Adaptation to P Element Transposon Invasion in Drosophila melanogaster

Program in Cell and Developmental Dynamics, University of Massachusetts Medical School, Worcester, MA 01655, USA.
Cell (Impact Factor: 32.24). 12/2011; 147(7):1551-63. DOI: 10.1016/j.cell.2011.11.042
Source: PubMed


Transposons evolve rapidly and can mobilize and trigger genetic instability. Piwi-interacting RNAs (piRNAs) silence these genome pathogens, but it is unclear how the piRNA pathway adapts to invasion of new transposons. In Drosophila, piRNAs are encoded by heterochromatic clusters and maternally deposited in the embryo. Paternally inherited P element transposons thus escape silencing and trigger a hybrid sterility syndrome termed P-M hybrid dysgenesis. We show that P-M hybrid dysgenesis activates both P elements and resident transposons and disrupts the piRNA biogenesis machinery. As dysgenic hybrids age, however, fertility is restored, P elements are silenced, and P element piRNAs are produced de novo. In addition, the piRNA biogenesis machinery assembles, and resident elements are silenced. Significantly, resident transposons insert into piRNA clusters, and these new insertions are transmitted to progeny, produce novel piRNAs, and are associated with reduced transposition. P element invasion thus triggers heritable changes in genome structure that appear to enhance transposon silencing.

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Available from: Jaspreet S Khurana
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    • "Piwi proteins and piRNAs are best known to suppress transposable elements (TEs) in animal germ cells, as supported by TE transcript up-regulation in Piwi pathway mutants (Aravin et al. 2004; Kalmykova et al. 2005; Saito et al. 2006; Vagin et al. 2006), a genetic role in hybrid dysgenesis studies (Brennecke et al. 2008; Chambeyron et al. 2008; Khurana et al. 2011; Grentzinger et al. 2012), and perfect complementarity between piRNA sequences and TE coding transcripts (Juliano et al. 2011; Siomi et al. 2011). In Drosophila, the precursors to TE-associated piRNAs can begin as long singlestranded transcripts from loci that trap TE relics in a biased orientation so that transcription generates piRNAs complementary to TEs (Brennecke et al. 2007; Lau et al. 2009a; Malone et al. 2009). "
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    ABSTRACT: Although Piwi proteins and Piwi-interacting RNAs (piRNAs) genetically repress transposable elements (TEs), it is unclear how the highly diverse piRNA populations direct Piwi proteins to silence TE targets without silencing the entire transcriptome. To determine the capacity of piRNA-mediated silencing, we introduced reporter genes into Drosophila OSS cells, which express microRNAs (miRNAs) and piRNAs, and compared the Piwi pathway to the Argonaute pathway in gene regulation. Reporter constructs containing several target sites that were robustly silenced by miRNAs were not silenced to the same degrees by piRNAs. However, another set of reporters we designed to enable a large number of both TE-directed and genic piRNAs to bind were robustly silenced by the PIWI/piRNA complex in OSS cells. These reporters show that a bulk of piRNAs are required to pair to the reporter's transcripts and not the reporter's DNA sequence to engage PIWI-mediated silencing. Following our genome-wide study of PIWI-regulated targets in OSS cells, we assessed candidate gene elements with our reporter platform. These results suggest TE sequences are the most direct of PIWI regulatory targets while coding genes are less directly affected by PIWI targeting. Finally, our study suggests that the PIWI transcriptional silencing mechanism triggers robust chromatin changes on targets with sufficient piRNA binding, and preferentially regulates TE transcripts because protein-coding transcripts lack a threshold of targeting by piRNA populations. This reporter platform will facilitate future dissections of the PIWI-targeting mechanism.
    Full-text · Article · Oct 2014 · RNA
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    • "In P-M hybrid dysgenesis, which is caused by activation of inducer P element from the paternal side, restoration of fertility in aged flies has been reported (Khurana et al., 2011). Interestingly , in the ovary of these aged flies, de novo integration of transposons into piRNA clusters is observed, indicating that acquisition of transposon sequence in piRNA clusters and piRNA production from the inserted sequence contribute to the restoration of fertility. "
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    ABSTRACT: Piwi proteins and Piwi-interacting RNAs (piRNAs) are essential for gametogenesis, embryogenesis, and stem cell maintenance in animals. Piwi proteins act on transposon RNAs by cleaving the RNAs and by interacting with factors involved in RNA regulation. Additionally, piRNAs generated from transposons and psuedogenes can be used by Piwi proteins to regulate mRNAs at the posttranscriptional level. Here we discuss piRNA biogenesis, recent findings on posttranscriptional regulation of mRNAs by the piRNA pathway, and the potential importance of this posttranscriptional regulation for a variety of biological processes such as gametogenesis, developmental transitions, and sex determination.
    Full-text · Article · Oct 2014 · Molecular Cell
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    • "Considering just the uniquely mapped reads, five out of seven variable piRNA clusters contained only TART elements (supplementary table S1, Supplementary Material online). The relationship between piRNAs and telomeric TEs in Drosophila has been studied and found to differ from the transposon-silencing function of piRNAs (Khurana et al. 2010; Shpiz and Kalmykova 2011). Our data does not allow us to speculate on possible functional consequences of the variability of these telomeric piRNA clusters but they may be interesting clusters for future studies. "

    Full-text · Article · Sep 2014 · Genome Biology and Evolution
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