Evidence for maternally transmitted small interfering RNA in the repression of transposition in Drosophila virilis

Abstract

Hybrid dysgenesis in Drosophila is a syndrome of gonadal atrophy, sterility, and male recombination, and it occurs in the progeny of crosses between males that harbor certain transposable elements (TEs) and females that lack them. Known examples of hybrid dysgenesis in Drosophila melanogaster result from mobilization of individual families of TEs, such as the P element, the I element, or hobo. An example of hybrid dysgenesis in Drosophila virilis is unique in that multiple, unrelated families of TEs become mobilized, but a TE designated Penelope appears to play a major role. In all known examples of hybrid dysgenesis, the paternal germ line transmits the TEs in an active state, whereas the female germ line maintains repression of the TEs. The mechanism of maternal maintenance of repression is not known. Recent evidence suggests that the molecular machinery of RNA interference may function as an important host defense against TEs. This protection is mediated by the action of endogenous small interfering RNAs (siRNAs) composed of dsRNA molecules of 21-25 nt that can target complementary transcripts for destruction. In this paper, we demonstrate that endogenous siRNA derived from the Penelope element is maternally loaded in embryos through the female germ line in D. virilis. We also present evidence that the maternal inheritance of these endogenous siRNAs may contribute to maternal repression of Penelope.hybrid dysgenesis ͉ maternal effect ͉ RNA interference ͉ transposable element

RNAi of met1 Reduces DNA Methylation and Induces Genome-Specific Changes in Gene Expression and Centromeric Small RNA Accumulation in Arabidopsis Allopolyploids

“…In Drosophila virilis, endogenous siRNAs are derived from the transposon Penelope in both males and females but only maternally loaded in embryos, which may suggest maternal transmission of Penelope siRNA in the repression of transposition (Blumenstiel and Hartl 2005). A. thaliana homeologous-specific changes in DNA methylation and small RNA accumulation in allopolyploids may be similar to the maternal repression of transposons because A. thaliana is used as a maternal parent in production of allotetraploids (Comai et al 2000;Wang et al 2004).…”

Cytotype Regulation by TelomericPElements inDrosophila melanogaster: Evidence for Involvement of an RNA Interference Gene

“…It has also been implicated in the control of transposable genetic elements. In Drosophila melanogaster, for example, RNAi appears to regulate the levels of RNAs derived from several kinds of retrotransposons, including elements with long terminal repeats and elements without these repeats (Vagin et al 2006), and in D. virilis, it has been implicated in the regulation of the retroelement Penelope (Blumenstiel and Hartl 2005). In this article, we test the hypothesis that the P element, an important cut-and-paste transposon in the D. melanogaster genome, is regulated by RNAi.…”

Conserved themes in small-RNA-mediated transposon control

“…In flies and fish, Piwi proteins and their associated piRNAs are maternally loaded into embryos [40,44,141,142]. Although the consequences of this can only be hypothesized, the analysis of fly hybrid dysgenic (see Glossary) crosses provides additional clues [143]. When reactive females (i.e.…”