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

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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.

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.

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  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

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