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Ancient deuterostome origins of vertebrate brain signalling centres

Author

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  • Ariel M. Pani

    (Committee on Evolutionary Biology, The University of Chicago, 1025 East 57th Street, Chicago, Illinois 60637, USA
    Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, Pacific Grove, California 93950, USA)

  • Erin E. Mullarkey

    (Committee on Neurobiology, The University of Chicago, 947 East 58th Street, Chicago, Illinois 60637, USA)

  • Jochanan Aronowicz

    (The University of Chicago, 1027 East 57th Street, Chicago, Illinois 60637, USA)

  • Stavroula Assimacopoulos

    (The University of Chicago, 947 East 58th Street, Chicago, Illinois 60637, USA)

  • Elizabeth A. Grove

    (Committee on Neurobiology, The University of Chicago, 947 East 58th Street, Chicago, Illinois 60637, USA
    The University of Chicago, 1027 East 57th Street, Chicago, Illinois 60637, USA
    The University of Chicago, 947 East 58th Street, Chicago, Illinois 60637, USA)

  • Christopher J. Lowe

    (Committee on Evolutionary Biology, The University of Chicago, 1025 East 57th Street, Chicago, Illinois 60637, USA
    Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, Pacific Grove, California 93950, USA
    The University of Chicago, 1027 East 57th Street, Chicago, Illinois 60637, USA)

Abstract

Neuroectodermal signalling centres induce and pattern many novel vertebrate brain structures but are absent, or divergent, in invertebrate chordates. This has led to the idea that signalling-centre genetic programs were first assembled in stem vertebrates and potentially drove morphological innovations of the brain. However, this scenario presumes that extant cephalochordates accurately represent ancestral chordate characters, which has not been tested using close chordate outgroups. Here we report that genetic programs homologous to three vertebrate signalling centres—the anterior neural ridge, zona limitans intrathalamica and isthmic organizer—are present in the hemichordate Saccoglossus kowalevskii. Fgf8/17/18 (a single gene homologous to vertebrate Fgf8, Fgf17 and Fgf18), sfrp1/5, hh and wnt1 are expressed in vertebrate-like arrangements in hemichordate ectoderm, and homologous genetic mechanisms regulate ectodermal patterning in both animals. We propose that these genetic programs were components of an unexpectedly complex, ancient genetic regulatory scaffold for deuterostome body patterning that degenerated in amphioxus and ascidians, but was retained to pattern divergent structures in hemichordates and vertebrates.

Suggested Citation

  • Ariel M. Pani & Erin E. Mullarkey & Jochanan Aronowicz & Stavroula Assimacopoulos & Elizabeth A. Grove & Christopher J. Lowe, 2012. "Ancient deuterostome origins of vertebrate brain signalling centres," Nature, Nature, vol. 483(7389), pages 289-294, March.
    • Handle: RePEc:nat:nature:v:483:y:2012:i:7389:d:10.1038_nature10838
    DOI: 10.1038/nature10838
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    Cited by:

    1. Alice M. H. Bedois & Hugo J. Parker & Andrew J. Price & Jason A. Morrison & Marianne E. Bronner & Robb Krumlauf, 2024. "Sea lamprey enlightens the origin of the coupling of retinoic acid signaling to vertebrate hindbrain segmentation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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