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, Oct 10, 2015
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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.
    Molecular Cell 10/2014; 56(1):18–27. DOI:10.1016/j.molcel.2014.09.012 · 14.02 Impact Factor
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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. "
    Genome Biology and Evolution 09/2014; 6(10):2786-2798. · 4.23 Impact Factor
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    • "The annotation for genes and exons were obtained from FlyBase (Release 5.45) and the annotation for piRNA clusters was from Brennecke et al. (19) as described above. "
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    ABSTRACT: Insertions and excisions of transposable elements (TEs) affect both the stability and variability of the genome. Studying the dynamics of transposition at the population level can provide crucial insights into the processes and mechanisms of genome evolution. Pooling genomic materials from multiple individuals followed by high-throughput sequencing is an efficient way of characterizing genomic polymorphisms in a population. Here we describe a novel method named TEMP, specifically designed to detect TE movements present with a wide range of frequencies in a population. By combining the information provided by pair-end reads and split reads, TEMP is able to identify both the presence and absence of TE insertions in genomic DNA sequences derived from heterogeneous samples; accurately estimate the frequencies of transposition events in the population and pinpoint junctions of high frequency transposition events at nucleotide resolution. Simulation data indicate that TEMP outperforms other algorithms such as PoPoolationTE, RetroSeq, VariationHunter and GASVPro. TEMP also performs well on whole-genome human data derived from the 1000 Genomes Project. We applied TEMP to characterize the TE frequencies in a wild Drosophila melanogaster population and study the inheritance patterns of TEs during hybrid dysgenesis. We also identified sequence signatures of TE insertion and possible molecular effects of TE movements, such as altered gene expression and piRNA production. TEMP is freely available at github:
    Nucleic Acids Research 04/2014; 42(11). DOI:10.1093/nar/gku323 · 9.11 Impact Factor
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