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Genes 2019, 10(3), 209; https://doi.org/10.3390/genes10030209

The Integrity of piRNA Clusters is Abolished by Insulators in the Drosophila Germline

1
Institute of Molecular Genetics, Russian Academy of Sciences, 123182 Moscow, Russia
2
Present Address: Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
*
Author to whom correspondence should be addressed.
Received: 29 January 2019 / Revised: 27 February 2019 / Accepted: 6 March 2019 / Published: 11 March 2019
(This article belongs to the Special Issue Repetitive DNA Sequences)
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Abstract

Piwi-interacting RNAs (piRNAs) control transposable element (TE) activity in the germline. piRNAs are produced from single-stranded precursors transcribed from distinct genomic loci, enriched by TE fragments and termed piRNA clusters. The specific chromatin organization and transcriptional regulation of Drosophila germline-specific piRNA clusters ensure transcription and processing of piRNA precursors. TEs harbour various regulatory elements that could affect piRNA cluster integrity. One of such elements is the suppressor-of-hairy-wing (Su(Hw))-mediated insulator, which is harboured in the retrotransposon gypsy. To understand how insulators contribute to piRNA cluster activity, we studied the effects of transgenes containing gypsy insulators on local organization of endogenous piRNA clusters. We show that transgene insertions interfere with piRNA precursor transcription, small RNA production and the formation of piRNA cluster-specific chromatin, a hallmark of which is Rhino, the germline homolog of the heterochromatin protein 1 (HP1). The mutations of Su(Hw) restored the integrity of piRNA clusters in transgenic strains. Surprisingly, Su(Hw) depletion enhanced the production of piRNAs by the domesticated telomeric retrotransposon TART, indicating that Su(Hw)-dependent elements protect TART transcripts from piRNA processing machinery in telomeres. A genome-wide analysis revealed that Su(Hw)-binding sites are depleted in endogenous germline piRNA clusters, suggesting that their functional integrity is under strict evolutionary constraints. View Full-Text
Keywords: drosophila; retrotransposons; transgene; piRNA cluster; insulator; Su(Hw); Rhino; germline; transcription; HeT-A and TART telomeric retrotransposons drosophila; retrotransposons; transgene; piRNA cluster; insulator; Su(Hw); Rhino; germline; transcription; HeT-A and TART telomeric retrotransposons
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This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited (CC BY 4.0).

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Radion, E.; Sokolova, O.; Ryazansky, S.; Komarov, P.A.; Abramov, Y.; Kalmykova, A. The Integrity of piRNA Clusters is Abolished by Insulators in the Drosophila Germline. Genes 2019, 10, 209.

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