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De novo piRNA cluster formation in the Drosophila germ line triggered by transgenes containing a transcribed transposon fragment

Olovnikov, Ivan and Ryazansky, Sergei and Shpiz, Sergey and Lavrov, Sergey and Abramov, Yuri and Vaury, Chantal and Jensen, Silke and Kalmykova, Alla (2013) De novo piRNA cluster formation in the Drosophila germ line triggered by transgenes containing a transcribed transposon fragment. Nucleic Acids Research, 41 (11). pp. 5757-5768. ISSN 0305-1048. https://resolver.caltech.edu/CaltechAUTHORS:20130722-091352950

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Abstract

PIWI-interacting RNAs (piRNAs) provide defence against transposable element (TE) expansion in the germ line of metazoans. piRNAs are processed from the transcripts encoded by specialized heterochromatic clusters enriched in damaged copies of transposons. How these regions are recognized as a source of piRNAs is still elusive. The aim of this study is to determine how transgenes that contain a fragment of the Long Interspersed Nuclear Elements (LINE)-like I transposon lead to an acquired TE resistance in Drosophila. We show that such transgenes, being inserted in unique euchromatic regions that normally do not produce small RNAs, become de novo bidirectional piRNA clusters that silence I-element activity in the germ line. Strikingly, small RNAs of both polarities are generated from the entire transgene and flanking genomic sequences—not only from the transposon fragment. Chromatin immunoprecipitation analysis shows that in ovaries, the trimethylated histone 3 lysine 9 (H3K9me3) mark associates with transgenes producing piRNAs. We show that transgene-derived hsp70 piRNAs stimulate in trans cleavage of cognate endogenous transcripts with subsequent processing of the non-homologous parts of these transcripts into piRNAs.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1093/nar/gkt310 DOIArticle
http://nar.oxfordjournals.org/content/41/11/5757PublisherArticle
ORCID:
AuthorORCID
Ryazansky, Sergei0000-0002-3171-2997
Additional Information:© 2013 The Author(s). Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. Received December 23, 2012; Revised March 6, 2013; Accepted April 3, 2013. First published online: April 24, 2013. The authors thank Alexei Aravin for help with small RNA cloning, Igor Antoshechkin (Caltech) for help with small RNA sequencing, Pierre Pouchin and Yoan Renaud for help with bioinformatic analysis and Alexandre Webster for editing the English. Funding: ‘Wildlife: Current State and Development’ of the Presidium of RAS (to A.K.); Russian Foundation for Basic Researches [09-04-00996 to S.S.]. Funding for open access charge: ‘Wildlife: Current State and Development’ of the Presidium of RAS.
Funders:
Funding AgencyGrant Number
Presidium of RASUNSPECIFIED
Russian Foundation for Basic Researches09-04-00996
Issue or Number:11
Record Number:CaltechAUTHORS:20130722-091352950
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130722-091352950
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:39484
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:22 Jul 2013 21:13
Last Modified:09 Mar 2020 13:19

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