Abstract
In the Drosophila germline, transposable elements (TEs) are silenced by PIWI-interacting RNA (piRNA) that originate from distinct genomic regions termed piRNA clusters and are processed by PIWI-subfamily Argonaute proteins. Here, we explore the variation in the ability to restrain an alien TE in different Drosophila strains. The I-element is a retrotransposon involved in the phenomenon of I-R hybrid dysgenesis in Drosophila melanogaster. Genomes of R strains do not contain active I-elements, but harbour remnants of ancestral I-related elements. The permissivity to I-element activity of R females, called reactivity, varies considerably in natural R populations, indicating the existence of a strong natural polymorphism in defense systems targeting transposons. To reveal the nature of such polymorphisms, we compared ovarian small RNAs between R strains with low and high reactivity and show that reactivity negatively correlates with the ancestral I-element-specific piRNA content. Analysis of piRNA clusters containing remnants of I-elements shows increased expression of the piRNA precursors and enrichment by the Heterochromatin Protein 1 homolog, Rhino, in weak R strains, which is in accordance with stronger piRNA expression by these regions. To explore the nature of the differences in piRNA production, we focused on two R strains, weak and strong, and showed that the efficiency of maternal inheritance of piRNAs as well as the I-element copy number are very similar in both strains. At the same time, germline and somatic uni-strand piRNA clusters generate more piRNAs in strains with low reactivity, suggesting the relationship between the efficiency of primary piRNA production and variable response to TE invasions. The strength of adaptive genome defense is likely driven by naturally occurring polymorphisms in the rapidly evolving piRNA pathway proteins. We hypothesize that hyper-efficient piRNA production is contributing to elimination of a telomeric retrotransposon HeT-A, which we have observed in one particular transposon-resistant R strain.
Highlights
The main function of the PIWI-interacting RNA system in Drosophila is suppression of transposon activity in the germline. piRNAs are processed from long transcripts, piRNAprecursors, encoded by distinct genomic regions enriched in transposable elements (TEs) remnants, termed piRNA clusters [1]. piRNAs recognize complementary targets, exerting RNA silencing at post-transcriptional and transcriptional levels [2]
Transposon activity in the germline is suppressed by the PIWI-interacting RNA pathway
We demonstrate a likely explanation as to why an overly active piRNA pathway can cause more harm than good in Drosophila: Highly efficient piRNA processing leads to elimination of domesticated telomeric retrotransposons essential for telomere elongation, an effect which has been observed in a natural strain that is extremely resistant to transposon invasion
Summary
The main function of the PIWI-interacting RNA (piRNA) system in Drosophila is suppression of transposon activity in the germline. piRNAs are processed from long transcripts, piRNAprecursors, encoded by distinct genomic regions enriched in TE remnants, termed piRNA clusters [1]. piRNAs recognize complementary targets, exerting RNA silencing at post-transcriptional and transcriptional levels [2]. PiRNAs are processed from long transcripts, piRNAprecursors, encoded by distinct genomic regions enriched in TE remnants, termed piRNA clusters [1]. PiRNAs recognize complementary targets, exerting RNA silencing at post-transcriptional and transcriptional levels [2]. PiRNAs generated in ovarian nurse cells are transmitted into the oocyte to launch the processing of piRNA cluster transcripts in the germline of the progeny through an epigenetic mechanism [6]. The maternal pool of piRNAs silences those TEs in the progeny that are present in the maternal genome. Invasion of alien TEs through paternal inheritance triggers a sterility syndrome, termed hybrid dysgenesis. This occurs due to the absence of maternally transmitted piRNAs complementary to the TE inherited with the paternal genome. Through several generations, TE silencing is established as a result of the generation of corresponding piRNAs by paternal TE copies or by de novo TE insertions within endogenous piRNA clusters [6,7]
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