The evolutionary origin of bilaterian smooth and striated myocytes

  1. Thibaut Brunet
  2. Antje HL Fischer
  3. Patrick RH Steinmetz
  4. Antonella Lauri
  5. Paola Bertucci
  6. Detlev Arendt  Is a corresponding author
  1. Howard Hughes Medical Institute, University of California, Berkeley, United States
  2. Ludwig-Maximilians University Munich, Germany
  3. University of Bergen, Norway
  4. Helmholtz Zentrum München, Germany
  5. European Molecular Biology Laboratory, Germany

Abstract

The dichotomy between smooth and striated myocytes is fundamental for bilaterian musculature, but its evolutionary origin is unsolved. In particular, interrelationships of visceral smooth muscles remain unclear. Absent in fly and nematode, they have not yet been characterized molecularly outside vertebrates. Here, we characterize expression profile, ultrastructure, contractility and innervation of the musculature in the marine annelid Platynereis dumerilii and identify smooth muscles around the midgut, hindgut and heart that resemble their vertebrate counterparts in molecular fingerprint, contraction speed, and nervous control. Our data suggest that both visceral smooth and somatic striated myocytes were present in the protostome-deuterostome ancestor, and that smooth myocytes later co-opted the striated contractile module repeatedly - for example in vertebrate heart evolution. During these smooth-to-striated myocyte conversions the core regulatory complex of transcription factors conveying myocyte identity remained unchanged, reflecting a general principle in cell type evolution.

Article and author information

Author details

  1. Thibaut Brunet

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1843-1613
  2. Antje HL Fischer

    Biochemistry, Ludwig-Maximilians University Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1843-1613
  3. Patrick RH Steinmetz

    Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  4. Antonella Lauri

    Institute for Biological and Medical Imaging, Helmholtz Zentrum München, München, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Paola Bertucci

    Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Detlev Arendt

    Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    For correspondence
    arendt@embl.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7833-050X

Funding

European Research Council (Brain Evo-Devo)

  • Thibaut Brunet
  • Paola Bertucci
  • Detlev Arendt

European Union's Seventh Framework Program (EVONET)

  • Antonella Lauri

European Union-Marie Curie Early Training Network (ZOONET)

  • Antje HL Fischer

European Molecular Biology Laboratory (International PhD Program)

  • Thibaut Brunet
  • Antje HL Fischer
  • Patrick RH Steinmetz
  • Antonella Lauri

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

Reviewing Editor

  1. Alejandro Sánchez Alvarado, Stowers Institute for Medical Research, United States

Publication history

  1. Received: August 24, 2016
  2. Accepted: December 1, 2016
  3. Accepted Manuscript published: December 1, 2016 (version 1)
  4. Accepted Manuscript updated: December 2, 2016 (version 2)
  5. Version of Record published: December 19, 2016 (version 3)

Copyright

© 2016, Brunet 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

  • 4,841
    Page views
  • 874
    Downloads
  • 47
    Citations

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

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. Thibaut Brunet
  2. Antje HL Fischer
  3. Patrick RH Steinmetz
  4. Antonella Lauri
  5. Paola Bertucci
  6. Detlev Arendt
(2016)
The evolutionary origin of bilaterian smooth and striated myocytes
eLife 5:e19607.
https://doi.org/10.7554/eLife.19607