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

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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

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Todd A Starich

Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, United States

Competing interests
The authors declare that no competing interests exist.
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.

"This ORCID iD identifies the author of this article:" 0000-0001-8179-8162
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.

"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.

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.