Pattern regulation in a regenerating jellyfish

  1. Chiara Sinigaglia  Is a corresponding author
  2. Sophie Peron
  3. Jeanne Eichelbrenner
  4. Sandra Chevalier
  5. Julia Steger
  6. Carine Barreau
  7. Evelyn Houliston
  8. Lucas Leclère  Is a corresponding author
  1. ENS Lyon, France
  2. Sorbonne Université, France
  3. University of Vienna, Austria

Abstract

Clytia hemisphaerica jellyfish, with their tetraradial symmetry, offer a novel paradigm for addressing patterning mechanisms during regeneration. Here we show that an interplay between mechanical forces, cell migration and proliferation allows jellyfish fragments to regain shape and functionality rapidly, notably by efficient restoration of the central feeding organ (manubrium). Fragmentation first triggers actomyosin-powered remodeling that restores body umbrella shape, causing radial smooth muscle fibers to converge around 'hubs' which serve as positional landmarks. Stabilization of these hubs, and associated expression of Wnt6, depends on the configuration of the adjoining muscle fiber 'spokes'. Stabilized hubs presage the site of the manubrium blastema, whose growth is Wnt/β-catenin dependent and fueled by both cell proliferation and long-range cell recruitment. Manubrium morphogenesis is modulated by its connections with the gastrovascular canal system. We conclude that body patterning in regenerating jellyfish emerges mainly from local interactions, triggered and directed by the remodeling process.

Data availability

Transcriptomic data are being deposited in ENA (EBI) - accession code PRJEB37920. All other data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Chiara Sinigaglia

    Institut de Genomique Fonctionelle de Lyon, ENS Lyon, Lyon, France
    For correspondence
    chi.sinigaglia@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7195-7091
  2. Sophie Peron

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeanne Eichelbrenner

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Sandra Chevalier

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Julia Steger

    Molecular Evolution and Development, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  6. Carine Barreau

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Evelyn Houliston

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9264-2585
  8. Lucas Leclère

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    For correspondence
    lucas.leclere@obs-vlfr.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7440-0467

Funding

Agence Nationale de la Recherche (ANR-13-PDOC-0016)

  • Lucas Leclère

Agence Nationale de la Recherche (ANR-19-CE13-0003)

  • Lucas Leclère

Fondation pour la Recherche Médicale (FDT201805005536)

  • Sophie Peron

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

Reviewing Editor

  1. Phillip A Newmark, Morgridge Institute for Research, United States

Publication history

  1. Received: March 24, 2020
  2. Accepted: September 5, 2020
  3. Accepted Manuscript published: September 7, 2020 (version 1)
  4. Version of Record published: September 29, 2020 (version 2)

Copyright

© 2020, Sinigaglia 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

  • 4,201
    Page views
  • 421
    Downloads
  • 14
    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)

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. Chiara Sinigaglia
  2. Sophie Peron
  3. Jeanne Eichelbrenner
  4. Sandra Chevalier
  5. Julia Steger
  6. Carine Barreau
  7. Evelyn Houliston
  8. Lucas Leclère
(2020)
Pattern regulation in a regenerating jellyfish
eLife 9:e54868.
https://doi.org/10.7554/eLife.54868

Further reading

    1. Developmental Biology
    2. Neuroscience
    Mariah L Hoye et al.
    Research Article

    Mutations in the RNA helicase, DDX3X, are a leading cause of Intellectual Disability and present as DDX3X syndrome, a neurodevelopmental disorder associated with cortical malformations and autism. Yet, the cellular and molecular mechanisms by which DDX3X controls cortical development are largely unknown. Here, using a mouse model of Ddx3x loss-of-function we demonstrate that DDX3X directs translational and cell cycle control of neural progenitors, which underlies precise corticogenesis. First, we show brain development is sensitive to Ddx3x dosage; complete Ddx3x loss from neural progenitors causes microcephaly in females, whereas hemizygous males and heterozygous females show reduced neurogenesis without marked microcephaly. In addition, Ddx3x loss is sexually dimorphic, as its paralog, Ddx3y, compensates for Ddx3x in the developing male neocortex. Using live imaging of progenitors, we show that DDX3X promotes neuronal generation by regulating both cell cycle duration and neurogenic divisions. Finally, we use ribosome profiling in vivo to discover the repertoire of translated transcripts in neural progenitors, including those which are DDX3X-dependent and essential for neurogenesis. Our study reveals invaluable new insights into the etiology of DDX3X syndrome, implicating dysregulated progenitor cell cycle dynamics and translation as pathogenic mechanisms.

    1. Developmental Biology
    2. Evolutionary Biology
    Mathi Thiruppathy et al.
    Short Report

    Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental gata3 dependence with the gills. Combined with work in chondrichthyans, our findings in a teleost fish point to the presence of a mandibular pseudobranch with serial homology to gills in the last common ancestor of jawed vertebrates, consistent with a gill origin of vertebrate jaws.