Abstract

Gene regulatory networks coordinate the formation of organs and structures that compose the evolving body plans of different organisms. We are using a simple chordate model, the Ciona embryo, to investigate the essential gene regulatory network that orchestrates morphogenesis of the notochord, a structure necessary for the proper development of all chordate embryos. Although numerous transcription factors expressed in the notochord have been identified in different chordates, several of them remain to be positioned within a regulatory framework. Here we focus on Xbp1, a transcription factor expressed during notochord formation in Ciona and other chordates. Through the identification of Xbp1-downstream notochord genes in Ciona, we found evidence of the early co-option of genes involved in the unfolded protein response to the notochord developmental program. We report the regulatory interplay between Xbp1 and Brachyury, and by extending these results to Xenopus, we show that Brachyury and Xbp1 form a cross-regulatory subcircuit of the notochord gene regulatory network that has been consolidated during chordate evolution.

Data availability

The complete dataset has been deposited into the NCBI Gene Expression Omnibus, under accession number GSE46751

The following data sets were generated

Article and author information

Author details

  1. Yushi Wu

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Arun Devotta

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Diana S José-Edwards

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jamie E Kugler

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Lenny J Negrón-Piñeiro

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Karina Braslavskaya

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jermyn Addy

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jean-Pierre Saint-Jeannet

    Department of Molecular Pathobiology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3259-2103
  9. Anna Di Gregorio

    Department of Molecular Pathobiology, New York University, New York, United States
    For correspondence
    adg13@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4089-7484

Funding

National Institutes of Health (R03HD098395)

  • Yushi Wu
  • Arun Devotta
  • Diana S José-Edwards
  • Jamie E Kugler
  • Lenny J Negrón-Piñeiro
  • Karina Braslavskaya
  • Jermyn Addy
  • Anna Di Gregorio

National Institutes of Health (graduate student training grant,T32HD007520)

  • Lenny J Negrón-Piñeiro

National Institutes of Health (graduate student training grant,T32GM008539)

  • Diana S José-Edwards

National Institutes of Health (Administrative supplement R03HD098395-02S1)

  • Lenny J Negrón-Piñeiro

New York University Center for Skeletal and Craniofacial Biology (Pilot grant)

  • Yushi Wu
  • Arun Devotta
  • Diana S José-Edwards
  • Jamie E Kugler
  • Lenny J Negrón-Piñeiro
  • Karina Braslavskaya
  • Jermyn Addy
  • Jean-Pierre Saint-Jeannet
  • Anna Di Gregorio

National Institutes of Health (Center Core Grant for the NYU CSCB 1P30DE020754)

  • Jean-Pierre Saint-Jeannet

National Institutes of Health (Center Grant for NYU Langone Health DART Microscopy Laboratory P30CA016087)

  • Yushi Wu
  • Anna Di Gregorio

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

Ethics

Animal experimentation: Procedure minimizing discomfort and pain - only applicable to XenopusThe collection of eggs from females primed with chorionic gonadotropin hormone requires minimum procedures occasioning virtually no pain or suffering. Surgical dissection of the testes is performed on euthanized males (see below), preventing discomfort.Methods of euthanasiaMale frogs will be euthanized during the procedure, in a two-step process. They will be initially anesthetized by immersion into a solution of ethyl amino benzoate (tricaine/MS222) and then a pithing procedure of the brain and the spinal cord will be used to terminate the animal. After pithing, respiration ceases signaling death. Female frogs will be euthanized in a similar manner when no longer producing viable eggs or appear ill.

Reviewing Editor

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

Version history

  1. Received: September 17, 2021
  2. Accepted: January 19, 2022
  3. Accepted Manuscript published: January 20, 2022 (version 1)
  4. Version of Record published: January 31, 2022 (version 2)

Copyright

© 2022, Wu 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.

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  1. Yushi Wu
  2. Arun Devotta
  3. Diana S José-Edwards
  4. Jamie E Kugler
  5. Lenny J Negrón-Piñeiro
  6. Karina Braslavskaya
  7. Jermyn Addy
  8. Jean-Pierre Saint-Jeannet
  9. Anna Di Gregorio
(2022)
Xbp1 and Brachyury establish an evolutionarily conserved subcircuit of the notochord gene regulatory network
eLife 11:e73992.
https://doi.org/10.7554/eLife.73992

Share this article

https://doi.org/10.7554/eLife.73992

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