Abstract
Transgenes containing a fragment of the I retrotransposon represent a powerful model of piRNA cluster de novo formation in the Drosophila germline. We revealed that the same transgenes located at different genomic loci form piRNA clusters with various capacity of small RNA production. Transgenic piRNA clusters are not established in piRNA pathway mutants. However, in the wild-type context, the endogenous ancestral I-related piRNAs heterochromatinize and convert the I-containing transgenes into piRNA-producing loci. Here, we address how the quantitative level of piRNAs influences the heterochromatinization and piRNA production. We show that a minimal amount of maternal piRNAs from ancestral I-elements is sufficient to form the transgenic piRNA clusters. Supplemental piRNAs stemming from active I-element copies do not stimulate additional chromatin changes or piRNA production from transgenes. Therefore, chromatin changes and piRNA production are initiated by a minimum threshold level of complementary piRNAs, suggesting a selective advantage of prompt cell response to the lowest level of piRNAs. It is noteworthy that the weak piRNA clusters do not transform into strong ones after being targeted by abundant I-specific piRNAs, indicating the importance of the genomic context for piRNA cluster establishment. Analysis of ovarian transcription profiles suggests that regions facilitating convergent transcription favor the formation of transgenic piRNA clusters.
Highlights
Piwi interacting RNAs play a key role in silencing of Transposable Elements (TEs) to prevent their excessive transposition in the germline. piRNAs have endogenous origin and are generated from long transcripts derived from distinct genomic regions termed piRNA clusters [1,2].Specific chromatin components of piRNA clusters along with RNA processing/export factors ensure the particular fate for piRNA precursors
Do the chromatin structure and targeting the transgenes? We found that the increase in the level of piRNAs targeting I-TG transgenes small RNA production from the transgenes depend on the amount of endogenous I-specific piRNAs does not stimulate additional changes of the chromatin state or piRNA production by the transgenes
Conclusions piRNAs play a key role in the control of TE activity mediating their transcriptional, cotranscriptional and posttranscriptional silencing. piRNA-mediated de novo piRNA cluster formation is another level of defense which results in the appearance of novel piRNA source loci in the genome
Summary
Piwi interacting RNAs (piRNAs) play a key role in silencing of Transposable Elements (TEs) to prevent their excessive transposition in the germline. Specific chromatin components of piRNA clusters along with RNA processing/export factors ensure the particular fate for piRNA precursors. In Drosophila, Rhino (Rhi) protein, a germline-specific ortholog of Heterochromatin Protein 1 (HP1), is considered as a key factor of piRNA cluster chromatin. Binding of Rhi mediates non-canonical transcription and processing of the piRNA precursors emerging from. PiRNA-mediated silencing is a potent mechanism of expression control realized through transcriptional [10,11] and co-transcriptional [12]. Despite the high regulatory potential of piRNAs, their practical application in the suppressing of the target gene expression is complicated by the fact that little is known about the prerequisites for the formation of a robust piRNA cluster
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