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Cited by 66Cephalopods and Marine BiologyChromosomal and Genetic VariationsGenomics and Phylogenetic Studies

Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization

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Schmidbaur, Hannah, Kawaguchi, Akane, Clarence, Tereza, Fu, Xiao, Hoang, Oi Pui, Zimmermann, Bob, Ritschard, Elena A., Weissenbacher, Anton +6 more·2022·Nature Communications
DOI 10.1038/s41467-022-29694-7PMC PMC9023564
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Abstract

Coleoid cephalopods (squid, cuttlefish, octopus) have the largest nervous system among invertebrates that together with many lineage-specific morphological traits enables complex behaviors. The genomic basis underlying these innovations remains unknown. Using comparative and functional genomics in the model squid Euprymna scolopes , we reveal the unique genomic, topological, and regulatory organization of cephalopod genomes. We show that coleoid cephalopod genomes have been extensively restructured compared to other animals, leading to the emergence of hundreds of tightly linked and evolutionary unique gene clusters (microsyntenies). Such novel microsyntenies correspond to topological compartments with a distinct regulatory structure and contribute to complex expression patterns. In particular, we identify a set of microsyntenies associated with cephalopod innovations (MACIs) broadly enriched in cephalopod nervous system expression. We posit that the emergence of MACIs was instrumental to cephalopod nervous system evolution and propose that microsyntenic profiling will be central to understanding cephalopod innovations.

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  • Comparable lineage-wide signatures are also shared across coleoid cephalopods, despite the dramatic chromosomal rearrangements that occurred since the octopus-squid divergence 241 million years ago.

    “Comparable lineage-wide signatures are also shared across coleoid cephalopods (octopuses and squids) (170), despite the dramatic chromosomal rearrangements that occurred (170) since the octopus–squid divergence 241 million years ago (171).”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [170]

    The Results and discussion section reports cephalopod-specific microsyntenic blocks shared by squid and octopus and evidence of large-scale chromosomal reorganization. It suggests that many translocations or chromosomal fusions occurred in the coleoid ancestor, however, rather than establishing that they occurred since the octopus–squid divergence. The 241-million-year date is attributed to a different citation in the citing sentence. (LLM, conf=0.84)

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Authors
Schmidbaur, H., Kawaguchi, A., Clarence, T., Fu, X., Hoang, O. P., Zimmermann, B., Ritschard, E. A., Weissenbacher, A., Foster, J. S., Nyholm, S. V., Bates, P. A., Albertin, C. B., Tanaka, E., & Simakov, O.
Affiliations
  • University of Vienna (AT)
  • Research Institute of Molecular Pathology (AT)
  • The Francis Crick Institute (GB)
  • Schönbrunner Tiergarten-GmbH (AT)
  • University of Florida (US)
  • University of Connecticut (US)
  • Marine Biological Laboratory (US)
Corresponding author
  • Albertin, Caroline B.
  • Tanaka, Elly
  • Simakov, Oleg
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2022-04-21
Volume
13
Issue
1
Pages
2172-2172
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-022-29694-7
PMC
PMC9023564
OpenAlex
W4224248851
Cited by
66
References
3
Citations by year
2026: 12 · 2025: 15 · 2024: 5 · 2023: 12 · 2022: 22
FWCI
11.25
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Open Access Server of the Woods Hole Scientific Community (Woods Hole Scientific Community) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • The Francis Crick Institute (cc-by)
Funders
  • National Science Foundation (1557914)
  • National Aeronautics and Space Administration (80NSSC18K1465)
  • University of Chicago
  • Wellcome Trust (FC001003)
  • Francis Crick Institute (10316, FC001003)
  • Cancer Research UK (FC001003, FC0001003)
  • Austrian Science Fund (P30686‐B29), P30686)
  • Universität Wien
  • Nuclear Safety and Security Commission
  • Medical Research Council (FC001003)
  • Japan Society for the Promotion of Science
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Cephalopods and Marine Biology
  • 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
Keywords
microsynteny, gene regulatory evolution, Euprymna scolopes, squid, Coleoidea, nervous system evolution, gene clusters, genome topology, gene expression patterns
MeSH terms
Animals, Invertebrates, Genome, Genomics, Cephalopoda, Decapodiformes

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