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1Department of Organismic and Evolutionary
Biology, Harvard University Herbaria, 22
Divinity Avenue, Cambridge, MA 02138, USA.
2Biodiversitaet der Pflanzen, Technische
Universitaet Muenchen, D-85354 Freising,
Small RNA-Directed Silencing: The
Fly Finds Its Inner Fission Yeast?
Several recent studies demonstrate that piRNAs guide Piwi protein to repress
transposon transcription in fly ovaries, much as fission yeast use siRNAs to
silence repeat sequences. Still mysterious though is how Piwi targets
euchromatic transposons for silencing, but not the specialized
heterochromatic loci that produce piRNA precursors.
Daniel Tianfang Ge
and Phillip D. Zamore
Fungi, plants, and animals devote
considerable resources to thwart
transposable elements from increasing
their numbers or moving to new
genomic locations, particularly in germ
cells. In fungi and plants, small
interfering RNAs (siRNAs) act via the
RNA interference (RNAi) pathway
to silence transposons and other
types of repetitive DNA. In contrast,
animals use PIWI-interacting
RNAs (piRNAs), a class of small
silencing RNAs distinct from siRNAs,
to silence germline transposons
and ensure fertility. Like siRNAs
and the mRNA-regulating microRNAs
(miRNAs), piRNAs direct Argonaute
proteins to silence complementary
nucleic acid targets. Unlike siRNAs
and miRNAs, piRNAs guide a
specialized sub-class of Argonautes,
the PIWI proteins, which are found
exclusively in animals and nearly
always in the germline or
In Drosophila, piRNAs bind
three different PIWI proteins:
P-element-induced wimpy testes
(Piwi), Aubergine (Aub), and
Argonaute3 (Ago3). Aub and Ago3 act
strictly in the ovary and testis germline,
where they silence transposons by
destroying their RNA transcripts. In
contrast, Piwi resides in the nucleus,
where it represses transposons in
both germ cells and their supporting
somatic cells [1–3]. Now, four papers
demonstrate that Piwi silences
transposons, at least in part, by
repressing their transcription [4–7].
These genome-scale studies support
and extend earlier evidence that Piwi
directs transcriptional silencing in the
nucleus [3,8,9]. By depleting Piwi in
the ovarian germline [5,6], ovarian
somatic follicle cells , or cultured,
immortalized ovarian somatic cells
(OSCs) , or by inserting ectopic
piRNA target sites into the fly genome
, all four studies find that piRNAs
guide Piwi to its target loci, where
it recruits enzymes that establish
(Figure 1A). The papers generally
support the view that piRNAs
tether Piwi to nascent transcripts:
RNA is required for Piwi to
co-immunoprecipitate with chromatin
 and with proteins known to bind
nascent RNA . Piwi bound to
nascent RNA via its piRNA guide
appears to recruit Su(var)3-9 , a
histone methyltransferase that
methylates histone H3 on lysine 9.
These ‘H3K9me3’ marks bind
heterochromatin protein 1 (HP1,
officially named Su(var)205),
generating chromatin that is refractory
to transcription, as reflected by
reduced occupancy with RNA
polymerase II (pol II) . Supporting
this view, depletion of Piwi reduces
the amount of H3K9me3 [4–6,9] and
HP1  and increases the amount of
RNA pol II [4,5] and nascent transcripts
[4,6,8] at transposon sequences.
These findings call to mind the
silences repetitive sequences in the
fission yeast, Schizosaccharomyces
pombe. siRNAs bound to S. pombe
Ago1 guide the ‘RITS’ complex
to nascent transcripts from
transposon-like repeats near the
centromere, where it recruits
proteins that establish repressive
Current Biology Vol 23 No 8