Diversification of the Caenorhabditis heat shock response by Helitron transposable elements
- University of California, San Diego, United States
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.
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C. elegans and C. briggsae HS RNAseqNCBI Gene Expression Omnibus, GSE135987.
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H3K27me3 ChIP from L3 stagemodMine, modEncode_5051.
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Release 20180527All available isotypes.
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HSF-1 ChIPNCBI Gene Expression Omnibus, GSE81523.
Article and author information
Author details
Matthew D Daugherty
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
- Christian R Landry, Université Laval, Canada
Version history
- Received: August 16, 2019
- Accepted: December 10, 2019
- Accepted Manuscript published: December 11, 2019 (version 1)
- 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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Diversification of the Caenorhabditis heat shock response by Helitron transposable elements
eLife 8:e51139.
https://doi.org/10.7554/eLife.51139
Further reading
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