Evolution and Dynamics of Small RNA Response to a Retroelement Invasion in Drosophila

Abstract

Although small RNAs efficiently control transposition activity of most transposons in the host genome, such an immune system is not always applicable against a new transposon's invasions. Here, we explored a possibility to introduce potentially mobile copy of the Penelope retroelement previously implicated in hybrid dysgenesis syndrome in Drosophila virilis into the genomes of two distant Drosophila species. The consequences of such introduction were monitored at different phases after experimental colonization as well as in D. virilis species, which is apparently in the process of ongoing Penelope invasion. We investigated the expression of Penelope and biogenesis of Penelope-derived small RNAs in D. virilis and D. melanogaster strains originally lacking active copies of this element after experimental Penelope invasion. These strains were transformed by constructs containing intact Penelope copies. We show that immediately after transformation, which imitates the first stage of retroelement invasion, Penelope undergoes transposition predominantly in somatic tissues, and may produce siRNAs that are apparently unable to completely silence its activity. However, at the later stages of colonization Penelope copies may jump into one of the piRNA-clusters, which results in production of homologous piRNAs that are maternally deposited and can silence euchromatic transcriptionally active copies of Penelope in trans and, hence, prevent further amplification of the invader in the host genome. Intact Penelope copies and different classes of Penelope-derived small RNAs were found in most geographical strains of D. virilis collected throughout the world. Importantly, all strains of this species containing full-length Penelope tested do not produce gonadal sterility in dysgenic crosses and, hence, exhibit neutral cytotype. To understand whether RNA interference mechanism able to target Penelope operates in related species of the virilis group, we correlated the presence of full-length and potentially active Penelope with the occurrence of piRNAs homologous to this transposable element in the ovaries of species comprising the group. It was demonstrated that Penelope-derived piRNAs are present in all virilis group species containing full-length but transcriptionally silent copies of this element that probably represent the remnants of its previous invasions taking place in the course of the virilis species divergent evolution.

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

“…Few TEs show aberrant expression in the hybrid sterile males compared with C. nigoni males Overexpression of TEs is frequently found in F1 hybrids and is associated with male sterility (Rozhkov et al 2013;Erwin et al 2015). We wondered whether misregulation of TEs might be associated with the observed male sterility in the introgression lines despite the fact that they were subjected to backcrossing for at least 15 generations (Bi et al 2015).…”

Multiple roles for Piwi in silencing Drosophila transposons

“…This supposition is supported by studies of P elements and Penelope, a Drosophila virilis transposon artificially introduced into Drosophila melanogaster. Acquisition of the ability to control these elements was associated with their integration into piRNA clusters (Ronsseray et al 1998;Brennecke et al 2008;Khurana et al 2011;Rozhkov et al 2013).…”

Genetic and Epigenetic Changes Involving (Retro)transposons in Animal Hybrids and Polyploids

“…Different mutants in the piRNA pathway can be associated with different types of derepressed TEs [Vagin et al, 2006;Chen et al, 2007;Chambeyron et al, 2008]. Malfunction of epigenetic controls results in transcriptional activation and mobilization of TEs in Drosophila dysgenic hybrids and can also involve changes in chromatin structure and modification [Blumenstiel and Hartl, 2005;Girard and Hannon, 2008;Rozhkov et al, 2010Rozhkov et al, , 2013.…”

“…Initially, maternally deposited siRNAs homologous to Penelope were reported in P-like strains but were absent from M-like strains [Blumenstiel and Hartl, 2005]. A more thorough analysis of small RNAs in D. virilis was performed by Rozhkov et al [2010Rozhkov et al [ , 2013, where Penelope was shown to be targeted by antisense siRNAs, and only a small proportion represented the 23-29-nt piRNA fraction, which could be related to germline silencing. The introduction of active Penelope into D. melanogaster , which has no preexisting Penelope copies in the genome, caused induction of both sense and antisense siRNAs in the transformed strains, suggesting that the siRNA pathway could play an important role at the initial stages of TE invasion, acting similar to an antiviral response.…”

“…The introduction of active Penelope into D. melanogaster , which has no preexisting Penelope copies in the genome, caused induction of both sense and antisense siRNAs in the transformed strains, suggesting that the siRNA pathway could play an important role at the initial stages of TE invasion, acting similar to an antiviral response. Following Penelope mobilization and amplification, its copies can insert into piRNA clusters, triggering production of piRNAs to maintain silencing in the germline [Rozhkov et al, 2013].…”