Telomeric Trans-Silencing: An Epigenetic Repression Combining RNA Silencing and Heterochromatin Formation

Abstract

The study of P-element repression in Drosophila melanogaster led to the discovery of the telomeric Trans-Silencing Effect (TSE), a repression mechanism by which a transposon or a transgene inserted in subtelomeric heterochromatin (Telomeric Associated Sequence or TAS) has the capacity to repress in trans in the female germline, a homologous transposon, or transgene located in euchromatin. TSE shows variegation among egg chambers in ovaries when silencing is incomplete. Here, we report that TSE displays an epigenetic transmission through meiosis, which involves an extrachromosomal maternally transmitted factor. We show that this silencing is highly sensitive to mutations affecting both heterochromatin formation (Su(var)205 encoding Heterochromatin Protein 1 and Su(var)3–7) and the repeat-associated small interfering RNA (or rasiRNA) silencing pathway (aubergine, homeless, armitage, and piwi). In contrast, TSE is not sensitive to mutations affecting r2d2, which is involved in the small interfering RNA (or siRNA) silencing pathway, nor is it sensitive to a mutation in loquacious, which is involved in the micro RNA (or miRNA) silencing pathway. These results, taken together with the recent discovery of TAS homologous small RNAs associated to PIWI proteins, support the proposition that TSE involves a repeat-associated small interfering RNA pathway linked to heterochromatin formation, which was co-opted by the P element to establish repression of its own transposition after its recent invasion of the D. melanogaster genome. Therefore, the study of TSE provides insight into the genetic properties of a germline-specific small RNA silencing pathway.

Repeat elements and the Arabidopsis DNA methylation landscape

“…In at least one case, in Drosophila, progressive effects over successive generations have been reported (Josse et al, 2007), providing interesting parallels with the scenario presented above.…”

Paramutation inDrosophilaRequires Both Nuclear and Cytoplasmic Actors of the piRNA Pathway and InducesCis-spreading of piRNA Production

“…lacZ expression assays were carried out using X-gal overnight staining as described in Lemaitre et al (1993), except that ovaries were fixed for 8 min. Transsilencing was quantified as previously described by determining the percentage of egg chambers with no lacZ expression in the germline (Josse et al 2007). It is referred to as the trans-silencing effect percentage (TSE %).…”

Transposon silencing: The extraordinary epigenetics of a transposon trap

“…I n a recent paper, Josse et al (2007) bring us closer to understanding the molecular basis of a powerful defence system against selfish DNA.…”

“…Using flies in which a reporter lacZ transgene is silenced by the TSE, Josse et al (2007) obtain a quantitative measure of its strength by assessing the proportion of egg chambers showing no lacZ expression. They find that the TSE uses a cytoplasmic factor, which accumulates over several generations in the female germline.…”

“…However, it does not matter which parent transmits the telomeric P. This rules out imprinting as a possible mechanism, so Josse et al (2007) investigate whether RNA interference is responsible. By determining which of the several mutations in distinct RNAi pathways affect the TSE, they show that the epigenetic effect is probably based on repeat associated small interfering RNA, a recently discovered small RNA pathway implicated in transposon silencing in the germline (Vagin et al, 2006).…”