1. Developmental Biology
  2. Evolutionary Biology
Download icon

Bichir external gills arise via heterochronic shift that accelerates hyoid arch development

  1. Jan Stundl
  2. Anna Pospisilova
  3. David Jandzik
  4. Peter Fabian
  5. Barbora Dobiasova
  6. Martin Minarik
  7. Brian D Metscher
  8. Vladimir Soukup  Is a corresponding author
  9. Robert Cerny  Is a corresponding author
  1. Charles University in Prague, Czech Republic
  2. University of Vienna, Austria
Research Article
  • Cited 4
  • Views 2,060
  • Annotations
Cite this article as: eLife 2019;8:e43531 doi: 10.7554/eLife.43531

Abstract

In most vertebrates, pharyngeal arches form in a stereotypic anterior-to-posterior progression. To gain insight into the mechanisms underlying evolutionary changes in pharyngeal arch development, here we investigate embryos and larvae of bichirs. Bichirs represent the earliest diverged living group of ray-finned fishes, and possess intriguing traits otherwise typical for lobe-finned fishes such as ventral paired lungs and larval external gills. In bichir embryos, we find that the anteroposterior way of formation of cranial segments is modified by the unique acceleration of the entire hyoid arch segment, with earlier and orchestrated development of the endodermal, mesodermal, and neural crest tissues. This major heterochronic shift in the anteroposterior developmental sequence enables early appearance of the external gills that represent key breathing organs of bichir free-living embryos and early larvae. Bichirs thus stay as unique models for understanding developmental mechanisms facilitating increased breathing capacity.

Article and author information

Author details

  1. Jan Stundl

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  2. Anna Pospisilova

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  3. David Jandzik

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  4. Peter Fabian

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  5. Barbora Dobiasova

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. Martin Minarik

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    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
  7. Brian D Metscher

    Department of Theoretical Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  8. Vladimir Soukup

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    For correspondence
    vladimir.soukup@natur.cuni.cz
    Competing interests
    The authors declare that no competing interests exist.
  9. Robert Cerny

    Department of Zoology, Charles University in Prague, Prague, Czech Republic
    For correspondence
    robert.cerny@natur.cuni.cz
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0022-0199

Funding

Charles University Grant Agency (1448514)

  • Jan Stundl

Charles University Grant Agency (640016)

  • Anna Pospisilova

Charles University Grant Agency (220213)

  • Martin Minarik

Czech Science Foundation (16-23836S)

  • Robert Cerny

Charles University Grant Agency (726516)

  • Martin Minarik

The Charles University grant SVV (260434/2019)

  • Jan Stundl
  • Anna Pospisilova
  • David Jandzik
  • Vladimir Soukup
  • Robert Cerny

The Charles University Research Centre program (204069)

  • Vladimir Soukup

The grant of the Scientific Grant Agency of Slovak Republic VEGA (1/0415/17)

  • David Jandzik

The European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant (751066)

  • David Jandzik

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

Reviewing Editor

  1. Tanya T Whitfield, University of Sheffield, United Kingdom

Publication history

  1. Received: November 9, 2018
  2. Accepted: March 15, 2019
  3. Accepted Manuscript published: March 26, 2019 (version 1)
  4. Version of Record published: March 29, 2019 (version 2)

Copyright

© 2019, Stundl 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

  • 2,060
    Page views
  • 194
    Downloads
  • 4
    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)

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

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

Further reading

    1. Developmental Biology
    2. Neuroscience
    Yasmine Cantaut-Belarif et al.
    Research Article Updated

    The cerebrospinal fluid (CSF) contains an extracellular thread conserved in vertebrates, the Reissner fiber, which controls body axis morphogenesis in the zebrafish embryo. Yet, the signaling cascade originating from this fiber to ensure body axis straightening is not understood. Here, we explore the functional link between the Reissner fiber and undifferentiated spinal neurons contacting the CSF (CSF-cNs). First, we show that the Reissner fiber is required in vivo for the expression of urp2, a neuropeptide expressed in CSF-cNs. We show that the Reissner fiber is also required for embryonic calcium transients in these spinal neurons. Finally, we study how local adrenergic activation can substitute for the Reissner fiber-signaling pathway to CSF-cNs and rescue body axis morphogenesis. Our results show that the Reissner fiber acts on CSF-cNs and thereby contributes to establish body axis morphogenesis, and suggest it does so by controlling the availability of a chemical signal in the CSF.

    1. Cell Biology
    2. Developmental Biology
    Danielle Yi et al.
    Research Article

    Brown adipose tissue is a metabolically beneficial organ capable of dissipating chemical energy into heat, thereby increasing energy expenditure. Here, we identify Dot1l, the only known H3K79 methyltransferase, as an interacting partner of Zc3h10 that transcriptionally activates the Ucp1 promoter and other BAT genes. Through a direct interaction, Dot1l is recruited by Zc3h10 to the promoter regions of thermogenic genes to function as a coactivator by methylating H3K79. We also show that Dot1l is induced during brown fat cell differentiation and by cold exposure and that Dot1l and its H3K79 methyltransferase activity is required for thermogenic gene program. Furthermore, we demonstrate that Dot1l ablation in mice using Ucp1-Cre prevents activation of Ucp1 and other target genes to reduce thermogenic capacity and energy expenditure, promoting adiposity. Hence, Dot1l plays a critical role in the thermogenic program and may present as a future target for obesity therapeutics.