Serotonin signaling by maternal neurons upon stress ensures progeny survival

Abstract

Germ cells are vulnerable to stress. Therefore, how organisms protect their future progeny from damage in a fluctuating environment is a fundamental question in biology. We show that in Caenorhabditis elegans, serotonin released by maternal neurons during stress ensures the viability and stress resilience of future offspring. Serotonin acts through a signal transduction pathway conserved between C. elegans and mammalian cells to enable the transcription factor HSF1 to alter chromatin in soon-to-be fertilized germ cells by recruiting the histone chaperone FACT, displacing histones, and initiating protective gene expression. Without serotonin release by maternal neurons, FACT is not recruited by HSF1 in germ cells, transcription occurs but is delayed, and progeny of stressed C. elegans mothers fail to complete development. These studies uncover a novel mechanism by which stress sensing by neurons is coupled to transcription response times of germ cells to protect future offspring.

Data availability

RNA-seq data have been deposited and available at https://www.ncbi.nlm.nih.gov/bioproject/PRJNA576016

The following data sets were generated

Article and author information

Author details

  1. Srijit Das

    Biology, The University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Felicia K Ooi

    Department of Biology, The University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4766-2477
  3. Johnny Cruz Corchado

    Department of Biology, The University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Leah C Fuller

    Biology, The University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Joshua A Weiner

    Biology, The University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3352-2847
  6. Veena Prahlad

    Biology, The University of Iowa, Iowa City, United States
    For correspondence
    veena-prahlad@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0413-6074

Funding

National Institutes of Health (AG 050653)

  • Veena Prahlad

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

Reviewing Editor

  1. Siu Sylvia Lee, Cornell University, United States

Version history

  1. Received: January 17, 2020
  2. Accepted: April 22, 2020
  3. Accepted Manuscript published: April 23, 2020 (version 1)
  4. Version of Record published: May 19, 2020 (version 2)

Copyright

© 2020, Das 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.

Metrics

  • 2,621
    views
  • 409
    downloads
  • 25
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Srijit Das
  2. Felicia K Ooi
  3. Johnny Cruz Corchado
  4. Leah C Fuller
  5. Joshua A Weiner
  6. Veena Prahlad
(2020)
Serotonin signaling by maternal neurons upon stress ensures progeny survival
eLife 9:e55246.
https://doi.org/10.7554/eLife.55246

Share this article

https://doi.org/10.7554/eLife.55246