An epithelial signalling centre in sharks supports homology of tooth morphogenesis in vertebrates

  1. Alexandre P Thiery
  2. Ariane S Standing
  3. Rory L Cooper
  4. Gareth J Fraser  Is a corresponding author
  1. King's College London, United Kingdom
  2. University of Florida, United States
  3. University of Geneva, Switzerland

Abstract

Development of tooth shape is regulated by the enamel knot signalling centre, at least in mammals. Fgf signalling regulates differential proliferation between the enamel knot and adjacent dental epithelia during tooth development, leading to formation of the dental cusp. The presence of an enamel knot in non-mammalian vertebrates is debated given differences in signalling. Here we show the conservation and restriction of fgf3, fgf10 and shh to the sites of future dental cusps in the shark (Scyliorhinus canicula), whilst also highlighting striking differences between the shark and mouse. We reveal shifts in tooth size, shape and cusp number following small molecule perturbations of canonical Wnt signalling. Resulting tooth phenotypes mirror observed effects in mammals, where canonical Wnt has been implicated as an upstream regulator of enamel knot signalling. In silico modelling of shark dental morphogenesis demonstrates how subtle changes in activatory and inhibitory signals can alter tooth shape, resembling developmental phenotypes and cusp shapes observed following experimental Wnt perturbation. Our results support the functional conservation of an enamel knot-like signalling centre throughout vertebrates and suggest that varied tooth types from sharks to mammals follow a similar developmental bauplan. Lineage-specific differences in signalling are not sufficient in refuting homology of this signalling centre, which is likely older than teeth themselves.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Alexandre P Thiery

    Department of Animal and Plant Sciences, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Ariane S Standing

    Department of Biology, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Rory L Cooper

    Department of Genetics and Evolution, University of Geneva, Geneva, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0172-4708
  4. Gareth J Fraser

    Department of Biology, University of Florida, Gainesville, United States
    For correspondence
    g.fraser@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7376-0962

Funding

Natural Environment Research Council (NE/K014595/1)

  • Gareth J Fraser

Leverhulme Trust (RPG-211)

  • Gareth J Fraser

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mária Hovořáková

Publication history

  1. Preprint posted: August 16, 2021 (view preprint)
  2. Received: August 19, 2021
  3. Accepted: May 9, 2022
  4. Accepted Manuscript published: May 10, 2022 (version 1)

Copyright

© 2022, Thiery et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alexandre P Thiery
  2. Ariane S Standing
  3. Rory L Cooper
  4. Gareth J Fraser
(2022)
An epithelial signalling centre in sharks supports homology of tooth morphogenesis in vertebrates
eLife 11:e73173.
https://doi.org/10.7554/eLife.73173

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