Diversification of the Caenorhabditis heat shock response by Helitron transposable elements

Elife. 2019 Dec 11;8:e51139. doi: 10.7554/eLife.51139.

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.

Keywords: C. elegans; Caenorhabditis; HSF-1; genetics; genomics; heat shock; transposons.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis / genetics
  • Caenorhabditis / physiology*
  • Caenorhabditis / radiation effects*
  • Caenorhabditis elegans Proteins / metabolism
  • DNA Transposable Elements*
  • Gene Expression Regulation
  • Gene Regulatory Networks
  • Heat-Shock Response*
  • Protein Binding
  • RNA Polymerase II / metabolism
  • Response Elements*
  • Transcription Factors / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • DNA Transposable Elements
  • Transcription Factors
  • heat shock factor-1, C elegans
  • RNA Polymerase II

Associated data

  • GEO/GSE135987
  • GEO/GSE81523