A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian

  1. Eleni Chrysostomou
  2. Hakima Flici
  3. Sebastian G Gornik
  4. Miguel Salinas-Saavedra
  5. James M Gahan
  6. Emma T McMahon
  7. Kerry Thompson
  8. Shirley Hanley
  9. Michelle Kincoyne
  10. Christine E Schnitzler
  11. Paul Gonzalez
  12. Andreas D Baxevanis
  13. Uri Frank  Is a corresponding author
  1. National University of Ireland, Galway, Ireland
  2. University of Florida, United States
  3. National Human Genome Research Institute, United States

Abstract

Neurogenesis is the generation of neurons from stem cells, a process that is regulated by SoxB transcription factors (TFs) in many animals. Although the roles of these TFs are well understood in bilaterians, how their neural function evolved is unclear. Here, we use Hydractinia symbiolongicarpus, a member of the early-branching phylum Cnidaria, to provide insight into this question. Using a combination of mRNA in situ hybridization, transgenesis, gene knockdown, transcriptomics, and in-vivo imaging, we provide a comprehensive molecular and cellular analysis of neurogenesis during embryogenesis, homeostasis, and regeneration in this animal. We show that SoxB genes act sequentially at least in some cases. Stem cells expressing Piwi1 and Soxb1, which have a broad developmental potential, become neural progenitors that express Soxb2 before differentiating into mature neural cells. Knockdown of SoxB genes resulted in complex defects in embryonic neurogenesis. Hydractinia neural cells differentiate while migrating from the aboral to the oral end of the animal, but it is unclear whether migration per se or exposure to different microenvironments is the main driver of their fate determination. Our data constitute a rich resource for studies aiming at addressing this question, which is at the heart of understanding the origin and development of animal nervous systems.

Data availability

The accession number for the RNA-seq datasets generated in this study is Sequence Read Archive (SRA): BioProjects PRJNA549873 (bulk RNA-seq) and PRJNA777228 (single cell RNA-seq). Accession numbers for each sample are listed in Table S2. The Hydractinia symbiolongicarpus genome is available through the NIH National Human Genome Research Institute (https://research.nhgri.nih.gov/hydractinia/). Corresponding data is archived in the NCBI Sequence Read Archive (SRA) under BioProject PRJNA807936.

The following data sets were generated

Article and author information

Author details

  1. Eleni Chrysostomou

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  2. Hakima Flici

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  3. Sebastian G Gornik

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8026-1336
  4. Miguel Salinas-Saavedra

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1598-9881
  5. James M Gahan

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  6. Emma T McMahon

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3933-8853
  7. Kerry Thompson

    Centre for Microscopy and Imaging, Discipline of Anatomy, School of Medicine, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2721-8977
  8. Shirley Hanley

    National Centre for Biomedical Engineering Science, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  9. Michelle Kincoyne

    Carbohydrate Signalling Group, National University of Ireland, Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  10. Christine E Schnitzler

    Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5001-6524
  11. Paul Gonzalez

    Computational and Statistical Genomics Branch, National Human Genome Research Institute, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Andreas D Baxevanis

    Computational and Statistical Genomics Branch, National Human Genome Research Institute, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5370-0014
  13. Uri Frank

    Centre for Chromosome Biology, National University of Ireland, Galway, Galway, Ireland
    For correspondence
    uri.frank@nuigalway.ie
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2094-6381

Funding

Wellcome Trust (210722/Z/18/Z)

  • Uri Frank

Science Foundation Ireland (11/PI/1020)

  • Uri Frank

National Science Foundation (1923259)

  • Uri Frank

National Science Foundation (1923259)

  • Christine E Schnitzler

National Human Genome Research Institute (ZIA HG000140)

  • Andy D Baxevanis

Science Foundation Ireland (13/SIRG/2125)

  • Sebastian G Gornik

Human Frontiers Science Program (LT000756/2020-L)

  • Miguel Salinas-Saavedra

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

Reviewing Editor

  1. Marianne E Bronner, California Institute of Technology, United States

Version history

  1. Preprint posted: March 24, 2022 (view preprint)
  2. Received: March 28, 2022
  3. Accepted: May 23, 2022
  4. Accepted Manuscript published: May 24, 2022 (version 1)
  5. Version of Record published: June 7, 2022 (version 2)
  6. Version of Record updated: January 6, 2023 (version 3)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Eleni Chrysostomou
  2. Hakima Flici
  3. Sebastian G Gornik
  4. Miguel Salinas-Saavedra
  5. James M Gahan
  6. Emma T McMahon
  7. Kerry Thompson
  8. Shirley Hanley
  9. Michelle Kincoyne
  10. Christine E Schnitzler
  11. Paul Gonzalez
  12. Andreas D Baxevanis
  13. Uri Frank
(2022)
A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian
eLife 11:e78793.
https://doi.org/10.7554/eLife.78793

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https://doi.org/10.7554/eLife.78793

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