The somatic piRNA pathway controls germline transposition over generations

Barckmann, Bridlin; El-Barouk, Marianne; Pélisson, Alain; Mugat, Bruno; Li, Blaise; Franckhauser, Celine; Lavier, Anna-Sophie Fiston; Mirouze, Marie; Fablet, Marie; Chambeyron, Séverine

doi:10.1093/nar/gky761

Cited by 39 publications

(46 citation statements)

References 65 publications

(81 reference statements)

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“…However, loss of piwi is associated with increased levels of antisense TE transcripts and of siRNAs, whereas double piwi Dicer-2 mutants show increased levels of transcripts from a large panel of TE families. Similar observations were made recently in ovarian somatic cells where double knockdown of piwi and Dicer-2 leads to synergistic derepression of LTR retrotransposons (Barckmann et al 2018). We thus propose a dual-layer repression mechanism whereby residual expression of TE that results from incomplete piwi-mediated TGS feeds Dicer-2 for siRNA production that in turn reduces TE transcript levels through PTGS.…”

Section: A Dual-layer Te Repression By Small Rnassupporting

confidence: 86%

Dual-layer transposon repression in heads of Drosophila melanogaster

Beek

Silva

Pouch

et al. 2018

RNA

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piRNA-mediated repression of transposable elements (TE) in the germline limits the accumulation of mutations caused by their transposition. It is not clear whether the piRNA pathway plays a role in adult, nongonadal tissues in To address this question, we analyzed the small RNA content of adult heads. We found that the varying amount of piRNA-sized, ping-pong positive molecules in heads correlates with contamination by gonadal tissue during RNA extraction, suggesting that most of the piRNAs detected in heads originate from gonads. We next sequenced the heads of wild-type and mutants to address whether loss of function would affect the low amount of piRNA-sized, ping-pong negative molecules that are still detected in heads hand-checked to avoid gonadal contamination. We find that loss of does not significantly affect these 24-28 nt RNAs. Instead, we observe increased siRNA levels against the majority of TE families. To determine the effect of this siRNA level change on transposon expression, we sequenced the transcriptome of wild-type, , and double-mutant heads. We find that RNA expression levels of the majority of TE in or mutants remain unchanged and that TE transcripts increase only in double-mutants. These results lead us to suggest a dual-layer model for TE repression in adult somatic tissues. Piwi-mediated gene silencing established during embryogenesis constitutes the first layer of TE repression whereas Dicer-2-dependent siRNA-mediated silencing provides a backup mechanism to repress TEs that escape silencing by Piwi.

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Section: A Dual-layer Te Repression By Small Rnassupporting

confidence: 86%

Dual-layer transposon repression in heads of Drosophila melanogaster

Beek

Silva

Pouch

et al. 2018

RNA

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show abstract

“…We investigated the fraction of dysgenic ovaries in the F1 and the fraction of hatched eggs (F2), two traits classically affected by HD. However, it is feasible that Tirant activity leads to entirely different phenotypic effects, especially since Tirant might be an endogenous retrovirus that multiplies by a different mechanism than the other three TEs that cause HD symptoms; Tirant may infect the germline via virus-like-particles, whereas the other three TEs are directly active in the germline (Calvi and Gelbart, 1994;Akkouche et al, 2012;Wang et al, 2018;Moon et al, 2018;Barckmann et al, 2018). Second, the severity of HD symptoms frequently depends on multiple factors, such as temperature and the age of flies (Kidwell et al, 1977;Bucheton, 1979;Kidwell and Novy, 1979;Serrato-Capuchina et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Tirant stealthily invaded naturalDrosophila melanogasterpopulations during the last century

Schwarz

Wierzbicki

Senti

et al. 2020

Preprint

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It was long thought that solely three different transposable elements -the I-element, the P-element and hobo -invaded natural D. melanogaster populations within the last century. By sequencing the 'living fossils' of Drosophila research, i.e. D. melanogaster strains sampled from natural populations at different time points, we show that a fourth TE, Tirant, invaded D. melanogaster populations during the past century. Tirant likely spread in D. melanogaster populations around 1938, followed by the I-element, hobo, and, lastly, the P-element. In addition to the recent insertions of the canonical Tirant, D. melanogaster strains harbour degraded Tirant sequences in the heterochromatin which are likely due to an ancient invasion, possibly predating the split of D. melanogaster and D. simulans. In contrast to the I-element, P-element and hobo, we did not find that Tirant induces any hybrid dysgenesis symptoms. This absence of apparent phenotypic effects may explain the late discovery of the Tirant invasion. Recent Tirant insertions were found in all investigated natural populations. Populations from Tasmania carry distinct Tirant sequences, likely due to a founder effect. By investigating the TE composition of natural populations and strains sampled at different time points, insertion site polymorphisms, piRNAs and phenotypic effects, we provide a comprehensive study of a natural TE invasion.

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“…What could be responsible for this pronounced discrepancy? Possible hypothesis are an insertion bias of somatic TEs into the flamenco locus or siRNAs contributing to TE silencing in the soma [Barckmann et al, 2018, Sultana et al, 2017.…”

Section: Discussionmentioning

confidence: 99%

Dynamics of transposable element invasions with piRNA clusters

Kofler¹

2018

Preprint

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In mammals and in invertebrates the proliferation of a newly invading transposable element (TE) is thought to be stopped by a random insertion of one member of the invading TE family into a piRNA cluster. This view is known as the trap model. Here we explore the dynamics of TE invasions under the trap model using large-scale computer simulations. We found that piRNA clusters confer a substantial benefit, effectively preventing extinction of host populations from an uncontrollable proliferation of deleterious TEs. We show that TE invasions under the trap model consists of three distinct phases: first the TE rapidly amplifies within the population, next TE proliferation is stopped by segregating cluster insertions and finally the TE is permanently inactivated by fixation of a cluster insertion. Suppression by segregating cluster insertions is unstable and bursts of TE activity may yet occur. The transpositon rate and the population size mostly influence the length of the phases but not the amount of TEs accumulating during an invasion. Solely the size of piRNA clusters was identified as a major factor influencing TE abundance. Investigating the impact of different cluster architectures we found that a single non-recombining cluster (e.g. the somatic cluster flamenco in Drosophila) is more efficient in stopping invasions than clusters distributed over several chromosomes (e.g germline cluster in Drosophila). With the somatic architecture fewer TEs accumulate during an invasion and fewer cluster insertions are required to stop the TE. The inefficiency of the germline architecture stems from recombination among cluster sites which makes it necessary that each diploid carries, on the average, four cluster insertions, such that most individuals will end up with at least one cluster insertion. Surprisingly we found that negative selection in a model with piRNA clusters can lead to a novel equilibrium state, where TE copy numbers remain stable despite only some individuals in a population carrying a cluster insertion. Finally when applying our approach to real data from Drosophila melanogaster we found that the trap model reasonably well accounts for the abundance of germline TEs but not of somatic TEs. The abundance of somatic TEs, such as gypsy, is much lower than expected.

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The somatic piRNA pathway controls germline transposition over generations

Cited by 39 publications

References 65 publications

Dual-layer transposon repression in heads of Drosophila melanogaster

Dual-layer transposon repression in heads of Drosophila melanogaster

Tirant stealthily invaded naturalDrosophila melanogasterpopulations during the last century

Dynamics of transposable element invasions with piRNA clusters

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