Nuclear Piwi/Piwi-interacting RNA complexes mediate co-transcriptional silencing of
transposable elements by inducing local heterochromatin formation. In Drosophila,
sumoylation plays an essential role in the assembly of the silencing complex; however,
the molecular mechanism by which the sumoylation machinery is recruited to the transposon
loci is poorly understood. Here, we show that the Drosophila E3 SUMO-ligase Su(var)2-10
directly binds to the Piwi protein. This interaction is mediated by the SUMO-interacting
motif-like (SIM-like) structure in the C-terminal domain of Su(var)2-10. We demonstrated
that the SIM-like structure binds to a special region found in the MID domain of the
Piwi protein, the structure of which is highly similar to the SIM-binding pocket of
SUMO proteins. Abrogation of the Su(var)2-10-binding surface of the Piwi protein resulted
in transposon derepression in the ovary of adult flies. Based on our results, we propose
a model in which the Piwi protein initiates local sumoylation in the silencing complex
by recruiting Su(var)2-10 to the transposon loci.
