Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome

  1. Melinda S Modrell
  2. Mike Lyne
  3. Adrian R Carr
  4. Harold H Zakon
  5. David Buckley
  6. Alexander S Campbell
  7. Marcus C Davis
  8. Gos Micklem
  9. Clare VH Baker  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. The University of Texas at Austin, United States
  3. Museo Nacional de Ciencias Naturales-MNCN-CSIC, Spain
  4. Kennesaw State University, United States

Abstract

The anamniote lateral line system, comprising mechanosensory neuromasts and electrosensory ampullary organs, is a useful model for investigating the developmental and evolutionary diversification of different organs and cell types. Zebrafish neuromast development is increasingly well understood, but neither zebrafish nor Xenopus is electroreceptive and our molecular understanding of ampullary organ development is rudimentary. We have used RNA-seq to generate a lateral line-enriched gene-set from late-larval paddlefish (Polyodon spathula). Validation of a subset reveals expression in developing ampullary organs of transcription factor genes critical for hair cell development, and genes essential for glutamate release at hair cell ribbon synapses, suggesting close developmental, physiological and evolutionary links between non-teleost electroreceptors and hair cells. We identify an ampullary organ-specific proneural transcription factor, and candidates for the voltage-sensing L-type Cav channel and rectifying Kv channel predicted from skate (cartilaginous fish) ampullary organ electrophysiology. Overall, our results illuminate ampullary organ development, physiology and evolution.

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The following data sets were generated

Article and author information

Author details

  1. Melinda S Modrell

    Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Mike Lyne

    Cambridge Systems Biology Centre, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Adrian R Carr

    Cambridge Systems Biology Centre, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Harold H Zakon

    Department of Neuroscience, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David Buckley

    Departmento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales-MNCN-CSIC, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexander S Campbell

    Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Marcus C Davis

    Department of Molecular and Cellular Biology, Kennesaw State University, Kennesaw, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2462-0138
  8. Gos Micklem

    Cambridge Systems Biology Centre, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6883-6168
  9. Clare VH Baker

    Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    cvhb1@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4434-3107

Funding

Biotechnology and Biological Sciences Research Council (BB/F00818X/1)

  • Clare VH Baker

Leverhulme Trust (RPG-383)

  • Clare VH Baker

Fisheries Society of the British Isles (Research Grant)

  • Melinda S Modrell

National Science Foundation (IOS 1557857)

  • Harold H Zakon

National Science Foundation (IOS 1144965)

  • Marcus C Davis

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

Ethics

Animal experimentation: All experiments were performed in accordance with the approved institutional guidelines and regulations of the Institutional Animal Care and Use Committee of Kennesaw State University (approved protocol #12-001).

Reviewing Editor

  1. Christine Petit, Institut Pasteur, France

Publication history

  1. Received: December 14, 2016
  2. Accepted: March 23, 2017
  3. Accepted Manuscript published: March 27, 2017 (version 1)
  4. Accepted Manuscript updated: March 31, 2017 (version 2)
  5. Accepted Manuscript updated: April 3, 2017 (version 3)
  6. Version of Record published: May 12, 2017 (version 4)

Copyright

© 2017, Modrell 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. Melinda S Modrell
  2. Mike Lyne
  3. Adrian R Carr
  4. Harold H Zakon
  5. David Buckley
  6. Alexander S Campbell
  7. Marcus C Davis
  8. Gos Micklem
  9. Clare VH Baker
(2017)
Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome
eLife 6:e24197.
https://doi.org/10.7554/eLife.24197
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