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Genome and transcriptome mechanisms driving cephalopod evolution

Author

Listed:
  • Caroline B. Albertin

    (Marine Biological Laboratory)

  • Sofia Medina-Ruiz

    (University of California)

  • Therese Mitros

    (University of California)

  • Hannah Schmidbaur

    (University of Vienna)

  • Gustavo Sanchez

    (Hiroshima University, Higashi Hiroshima)

  • Z. Yan Wang

    (University of Chicago)

  • Jane Grimwood

    (Hudson Alpha Institute of Biotechnology)

  • Joshua J. C. Rosenthal

    (Marine Biological Laboratory)

  • Clifton W. Ragsdale

    (University of Chicago)

  • Oleg Simakov

    (University of Vienna)

  • Daniel S. Rokhsar

    (University of California
    Okinawa Institute for Science and Technology
    Chan-Zuckerberg BioHub)

Abstract

Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations. To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid, Doryteuthis (Loligo) pealeii, and the California two-spot octopus, Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid, Euprymna scolopes. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29748-w
    DOI: 10.1038/s41467-022-29748-w
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    References listed on IDEAS

    as
    1. Daohan Jiang & Jianzhi Zhang, 2019. "The preponderance of nonsynonymous A-to-I RNA editing in coleoids is nonadaptive," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    2. Nicholas H. Putnam & Thomas Butts & David E. K. Ferrier & Rebecca F. Furlong & Uffe Hellsten & Takeshi Kawashima & Marc Robinson-Rechavi & Eiichi Shoguchi & Astrid Terry & Jr-Kai Yu & E`lia Benito-Gut, 2008. "The amphioxus genome and the evolution of the chordate karyotype," Nature, Nature, vol. 453(7198), pages 1064-1071, June.
    3. 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.
    4. Meng How Tan & Qin Li & Raghuvaran Shanmugam & Robert Piskol & Jennefer Kohler & Amy N. Young & Kaiwen Ivy Liu & Rui Zhang & Gokul Ramaswami & Kentaro Ariyoshi & Ankita Gupte & Liam P. Keegan & Cyril , 2017. "Dynamic landscape and regulation of RNA editing in mammals," Nature, Nature, vol. 550(7675), pages 249-254, October.
    5. 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.
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