Conservation of peripheral nervous system formation mechanisms in divergent ascidian embryos

  1. Joshua F Coulcher
  2. Agnès Roure
  3. Rafath Chowdhury
  4. Méryl Robert
  5. Laury Lescat
  6. Aurélie Bouin
  7. Juliana Carvajal Cadavid
  8. Hiroki Nishida
  9. Sébastien Darras  Is a corresponding author
  1. CNRS, France
  2. Albert Einstein college of medicine, United States
  3. Osaka University, Japan

Abstract

Ascidians with very similar embryos but highly divergent genomes are thought to have undergone extensive developmental system drift. We compared, in four species (Ciona and Phallusia for Phlebobranchia, Molgula and Halocynthia for Stolidobranchia), gene expression and gene regulation for a network of six transcription factors regulating peripheral nervous system (PNS) formation in Ciona. All genes, but one in Molgula, were expressed in the PNS with some differences correlating with phylogenetic distance. Cross-species transgenesis indicated strong levels of conservation, except in Molgula, in gene regulation despite lack of sequence conservation of the enhancers. Developmental system drift in ascidians is thus higher for gene regulation than for gene expression; and is impacted not only by phylogenetic distance, but also in a clade-specific manner and unevenly within a network. Finally, considering that Molgula is divergent in our analyses, this suggests deep conservation of developmental mechanisms in ascidians after 390 My of separate evolution.

Data availability

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

Article and author information

Author details

  1. Joshua F Coulcher

    BIOM, CNRS, Banyuls-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Agnès Roure

    BIOM, CNRS, Banyuls-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Rafath Chowdhury

    BIOM, CNRS, Banyuls-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Méryl Robert

    BIOM, CNRS, Banyuls-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Laury Lescat

    dept of Developmental and molecular Biology, Albert Einstein college of medicine, Bronx, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Aurélie Bouin

    BIOM, CNRS, Banyuls-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Juliana Carvajal Cadavid

    BIOM, CNRS, Banyuls-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Hiroki Nishida

    Department of Biological Sciences, Osaka University, Toyonaka, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7249-1668
  9. Sébastien Darras

    BIOM, CNRS, Banyuls-sur-mer, France
    For correspondence
    sebastien.darras@obs-banyuls.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0590-0062

Funding

Agence Nationale de la Recherche (ANR-11-JSV2-007)

  • Sébastien Darras

Agence Nationale de la Recherche (ANR-17-CE13-0027)

  • Sébastien Darras

Fondation des Treilles

  • Joshua F Coulcher

Centre National de la Recherche Scientifique (DBM2020)

  • Sébastien Darras

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

Reviewing Editor

  1. Shigehiro Kuraku, RIKEN Center for Biosystems Dynamics Research, Japan

Publication history

  1. Received: May 21, 2020
  2. Accepted: November 13, 2020
  3. Accepted Manuscript published: November 16, 2020 (version 1)
  4. Version of Record published: December 2, 2020 (version 2)

Copyright

© 2020, Coulcher 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. Joshua F Coulcher
  2. Agnès Roure
  3. Rafath Chowdhury
  4. Méryl Robert
  5. Laury Lescat
  6. Aurélie Bouin
  7. Juliana Carvajal Cadavid
  8. Hiroki Nishida
  9. Sébastien Darras
(2020)
Conservation of peripheral nervous system formation mechanisms in divergent ascidian embryos
eLife 9:e59157.
https://doi.org/10.7554/eLife.59157

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