Abstract
The control of transposable element (TE) activity in germ cells provides genome integrity over generations. A distinct small RNA–mediated pathway utilizing Piwi-interacting RNAs (piRNAs) suppresses TE expression in gonads of metazoans. In the fly, primary piRNAs derive from so-called piRNA clusters, which are enriched in damaged repeated sequences. These piRNAs launch a cycle of TE and piRNA cluster transcript cleavages resulting in the amplification of piRNA and TE silencing. Using genome-wide comparison of TE insertions and ovarian small RNA libraries from two Drosophila strains, we found that individual TEs inserted into euchromatic loci form novel dual-stranded piRNA clusters. Formation of the piRNA-generating loci by active individual TEs provides a more potent silencing response to the TE expansion. Like all piRNA clusters, individual TEs are also capable of triggering the production of endogenous small interfering (endo-si) RNAs. Small RNA production by individual TEs spreads into the flanking genomic regions including coding cellular genes. We show that formation of TE-associated small RNA clusters can down-regulate expression of nearby genes in ovaries. Integration of TEs into the 3′ untranslated region of actively transcribed genes induces piRNA production towards the 3′-end of transcripts, causing the appearance of genic piRNA clusters, a phenomenon that has been reported in different organisms. These data suggest a significant role of TE-associated small RNAs in the evolution of regulatory networks in the germline.
Highlights
A large number of transposable element (TE) families populate the genome of Drosophila melanogaster, comprising 22% of the whole genome [1]
Silencing of transposable elements (TEs) in germ cells depends on a distinct class of small RNAs, Piwi-interacting RNAs
According to the current model, individual TEs and their transcripts are considered merely as targets of cluster-derived primary Piwi-interacting RNAs (piRNAs), which exert post-transcriptional and transcriptional silencing in Drosophila
Summary
A large number of transposable element (TE) families populate the genome of Drosophila melanogaster, comprising 22% of the whole genome [1]. Most of the heterochromatic TEs are destroyed by insertions of other transposons, are not capable of autonomous transposition, and are concentrated in a number of mainly pericentromeric regions. These regions—termed piRNA clusters—were previously considered ‘junk’ DNA and are implicated in a defense system called the Piwi-interacting RNA (piRNA) pathway [6,7]. In the follicle (somatic) cells, single-stranded clusters (e.g., X-linked flamenco locus) contain transposon fragments inverted relative to the direction of transcription and produce piRNAs that are almost exclusively antisense to TEs [6,8]. Individual TE coding transcripts are recognized as a source of primary piRNAs [15]. piRNA clusters produce significant amounts of endogenous small interfering RNAs (endo-siRNAs) in a Dicer-2-dependent manner
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