TheflamencoLocus Controls thegypsyandZAMRetroviruses and Is Required for Drosophila Oogenesis

Abstract

In Drosophila, the as yet uncloned heterochromatic locus flamenco (flam) controls mobilization of the endogenous retrovirus gypsy through the repeat-associated small interfering (rasi) RNA silencing pathway. Restrictive alleles (flamR) downregulate accumulation of gypsy transcripts in the somatic follicular epithelium of the ovary. In contrast, permissive alleles (flamP) are unable to repress gypsy. DIP1, the closest transcription unit to a flam-insertional mutation, was considered as a good candidate to be a gypsy regulator, since it encodes a dsRNA-binding protein. To further characterize the locus we analyzed P-induced flam mutants and generated new mutations by transposon mobilization. We show that flam is required somatically for morphogenesis of the follicular epithelium, the tissue where gypsy is repressed. This developmental activity is necessary to control gypsy and another retroelement, ZAM. We also show that flam is not DIP1, as none of the new permissive mutants affect the DIP1 coding sequence. In addition, two deletions removing DIP1 coding sequences do not affect any of the flamenco functions. Our results suggest that flamenco extends proximally to DIP1, spanning >130 kb of transposon-rich heterochromatin. We propose a model explaining the multiple functions of this large heterochromatic locus.

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

“…The recognition of somatic piRNA clusters allowed us (1) to distinguish populations of maternally transmitted and ovary-restricted piRNAs in the animal, and (2) to demonstrate that somatic TE master loci such as flamenco are processed by a primary piRNA biogenesis mechanism that does not rely upon ping-pong exchange. These findings correlate well with genetic evidence that flamenco restricts gypsy, ZAM, and idefix specifically in somatic follicle cells (Prud'homme et al 1995;Mevel-Ninio et al 2007), and that gypsy and ZAM have indeed adopted a specific habitat in follicle cells (Pelisson et al 1994;Leblanc et al 2000). Taken together, these observations suggest that the primary piRNA pathway and specialized master clusters evolved in concert with the colonization of a follicular niche by specific TEs.…”

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

“…In addition to our real-time PCR results, other studies also demonstrated that piRNAs can repress activities of retrotransposons such as gypsy, Idefix, ZAM, roo, mdg1, copia, I element, and Het-A (Sarot et al 2004;Vagin et al 2006;Klenov et al 2007;Mevel-Ninio et al 2007;Pelisson et al 2007;Brennecke et al 2008;Chambeyron et al 2008;Desset et al 2008). Using whole-genome tiling microarrays and quantitative RT-PCR, Li et al (2009) found that expression levels of a large number of retrotransposon families are upregulated in the absence of AGO3.…”

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]. The other genetically characterized piRNA locus is X-TAS, which is located in the pericentromeric region of the X chromosome.…”