Abstract
BackgroundTransposable elements (TEs) are an almost universal constituent of eukaryotic genomes. In animals, Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and thus restricting TE activity. Nevertheless, TE content varies widely across eukaryotes and the dynamics of TE activity and TE silencing across evolutionary time is poorly understood.ResultsHere, we used experimentally evolved populations of C. elegans to study the dynamics of TE expression over 409 generations. The experimental populations were evolved at population sizes of 1, 10 and 100 individuals to manipulate the efficiency of natural selection versus genetic drift. We demonstrate increased TE expression relative to the ancestral population, with the largest increases occurring in the smallest populations. We show that the transcriptional activation of TEs within active regions of the genome is associated with failure of piRNA-mediated silencing, whilst desilenced TEs in repressed chromatin domains retain small RNAs. Additionally, we find that the sequence context of the surrounding region influences the propensity of TEs to lose silencing through failure of small RNA-mediated silencing.ConclusionsOur results show that natural selection in C. elegans is responsible for maintaining low levels of TE expression, and provide new insights into the epigenomic features responsible.
Highlights
Transposable elements (TEs) are an almost universal constituent of eukaryotic genomes
The nematode Caenorhabditis elegans is a wellestablished model for small-RNA mediated silencing. Piwi-interacting small RNAs (piRNAs) in C. elegans are unusual in that the two piRNA clusters on Chromosome IV are composed of individual RNA polymerase II (RNA pol II) transcription loci where each piRNA has its own upstream motif [5,6,7,8]. piRNA clusters are located within H3K27me3-rich chromatin, which, together with cis-acting RNA pol II pausing sequences downstream of the piRNA, enforce production of ~ 28 nucleotide piRNA precursors [9]. piRNA precursors are further trimmed to result in mature 21-nucleotide piRNAs with a uracil as the first nucleotide (21 U-RNAs), which associate with the C. elegans Piwi protein PRG-1 [5,6,7]
Relaxed selection leads to increased TE expression In order to assess the effect of selection on TE expression, we generated spontaneous mutation accumulation (MA) lines of C. elegans and propagated them by randomly selecting N individuals at each generation, where N was either 1, 10 or 100 [44]
Summary
Transposable elements (TEs) are an almost universal constituent of eukaryotic genomes. Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and restricting TE activity. Transposable elements (TEs) are almost ubiquitous across eukaryotic genomes [1]. Their ability to replicate independently of the host genome, coupled with the existence of multiple copies liable to ectopic recombination means they present a potential threat to genome stability. PiRNA precursors are further trimmed to result in mature 21-nucleotide piRNAs with a uracil as the first nucleotide (21 U-RNAs), which associate with the C. elegans Piwi protein PRG-1 [5,6,7]. Downstream of PRG1, piRNA silencing relies on a nematode-specific class of secondary small RNAs known as 22G-RNAs [6]. Whilst removal of piRNAs alone has mild effects on TE expression, combining mutations of PRG1 with mutations disrupting the 22G-RNA biogenesis machinery leads to reactivation of several TEs [16, 17]
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