Abstract
The piwi-interacting RNAs (piRNA) are small RNAs that target selfish transposable elements (TEs) in many animal genomes. Until now, piRNAs’ role in TE population dynamics has only been discussed in the context of their suppression of TE transposition, which alone is not sufficient to account for the skewed frequency spectrum and stable containment of TEs. On the other hand, euchromatic TEs can be epigenetically silenced via piRNA-dependent heterochromatin formation and, similar to the widely known “Position-effect variegation”, heterochromatin induced by TEs can “spread” into nearby genes. We hypothesized that the piRNA-mediated spread of heterochromatin from TEs into adjacent genes has deleterious functional effects and leads to selection against individual TEs. Unlike previously identified deleterious effects of TEs due to the physical disruption of DNA, the functional effect we investigated here is mediated through the epigenetic influences of TEs. We found that the repressive chromatin mark, H3K9me, is elevated in sequences adjacent to euchromatic TEs at multiple developmental stages in Drosophila melanogaster. Furthermore, the heterochromatic states of genes depend not only on the number of and distance from adjacent TEs, but also on the likelihood that their nearest TEs are targeted by piRNAs. These variations in chromatin status probably have functional consequences, causing genes near TEs to have lower expression. Importantly, we found stronger selection against TEs that lead to higher H3K9me enrichment of adjacent genes, demonstrating the pervasive evolutionary consequences of TE-induced epigenetic silencing. Because of the intrinsic biological mechanism of piRNA amplification, spread of TE heterochromatin could result in the theoretically required synergistic deleterious effects of TE insertions for stable containment of TE copy number. The indirect deleterious impact of piRNA-mediated epigenetic silencing of TEs is a previously unexplored, yet important, element for the evolutionary dynamics of TEs.
Highlights
Transposable elements (TEs) are genetic elements that increase their copy number in the host genome by copying themselves to new genomic locations
The piwi-interacting RNAs are small RNAs that can suppress the expression of selfish transposable elements (TEs) in many animal genomes
One mechanism by which piwi-interacting RNAs (piRNA) silence TEs is through the formation of heterochromatin, which is condensed chromatin and generally associated with repressed gene expression
Summary
Transposable elements (TEs) are genetic elements that increase their copy number in the host genome by copying themselves to new genomic locations. Regulation of transposition rate is unlikely to account for the observed low population frequency of most TEs in outbreeding populations such as Drosophila ([4,16,17,18,19], reviewed in [15]). Instead, both theoretical analyses and empirical results support that selection against deleterious impacts of TEs plays a primary role in the evolutionary dynamics of TEs [15,20,21]. Without regulated TE transposition, selection alone can result in an equilibrium of TE copy number and lead to the skewed frequency spectrum of TEs in natural populations
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