Gap junctions deliver malonyl-CoA from soma to germline to support embryogenesis in Caenorhabditis elegans

  1. Todd A Starich
  2. Xiaofei Bai
  3. David Greenstein  Is a corresponding author
  1. University of Minnesota, United States
  2. National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, United States

Abstract

Gap junctions are ubiquitous in metazoans and play critical roles in important biological processes, including electrical conduction and development. Yet, only a few defined molecules passing through gap junction channels have been linked to specific functions. We isolated gap junction channel mutants that reduce coupling between the soma and germ cells in the C. elegans gonad. We provide evidence that malonyl-CoA, the rate-limiting substrate for fatty acid synthesis (FAS), is produced in the soma and delivered through gap junctions to the germline; there it is used in fatty acid synthesis to critically support embryonic development. Separation of malonyl-CoA production from its site of utilization facilitates somatic control of germline development. Additionally, we demonstrate that loss of malonyl-CoA production in the intestine negatively impacts germline development independently of FAS. Our results suggest that metabolic outsourcing of malonyl-CoA may be a strategy by which the soma communicates nutritional status to the germline.

Data availability

All C. elegans strains are available from the Caenorhabditis Genetics Center or by request. All data supporting the findings of this study are contained within the manuscript, figures tables, or source data provided.

Article and author information

Author details

  1. Todd A Starich

    Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiaofei Bai

    National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8179-8162
  3. David Greenstein

    Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, United States
    For correspondence
    green959@umn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8189-2087

Funding

National Institutes of Health (GM57173)

  • David Greenstein

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

Reviewing Editor

  1. Michael Buszczak, University of Texas Southwestern Medical Center, United States

Publication history

  1. Received: May 6, 2020
  2. Accepted: July 30, 2020
  3. Accepted Manuscript published: July 31, 2020 (version 1)
  4. Version of Record published: August 24, 2020 (version 2)

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. Todd A Starich
  2. Xiaofei Bai
  3. David Greenstein
(2020)
Gap junctions deliver malonyl-CoA from soma to germline to support embryogenesis in Caenorhabditis elegans
eLife 9:e58619.
https://doi.org/10.7554/eLife.58619

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