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.

Data availability

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.

Metrics

  • 2,228
    Page views
  • 535
    Downloads
  • 29
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Developmental Biology
    Greta Rossi, Gabriele Ordazzo ... Vania Broccoli
    Research Article Updated

    Wolfram syndrome 1 (WS1) is a rare genetic disorder caused by mutations in the WFS1 gene leading to a wide spectrum of clinical dysfunctions, among which blindness, diabetes, and neurological deficits are the most prominent. WFS1 encodes for the endoplasmic reticulum (ER) resident transmembrane protein wolframin with multiple functions in ER processes. However, the WFS1-dependent etiopathology in retinal cells is unknown. Herein, we showed that Wfs1 mutant mice developed early retinal electrophysiological impairments followed by marked visual loss. Interestingly, axons and myelin disruption in the optic nerve preceded the degeneration of the retinal ganglion cell bodies in the retina. Transcriptomics at pre-degenerative stage revealed the STAT3-dependent activation of proinflammatory glial markers with reduction of the homeostatic and pro-survival factors glutamine synthetase and BDNF. Furthermore, label-free comparative proteomics identified a significant reduction of the monocarboxylate transport isoform 1 (MCT1) and its partner basigin that are highly enriched on retinal glia and myelin-forming oligodendrocytes in optic nerve together with wolframin. Loss of MCT1 caused a failure in lactate transfer from glial to neuronal cell bodies and axons leading to a chronic hypometabolic state. Thus, this bioenergetic impairment is occurring concurrently both within the axonal regions and cell bodies of the retinal ganglion cells, selectively endangering their survival while impacting less on other retinal cells. This metabolic dysfunction occurs months before the frank RGC degeneration suggesting an extended time-window for intervening with new therapeutic strategies focused on boosting retinal and optic nerve bioenergetics in WS1.

    1. Developmental Biology
    Kavitha Chinnaiya, Sarah Burbridge ... Marysia Placzek
    Research Article

    The tuberal hypothalamus controls life-supporting homeostatic processes, but despite its fundamental role, the cells and signalling pathways that specify this unique region of the CNS in embryogenesis are poorly characterised. Here we combine experimental and bioinformatic approaches in the embryonic chick to show that the tuberal hypothalamus is progressively generated from hypothalamic floor plate-like cells. Fate-mapping studies show that a stream of tuberal progenitors develops in the anterior-ventral neural tube as a wave of neuroepithelial-derived BMP signalling sweeps from anterior to posterior through the hypothalamic floor plate. As later-specified posterior tuberal progenitors are generated, early-specified anterior tuberal progenitors become progressively more distant from these BMP signals and differentiate into tuberal neurogenic cells. Gain- and loss-of-function experiments in vivo and ex vivo show that BMP signalling initiates tuberal progenitor specification, but must be eliminated for these to progress to anterior neurogenic progenitors. ScRNA-Seq profiling shows that tuberal progenitors that are specified after the major period of anterior tuberal specification begin to upregulate genes that characterise radial glial cells. This study provides an integrated account of the development of the tuberal hypothalamus.