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.

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

  • 6,206
    views
  • 1,001
    downloads
  • 89
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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

Share this article

https://doi.org/10.7554/eLife.19607

Further reading

    1. Developmental Biology
    Yanlin Hou, Zhengwen Nie ... Hans R Scholer
    Research Article

    During the first lineage segregation, mammalian embryos generate the inner cell mass (ICM) and trophectoderm (TE). ICM gives rise to the epiblast (EPI) that forms all cell types of the body, an ability referred to as pluripotency. The molecular mechanisms that induce pluripotency in embryos remain incompletely elucidated. Using knockout (KO) mouse models in conjunction with low-input ATAC-seq and RNA-seq, we found that Oct4 and Sox2 gradually come into play in the early ICM, coinciding with the initiation of Sox2 expression. Oct4 and Sox2 activate the pluripotency-related genes through the putative OCT-SOX enhancers in the early ICM. Furthermore, we observed a substantial reorganization of chromatin landscape and transcriptome from the morula to the early ICM stages, which was partially driven by Oct4 and Sox2, highlighting their pivotal role in promoting the developmental trajectory toward the ICM. Our study provides new insights into the establishment of the pluripotency network in mouse preimplantation embryos.

    1. Developmental Biology
    2. Neuroscience
    Maria I Lazaro-Pena, Carlos A Diaz-Balzac
    Insight

    The ligand Netrin mediates axon guidance through a combination of haptotaxis over short distances and chemotaxis over longer distances.