Opposing roles for Bmp signalling during the development of electrosensory lateral line organs

  1. Alexander S Campbell
  2. Martin Minařík
  3. Roman Franěk
  4. Michaela Vazačová
  5. Miloš Havelka
  6. David Gela
  7. Martin Pšenička
  8. Clare VH Baker  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. University of South Bohemia in České Budějovice, Czech Republic

Abstract

The lateral line system enables fishes and aquatic-stage amphibians to detect local water movement via mechanosensory hair cells in neuromasts, and many species to detect weak electric fields via electroreceptors (modified hair cells) in ampullary organs. Both neuromasts and ampullary organs develop from lateral line placodes, but the molecular mechanisms underpinning ampullary organ formation are understudied relative to neuromasts. This is because the ancestral lineages of zebrafish (teleosts) and Xenopus (frogs) independently lost electroreception. We identified Bmp5 as a promising candidate via differential RNA-seq in an electroreceptive ray-finned fish, the Mississippi paddlefish (Polyodon spathula; Modrell et al., 2017, eLife 6: e24197). In an experimentally tractable relative, the sterlet sturgeon (Acipenser ruthenus), we found that Bmp5 and four other Bmp pathway genes are expressed in the developing lateral line, and that Bmp signalling is active. Furthermore, CRISPR/Cas9-mediated mutagenesis targeting Bmp5 in G0-injected sterlet embryos resulted in fewer ampullary organs. Conversely, when Bmp signalling was inhibited by DMH1 treatment shortly before the formation of ampullary organ primordia, supernumerary ampullary organs developed. These data suggest that Bmp5 promotes ampullary organ development, whereas Bmp signalling via another ligand(s) prevents their overproduction. Taken together, this demonstrates opposing roles for Bmp signalling during ampullary organ formation.

Data availability

Previously published sterlet transcriptome assemblies (from pooled stage 40-45 sterlet heads; Minařík et al., 2024a) are available at DDBJ/EMBL/GenBank under the accessions GKLU00000000 (https://www.ncbi.nlm.nih.gov/nuccore/GKLU00000000) and GKEF01000000 (https://www.ncbi.nlm.nih.gov/nuccore/GKEF00000000.1). Previously published paddlefish RNA-seq data (from pooled paddlefish opercula and fin tissue at stage 46; Modrell et al., 2017a) are available via the NCBI Gene Expression Omnibus (GEO) database (https://www.ncbi.nlm.nih.gov/geo/) under accession code GSE92470.

The following previously published data sets were used

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0009-0003-1539-214X
  2. Martin Minařík

    Department of Physiology, Development and Neuroscience, 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:" 0000-0001-6660-0031
  3. Roman Franěk

    Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3464-1872
  4. Michaela Vazačová

    Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  5. Miloš Havelka

    Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. David Gela

    Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  7. Martin Pšenička

    Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  8. 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

Anatomical Society (Research Studentship)

  • Alexander S Campbell
  • Clare VH Baker

Biotechnology and Biological Sciences Research Council (BB/P001947/1)

  • Clare VH Baker

Cambridge Philosophical Society (Research Studentship)

  • Alexander S Campbell

Cambridge Isaac Newton Trust (Grant 20.07(c))

  • Clare VH Baker

Ministry of Education, Youth and Sports of the Czech Republic (projects CENAKVA (LM2018099) and Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370))

  • Roman Franěk
  • Michaela Vazačová
  • Martin Pšenička

Czech Science Foundation (project 22-31141J)

  • Roman Franěk
  • Michaela Vazačová
  • Martin Pšenička

School of the Biological Sciences, University of Cambridge

  • Martin Minařík

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

Ethics

Animal experimentation: Sterlet animal work was reviewed and approved by The Animal Research Committee of Research Institute of Fish Culture and Hydrobiology, Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic and Ministry of Agriculture of the Czech Republic (MSMT-12550/2016-3). Experimental fish were maintained according to the principles of the European Union (EU) Harmonized Animal Welfare Act of the Czech Republic, and Principles of Laboratory Animal Care and National Laws 246/1992 "Animal Welfare" on the protection of animals.

Copyright

© 2025, Campbell et al.

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

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  1. Alexander S Campbell
  2. Martin Minařík
  3. Roman Franěk
  4. Michaela Vazačová
  5. Miloš Havelka
  6. David Gela
  7. Martin Pšenička
  8. Clare VH Baker
(2025)
Opposing roles for Bmp signalling during the development of electrosensory lateral line organs
eLife 14:e99798.
https://doi.org/10.7554/eLife.99798

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https://doi.org/10.7554/eLife.99798

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