The enteric nervous system of the C. elegans pharynx is specified by the Sine oculis-like homeobox gene ceh-34

  1. Berta Vidal
  2. Burcu Gulez
  3. Wen Xi Cao
  4. Eduardo Leyva-Diaz
  5. Molly B Reilly
  6. Tessa Tekieli
  7. Oliver Hobert  Is a corresponding author
  1. Columbia University, Howard Hughes Medical Institute, United States

Abstract

Overarching themes in the terminal differentiation of the enteric nervous system, an autonomously acting unit of animal nervous systems, have so far eluded discovery. We describe here the overall regulatory logic of enteric nervous system differentiation of the nematode Caenorhabditis elegans that resides within the foregut (pharynx) of the worm. A C. elegans homolog of the Drosophila Sine oculis homeobox gene, ceh-34, is expressed in all 14 classes of interconnected pharyngeal neurons from their birth throughout their life time, but in no other neuron type of the entire animal. Constitutive and temporally controlled ceh-34 removal shows that ceh-34 is required to initiate and maintain the neuron type-specific terminal differentiation program of all pharyngeal neuron classes, including their circuit assembly. Through additional genetic loss of function analysis, we show that within each pharyngeal neuron class, ceh-34 cooperates with different homeodomain transcription factors to individuate distinct pharyngeal neuron classes. Our analysis underscores the critical role of homeobox genes in neuronal identity specification and links them to the control of neuronal circuit assembly of the enteric nervous system. Together with the pharyngeal nervous system simplicity as well as its specification by a Sine oculis homolog, our findings invite speculations about the early evolution of nervous systems.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Berta Vidal

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Burcu Gulez

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Wen Xi Cao

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Eduardo Leyva-Diaz

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Molly B Reilly

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, 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:" 0000-0002-7180-7763
  6. Tessa Tekieli

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Oliver Hobert

    Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, United States
    For correspondence
    or38@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7634-2854

Funding

Howard Hughes Medical Institute (N/A)

  • Oliver Hobert

National Institutes of Health (R01 NS039996)

  • Oliver Hobert

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

Reviewing Editor

  1. Douglas Portman, University of Rochester, United States

Publication history

  1. Preprint posted: December 1, 2021 (view preprint)
  2. Received: December 1, 2021
  3. Accepted: March 23, 2022
  4. Accepted Manuscript published: March 24, 2022 (version 1)
  5. Version of Record published: April 7, 2022 (version 2)

Copyright

© 2022, Vidal 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. Berta Vidal
  2. Burcu Gulez
  3. Wen Xi Cao
  4. Eduardo Leyva-Diaz
  5. Molly B Reilly
  6. Tessa Tekieli
  7. Oliver Hobert
(2022)
The enteric nervous system of the C. elegans pharynx is specified by the Sine oculis-like homeobox gene ceh-34
eLife 11:e76003.
https://doi.org/10.7554/eLife.76003

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