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: 33.12). 12/2011; 147(7):1551-63. DOI: 10.1016/j.cell.2011.11.042
Source: PubMed

ABSTRACT 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, Aug 18, 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 · 14.46 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. · 4.53 Impact Factor
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    • "Increasing evidence suggests that these adaptive changes are driven by intragenomic conflicts (Brown and O'Neill, 2010; Crespi and Nosil, 2013). Possible conflict scenarios involve selfish DNA elements like transposable elements (Khurana et al., 2011; Kidwell et al., 1977) or centromeres that favor their own transmission, often at the expense of the overall fitness of the host organism (Fishman and Saunders, 2008; Hedges and Belancio, 2011; Pardo-Manuel de Villena and Sapienza, 2001). Such conflicts are supposed to promote the coevolution of compensatory mechanisms or factors, which may cause incompatibilities in hybrids (Malik and Henikoff, 2001; 2009). "
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    Developmental Cell 11/2013; 27(4). DOI:10.1016/j.devcel.2013.10.001 · 10.37 Impact Factor
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