1. Genetics and Genomics

Diversification of the Caenorhabditis heat shock response by Helitron transposable elements

  1. Jacob M Garrigues
  2. Brian V Tsu
  3. Matthew D Daugherty
  4. Amy E Pasquinelli  Is a corresponding author
  1. University of California, San Diego, United States
https://doi.org/10.7554/eLife.51139
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  1. Jacob M Garrigues
  2. Brian V Tsu
  3. Matthew D Daugherty
  4. Amy E Pasquinelli
(2019)
Diversification of the Caenorhabditis heat shock response by Helitron transposable elements
eLife 8:e51139.
https://doi.org/10.7554/eLife.51139
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Abstract

Heat Shock Factor 1 (HSF-1) is a key regulator of the heat shock response (HSR). Upon heat shock, HSF-1 binds well-conserved motifs, called Heat Shock Elements (HSEs), and drives expression of genes important for cellular protection during this stress. Remarkably, we found that substantial numbers of HSEs in multiple Caenorhabditis species reside within Helitrons, a type of DNA transposon. Consistent with Helitron-embedded HSEs being functional, upon heat shock they display increased HSF-1 and RNA polymerase II occupancy and up-regulation of nearby genes in C. elegans. Interestingly, we found that different genes appear to be incorporated into the HSR by species-specific Helitron insertions in C. elegans and C. briggsae and by strain-specific insertions among different wild isolates of C. elegans. Our studies uncover previously unidentified targets of HSF-1 and show that Helitron insertions are responsible for rewiring and diversifying the Caenorhabditis HSR.

Data availability

The RNA-seq datasets generated in this study are available at the Gene Expression Omnibus (GEO) under accession number GSE135987.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Jacob M Garrigues

    Division of Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Brian V Tsu

    Division of Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Matthew D Daugherty

    Division of Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4879-9603

  4. Amy E Pasquinelli

    Division of Biology, University of California, San Diego, La Jolla, United States
    For correspondence
    apasquinelli@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9511-0039

Funding

National Institute of General Medical Sciences (R35 GM127012)

  • Amy E Pasquinelli

National Institute of General Medical Sciences (GM133633)

  • Matthew D Daugherty

National Cancer Institute (T32 CA009523)

  • Jacob M Garrigues

National Institute of General Medical Sciences (T32 GM007240)

  • Brian V Tsu

Pew Charitable Trusts

  • Matthew D Daugherty

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

Reviewing Editor

  1. Christian R Landry, Université Laval, Canada

Version history

  1. Received: August 16, 2019
  2. Accepted: December 10, 2019
  3. Accepted Manuscript published: December 11, 2019 (version 1)
  4. Version of Record published: December 23, 2019 (version 2)

Copyright

© 2019, Garrigues 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. Jacob M Garrigues
  2. Brian V Tsu
  3. Matthew D Daugherty
  4. Amy E Pasquinelli
(2019)
Diversification of the Caenorhabditis heat shock response by Helitron transposable elements
eLife 8:e51139.
https://doi.org/10.7554/eLife.51139

Share this article

https://doi.org/10.7554/eLife.51139

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