DrosophilaP element: Transposition, regulation and evolution

Coen, Dario; Lemaître, Bruno; Delattre, Marie; Quesneville, Hadi; Ronsseray, Stéphane; Simonelig, Martine; Higuet, Dominique; Lehmann, Monique; Montchamp, C.; Nouaud, Danielle

doi:10.1007/bf01435240

Cited by 23 publications

(15 citation statements)

References 101 publications

(73 reference statements)

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“…Various mechanisms of repression of TE activities have been incorporated into our understanding of the population genetics of TEs, including self-regulation of copy number by reducing transposition rates (Charlesworth and Charlesworth 1983;Langley et al 1983), cis-acting regulation (transposition immunity) and trans-acting regulation (transposition repression) of TEs (Charlesworth and Langley 1986), regulation of transposition by host factors (Badge and Brookfield 1998), or more specifically, regulation of transposition by the interaction between TEs and the host genome such as the P-M hybrid dysgenesis system (Engels 1986;Boussy et al 1988;Brookfield 1991;Coen et al 1994;Anxolabehere 1997, 1998) or the I-R hybrid dysgenesis system (Proust et al 1992;Chaboissier et al 1995;Jensen et al 1995Jensen et al , 2002. Recently, it was discovered that PIWI-interacting RNAs (piRNAs), a class of small (26-31 bp) RNA molecules, are crucial repressors of active TEs in the germlines of fruit flies and worms (Aravin et al 2001Nishida and Siomi 2006;Vagin et al 2006;Brennecke et al 2007Brennecke et al , 2008Nishida et al 2007;Yin and Lin 2007;Das et al 2008;Ghildiyal et al 2008;Girard and Hannon 2008;Siomi and Siomi 2008;Li et al 2009;).…”

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confidence: 99%

Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila

Lü¹,

Clark²

2009

Genome Res.

102

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Transposable elements (TEs) are mobile DNA sequences that make up a large fraction of eukaryotic genomes. Recently it was discovered that PIWI-interacting RNAs (piRNAs), a class of small RNA molecules that are mainly generated from transposable elements, are crucial repressors of active TEs in the germline of fruit flies. By quantifying expression levels of 32 TE families in piRNA pathway mutants relative to wild-type fruit flies, we provide evidence that piRNAs can severely silence the activities of retrotransposons. We incorporate piRNAs into a population genetic framework for retrotransposons and perform forward simulations to model the population dynamics of piRNA loci and their targets. Using parameters optimized for Drosophila melanogaster, our simulation results indicate that (1) piRNAs can significantly reduce the fitness cost of retrotransposons; (2) retrotransposons that generate piRNAs (piRTs) are selectively more advantageous, and such retrotransposon insertions more easily attain high frequency or fixation; (3) retrotransposons that are repressed by piRNAs (targetRTs), however, also have an elevated probability of reaching high frequency or fixation in the population because their deleterious effects are attenuated. By surveying the polymorphisms of piRT and targetRT insertions across nine strains of D. melanogaster, we verified these theoretical predictions with population genomic data. Our theoretical and empirical analysis suggests that piRNAs can significantly increase the fitness of individuals that bear them; however, piRNAs may provide a shelter or Trojan horse for retrotransposons, allowing them to increase in frequency in a population by shielding the host from the deleterious consequences of retrotransposition.[Supplemental material is available online at http://www.genome.org.] Like other kinds of mutations, however, most mutations created by TE insertions are deleterious to the host and are thus selected against. Approximately 50%-80% of mutations arising in D. melanogaster can be attributed to TEs (Finnegan 1992;Ashburner et al. 2004). Based on the copy number of TEs in D. melanogaster, it was estimated that TEs can decrease the fitness of hosts by 0.4%-5% (Eanes et al. 1987;Charlesworth and Langley 1989;Mackay et al. 1992;Pasyukova et al. 2004). The fitness costs of TEs are generally mediated through the following mechanisms: (1) TE insertions disrupt genes (Charlesworth and Charlesworth 1983;Finnegan 1992;McDonald et al. 1997); (2) transcription and translation of TE-encoded genes are costly (Brookfield 1991; Nuzhdin 1999); and (3) ectopic recombination among dispersed and heterozygous TEs creates deleterious chromosomal rearrangements (Montgomery et al. 1987;Langley et al. 1988;Charlesworth and Langley 1989;Petrov et al. 2003). It has been demonstrated that different TE families are regulated by different mechanisms, although these mechanisms are not mutually exclusive (Biemont et al. 1994;Carr et al. 2002;Petrov et al. 2003). Despite their being under strong selective pressure, TEs ...

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confidence: 99%

Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila

Lü¹,

Clark²

2009

Genome Res.

102

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“…In both systems, it appears that establishment of repressive capacities, following paternal inheritance of I-or P-elements carrying genomes in a cytoplasm devoid of I-or P-homologous piRNAs, is progressive and require several generations to be completed (Engels 1979(Engels , 1989Bregliano et al 1980;Finnegan 1989;Rio 2002). For example, experiments were performed with a line [Lk-P(1A)] carrying only two regulatory P-elements inserted in a telomeric strong piRNA-producing locus (TAS) (Coen et al 1994;Ronsseray et al 1996). It was shown that paternal transmission of the telomeric P-element locus in a cytoplasm devoid of P-homologous piRNAs, followed by maternal inheritance of the telomeric P-elements in successive generations, requires four generations to progressively establish complete P-repression (Coen et al 1994).…”

Section: Discussionmentioning

confidence: 99%

“…For example, experiments were performed with a line [Lk-P(1A)] carrying only two regulatory P-elements inserted in a telomeric strong piRNA-producing locus (TAS) (Coen et al 1994;Ronsseray et al 1996). It was shown that paternal transmission of the telomeric P-element locus in a cytoplasm devoid of P-homologous piRNAs, followed by maternal inheritance of the telomeric P-elements in successive generations, requires four generations to progressively establish complete P-repression (Coen et al 1994). Thus, during these generations, a progressive spreading must occur within the TAS locus for piRNA production capacity, which finally results in strong production of piRNAs homologous, not only to the TAS, but also to the P-element.…”

Section: Discussionmentioning

confidence: 99%

“…However, some observations remain to be explained. First, according to this model, when telomeric P-insertions are paternally introduced in a lineage and thereupon are maternally transmitted, establishment of repression would be expected to require only one generation to be completed but in fact it was shown to be progressive over generations (Coen et al 1994). It is possible that nuclear reinforcement mediated by trailer piRNAs loaded on Piwi on the piRNA-producing locus is necessary, and this reinforcement involves maternal transmission to be efficient and thus requires more than one generation to be completed.…”

Section: Discussionmentioning

confidence: 99%

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Paramutation inDrosophilaRequires Both Nuclear and Cytoplasmic Actors of the piRNA Pathway and InducesCis-spreading of piRNA Production

et al. 2015

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Transposable element activity is repressed in the germline in animals by PIWI-interacting RNAs (piRNAs), a class of small RNAs produced by genomic loci mostly composed of TE sequences. The mechanism of induction of piRNA production by these loci is still enigmatic. We have shown that, in Drosophila melanogaster, a cluster of tandemly repeated P-lacZ-white transgenes can be activated for piRNA production by maternal inheritance of a cytoplasm containing homologous piRNAs. This activated state is stably transmitted over generations and allows trans-silencing of a homologous transgenic target in the female germline. Such an epigenetic conversion displays the functional characteristics of a paramutation, i.e., a heritable epigenetic modification of one allele by the other. We report here that piRNA production and trans-silencing capacities of the paramutated cluster depend on the function of the rhino, cutoff, and zucchini genes involved in primary piRNA biogenesis in the germline, as well as on that of the aubergine gene implicated in the ping-pong piRNA amplification step. The 21-nt RNAs, which are produced by the paramutated cluster, in addition to 23-to 28-nt piRNAs are not necessary for paramutation to occur. Production of these 21-nt RNAs requires Dicer-2 but also all the piRNA genes tested. Moreover, cytoplasmic transmission of piRNAs homologous to only a subregion of the transgenic locus can generate a strong paramutated locus that produces piRNAs along the whole length of the transgenes. Finally, we observed that maternally inherited transgenic small RNAs can also impact transgene expression in the soma. In conclusion, paramutation involves both nuclear (Rhino, Cutoff) and cytoplasmic (Aubergine, Zucchini) actors of the piRNA pathway. In addition, since it is observed between nonfully homologous loci located on different chromosomes, paramutation may play a crucial role in epigenome shaping in Drosophila natural populations.KEYWORDS gene regulation; trans-generational epigenetics; noncoding small RNAs; mobile DNA; Drosophila G ENOMES must confront the presence of a large fraction of mobile DNA whose activity can result in severe deleterious effects on chromosome stability and gametogenesis. In the germline of animals, a system of genomic traps exists into which any transposable element (TE) can insert, thereby generating loci that contain a catalog of potentially dangerous sequences that have to be repressed (Brennecke et al. 2007;Pane et al. 2011;Iwasaki et al. 2015). In the Drosophila melanogaster germline, most of these loci are transcribed in both directions (dual-strand clusters) and undergo noncanonical transcription and RNA processing (Mohn et al. 2014;Zhang et al. 2014). This results in production of noncoding small RNAs having the capacity to target the transcripts of the homologous, potentially active, TE copies scattered throughout the genome. These small RNAs are called PIWI-interacting RNAs (piRNAs) and repress TE activity at both the transcriptional and post-transcriptional levels (Sa...

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“…However, the regulation of the transcription and transposition of these two elements has been reported as a result of crosses under conditions implying hybrid dysgenesis. In non-dysgenic crosses, the activity of the I and P elements is totally or partially repressed (Busseau et al, 1994;Coen et al, 1994). Expression of the transposable elements therefore seems to be severely controlled in germlines, presumably to limit any increase in the copy number with its associated deleterious effects.…”

Section: Is Expressed Only In Malesmentioning

confidence: 99%

Tissue-specificity of 412 retrotransposon expression in Drosophila simulans and D. melanogaster

et al. 2002

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We analyse the expression of the retrotransposon 412 in the soma, testes, and ovaries in populations of Drosophila simulans and D. melanogaster, using RT-PCR and in situ hybridization. We find that expression of 412 is highly variable in the soma, confirming previous findings based on Northern blots. No 412 RNA is detected in the ovaries by either in situ hybridization or RT-PCR, in any population of either species. Transcripts are, however, detected in the male germline, which show a very characteristic spatial pat-

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DrosophilaP element: Transposition, regulation and evolution

Cited by 23 publications

References 101 publications

Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila

Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila

Paramutation inDrosophilaRequires Both Nuclear and Cytoplasmic Actors of the piRNA Pathway and InducesCis-spreading of piRNA Production

Tissue-specificity of 412 retrotransposon expression in Drosophila simulans and D. melanogaster

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