Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene.

Abstract

Gypsy displays striking similarities to vertebrate retroviruses, including the presence of a yet uncharacterized additional open reading frame (ORF3) and the recent evidence for infectivity. It is mobilized with high frequency in the germline of the progeny of females homozygous for the flamenco permissive mutation. We report the characterization of a gypsy subgenomic ORF3 RNA encoding typical retroviral envelope proteins. In females, env expression is strongly repressed by one copy of the non‐permissive allele of flamenco. A less dramatic reduction in the accumulation of other transcripts and retrotranscripts is also observed. These effects correlate well with the inhibition of gypsy transposition in the progeny of these females, and are therefore likely to be responsible for this phenomenon. The effects of flamenco on gypsy expression are apparently restricted to the somatic follicle cells that surround the maternal germline. Moreover, permissive follicle cells display a typically polarized distribution of gypsy RNAs and envelope proteins, both being mainly accumulated at the apical pole, close to the oocyte. We propose a model suggesting that gypsy germinal transposition might occur only in individuals that have maternally inherited enveloped gypsy particles due to infection of the maternal germline by the soma.

Conserved themes in small-RNA-mediated transposon control

“…The first corresponds to the flamenco locus [43], which was long known to be required for the repression of several transposon families such as Gypsy, Idéfix and ZAM [51][52][53]. flamenco piRNAs associate almost exclusively with one Piwi family member, Piwi itself, and, consistent with their sharing a common function, flamenco and piwi mutants show overlapping phenotypes, with both showing severe defects in ovary development [54,55].…”

Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters

“…It is proximal to the DISCO interacting protein 1 gene (DIP1) and close to pericentromeric heterochromatin. Before the identification of piRNAs, this locus had been shown to regulate the Gypsy retrotransposon (7,8 (9) and for Gypsy and ZAM in flam mutant lines (11). Brennecke et al (6) showed the potential for the flam cluster to produce 79% of all ovarian piRNAs that target ZAM and 30% and 33% of those matching Idefix and Gypsy, respectively.…”

Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line

“…A long history of genetic analyses of D. melanogaster oogenesis (Gillespie and Berg 1995;Cox et al 1998;Harris and Macdonald 2001;Cook et al 2004;Pane et al 2007) and TE control (Rubin et al 1982;Bucheton et al 1984;Pelisson et al 1994;Prud'homme et al 1995) proved to uncover many of the key features and factors involved in the piRNA pathway. Recent cloning of small RNAs associated with Piwi-subclass proteins provided mechanistic insight into piRNA biogenesis in Drosophila (Saito et al 2006;Vagin et al 2006;Brennecke et al 2007;Gunawardane et al 2007;Nishida et al 2007) and vertebrates (Aravin et al 2006Girard et al 2006;Grivna et al 2006;Lau et al 2006).…”