A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian
- National University of Ireland, Galway, Ireland
- University of Florida, United States
- 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.
Article and author information
Author details
Sebastian G Gornik
Miguel Salinas-Saavedra
Christine E Schnitzler
Andreas D Baxevanis
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
- Marianne E Bronner, California Institute of Technology, United States
Version history
- Preprint posted: March 24, 2022 (view preprint)
- Received: March 28, 2022
- Accepted: May 23, 2022
- Accepted Manuscript published: May 24, 2022 (version 1)
- Version of Record published: June 7, 2022 (version 2)
- 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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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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