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

Author

Listed:
  • Hannah Schmidbaur

    (University of Vienna)

  • Akane Kawaguchi

    (Institute for Molecular Pathology)

  • Tereza Clarence

    (The Francis Crick Institute)

  • Xiao Fu

    (The Francis Crick Institute)

  • Oi Pui Hoang

    (University of Vienna)

  • Bob Zimmermann

    (University of Vienna)

  • Elena A. Ritschard

    (University of Vienna
    Stazione Zoologica Anton Dohrn)

  • Anton Weissenbacher

    (Vienna Zoo)

  • Jamie S. Foster

    (University of Florida, Space Life Science Lab)

  • Spencer V. Nyholm

    (University of Connecticut)

  • Paul A. Bates

    (The Francis Crick Institute)

  • Caroline B. Albertin

    (Marine Biological Laboratory)

  • Elly Tanaka

    (Institute for Molecular Pathology)

  • Oleg Simakov

    (University of Vienna)

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.

Suggested Citation

  • Hannah Schmidbaur & Akane Kawaguchi & Tereza Clarence & Xiao Fu & Oi Pui Hoang & Bob Zimmermann & Elena A. Ritschard & Anton Weissenbacher & Jamie S. Foster & Spencer V. Nyholm & Paul A. Bates & Carol, 2022. "Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29694-7
    DOI: 10.1038/s41467-022-29694-7
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    References listed on IDEAS

    as
    1. Oleg Simakov & Ferdinand Marletaz & Sung-Jin Cho & Eric Edsinger-Gonzales & Paul Havlak & Uffe Hellsten & Dian-Han Kuo & Tomas Larsson & Jie Lv & Detlev Arendt & Robert Savage & Kazutoyo Osoegawa & Pi, 2013. "Insights into bilaterian evolution from three spiralian genomes," Nature, Nature, vol. 493(7433), pages 526-531, January.
    2. Caroline B. Albertin & Oleg Simakov & Therese Mitros & Z. Yan Wang & Judit R. Pungor & Eric Edsinger-Gonzales & Sydney Brenner & Clifton W. Ragsdale & Daniel S. Rokhsar, 2015. "The octopus genome and the evolution of cephalopod neural and morphological novelties," Nature, Nature, vol. 524(7564), pages 220-224, August.
    3. Nadezda Kryuchkova-Mostacci & Marc Robinson-Rechavi, 2016. "Tissue-Specificity of Gene Expression Diverges Slowly between Orthologs, and Rapidly between Paralogs," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-13, December.
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    Cited by:

    1. Caroline B. Albertin & Sofia Medina-Ruiz & Therese Mitros & Hannah Schmidbaur & Gustavo Sanchez & Z. Yan Wang & Jane Grimwood & Joshua J. C. Rosenthal & Clifton W. Ragsdale & Oleg Simakov & Daniel S. , 2022. "Genome and transcriptome mechanisms driving cephalopod evolution," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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