Diversification of the Caenorhabditis heat shock response by Helitron transposable elements

Abstract
Data availability
Article and author information
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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

(2019) C. elegans and C. briggsae HS RNAseq
NCBI Gene Expression Omnibus, GSE135987.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE135987

The following previously published data sets were used

1. Contrino S
2. Smith RN
3. Butano D
4. Carr A
5. Hu F
6. Lyne R
7. Rutherford K
8. Kalderimis A
9. Sullivan J
10. Carbon S
11. Kephart ET
12. Lloyd P
13. Stinson EO
14. Washington NL
15. Perry MD
16. Ru-zanov P
17. Zha Z
18. Lewis SE
19. Stein LD
20. Micklem G
(2012) H3K27me3 ChIP from L3 stage
modMine, modEncode_5051.

https://cdn.elifesciences.org/articles/51139/intermine.modencode.org
(2017) Release 20180527
All available isotypes.

https://cdn.elifesciences.org/articles/51139/elegansvariation.org
1. Li J
2. Chauve L
3. Phelps G
4. Brielmann RM
5. Morimoto RI
(2016) HSF-1 ChIP
NCBI Gene Expression Omnibus, GSE81523.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE81523

Article and author information

Author details

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.
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.
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.

"This ORCID iD identifies the author of this article:" 0000-0002-4879-9603
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.

"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.

Copyright

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.