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Elephant shark genome provides unique insights into gnathostome evolution

Author

Listed:
  • Byrappa Venkatesh

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673
    Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228)

  • Alison P. Lee

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Vydianathan Ravi

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Ashish K. Maurya

    (Developmental and Biomedical Genetics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Michelle M. Lian

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Jeremy B. Swann

    (Max-Planck-Institute of Immunobiology and Epigenetics, Stuebeweg 51, 79108 Freiburg, Germany)

  • Yuko Ohta

    (University of Maryland)

  • Martin F. Flajnik

    (University of Maryland)

  • Yoichi Sutoh

    (Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan)

  • Masanori Kasahara

    (Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan)

  • Shawn Hoon

    (Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673)

  • Vamshidhar Gangu

    (Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673)

  • Scott W. Roy

    (San Francisco State University)

  • Manuel Irimia

    (University of Toronto, Toronto, Ontario M5S 3E1, Canada)

  • Vladimir Korzh

    (Fish Developmental Biology Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Igor Kondrychyn

    (Fish Developmental Biology Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Zhi Wei Lim

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Boon-Hui Tay

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Sumanty Tohari

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Kiat Whye Kong

    (Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673)

  • Shufen Ho

    (Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673)

  • Belen Lorente-Galdos

    (Institut de Biologia Evolutiva (UPF-CSIC), PRBB, 08003 Barcelona, Spain
    Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain)

  • Javier Quilez

    (Institut de Biologia Evolutiva (UPF-CSIC), PRBB, 08003 Barcelona, Spain
    Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain)

  • Tomas Marques-Bonet

    (Institut de Biologia Evolutiva (UPF-CSIC), PRBB, 08003 Barcelona, Spain
    Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain)

  • Brian J. Raney

    (Center for Biomolecular Science and Engineering, School of Engineering, University of California Santa Cruz)

  • Philip W. Ingham

    (Developmental and Biomedical Genetics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Alice Tay

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • LaDeana W. Hillier

    (The Genome Institute at Washington University)

  • Patrick Minx

    (The Genome Institute at Washington University)

  • Thomas Boehm

    (Max-Planck-Institute of Immunobiology and Epigenetics, Stuebeweg 51, 79108 Freiburg, Germany)

  • Richard K. Wilson

    (The Genome Institute at Washington University)

  • Sydney Brenner

    (Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673)

  • Wesley C. Warren

    (The Genome Institute at Washington University)

Abstract

The emergence of jawed vertebrates (gnathostomes) from jawless vertebrates was accompanied by major morphological and physiological innovations, such as hinged jaws, paired fins and immunoglobulin-based adaptive immunity. Gnathostomes subsequently diverged into two groups, the cartilaginous fishes and the bony vertebrates. Here we report the whole-genome analysis of a cartilaginous fish, the elephant shark (Callorhinchus milii). We find that the C. milii genome is the slowest evolving of all known vertebrates, including the ‘living fossil’ coelacanth, and features extensive synteny conservation with tetrapod genomes, making it a good model for comparative analyses of gnathostome genomes. Our functional studies suggest that the lack of genes encoding secreted calcium-binding phosphoproteins in cartilaginous fishes explains the absence of bone in their endoskeleton. Furthermore, the adaptive immune system of cartilaginous fishes is unusual: it lacks the canonical CD4 co-receptor and most transcription factors, cytokines and cytokine receptors related to the CD4 lineage, despite the presence of polymorphic major histocompatibility complex class II molecules. It thus presents a new model for understanding the origin of adaptive immunity.

Suggested Citation

  • Byrappa Venkatesh & Alison P. Lee & Vydianathan Ravi & Ashish K. Maurya & Michelle M. Lian & Jeremy B. Swann & Yuko Ohta & Martin F. Flajnik & Yoichi Sutoh & Masanori Kasahara & Shawn Hoon & Vamshidha, 2014. "Elephant shark genome provides unique insights into gnathostome evolution," Nature, Nature, vol. 505(7482), pages 174-179, January.
  • Handle: RePEc:nat:nature:v:505:y:2014:i:7482:d:10.1038_nature12826
    DOI: 10.1038/nature12826
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    Cited by:

    1. Hong-Yan Wang & Jian-Yang Chen & Yanan Li & Xianghui Zhang & Xiang Liu & Yifang Lu & Hang He & Yubang Li & Hongxi Chen & Qun Liu & Yingyi Huang & Zhao Jia & Shuo Li & Yangqing Zhang & Shenglei Han & S, 2024. "Single-cell RNA sequencing illuminates the ontogeny, conservation and diversification of cartilaginous and bony fish lymphocytes," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Anthony K. Redmond & Dearbhaile Casey & Manu Kumar Gundappa & Daniel J. Macqueen & Aoife McLysaght, 2023. "Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Yuuki Y. Watanabe & Nicholas L. Payne, 2023. "Thermal sensitivity of metabolic rate mirrors biogeographic differences between teleosts and elasmobranchs," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    4. Shan Nan Chen & Zhen Gan & Jing Hou & Yue Cong Yang & Lin Huang & Bei Huang & Su Wang & Pin Nie, 2022. "Identification and establishment of type IV interferon and the characterization of interferon-υ including its class II cytokine receptors IFN-υR1 and IL-10R2," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

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