywords
early vertebrate evolution, polyploidization, tetraploidization, allotetraploidization, macrosynteny, elephant shark, chromosome-level genome assembly, microchromosomes
MeSH terms
Animals, Chromosomes, Humans, Lampreys, Models, Genetic, Phylogeny, Polyploidy, Sharks, Genetic Variation, Vertebrates, Genome, Sequence Analysis, DNA, Evolution, Molecular, Synteny

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