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.
Highlights
Repression of transposable elements (TEs) involves complex mechanisms that can be linked to either small RNA silencing pathways or chromatin structure modifications depending on the species and/or the TE family [1,2,3,4,5,6]
We have found that this epigenetic silencing is sensitive to mutations in genes involved in heterochromatin formation and in a recently discovered silencing pathway based on small RNAs
We found that Trans-Silencing Effect (TSE) is strongly affected both by mutations in genes involved in heterochromatin formation and in the recently discovered small RNA silencing pathway called ‘‘repeat-associated small interfering RNAs’’ pathway [3,4,6,29]
Summary
Repression of transposable elements (TEs) involves complex mechanisms that can be linked to either small RNA silencing pathways or chromatin structure modifications depending on the species and/or the TE family [1,2,3,4,5,6]. Strong repression of the DNA P TE, by a cellular state that has been called ‘‘P cytotype’’ [10], can be established by one or two telomeric P elements inserted in heterochromatic ‘‘Telomeric Associated Sequences’’ (TAS) at the 1A cytological site corresponding to the left end of the X chromosome [20,21,22,23,24]. This includes repression of dysgenic sterility resulting from P transposition. P repression corresponds to a new picture of TE repression shown, using an assay directly linked to transposition, to be affected by heterochromatin and small RNA silencing mutants
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