Direct interaction of Su(var)2‐10 via the SIM‐binding site of the Piwi protein is required for transposon silencing in Drosophila melanogaster

Abstract

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.