RNA polymerase V transcription guides ARGONAUTE4 to chromatin

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Abstract
Craig Pikaard and colleagues show that AGO4 is recruited to target loci through physical interactions with nascent RNA polymerase V transcripts. They also show that the SMC hinge-domain protein DMS3 functions in the assembly of Pol V transcription complexes. Retrotransposons and repetitive DNA elements in eukaryotes are silenced by small RNA–directed heterochromatin formation. In Arabidopsis, this process involves 24-nt siRNAs that bind to ARGONAUTE4 (AGO4) and facilitate the targeting of complementary loci1,2 via unknown mechanisms. Nuclear RNA polymerase V (Pol V) is an RNA silencing enzyme recently shown to generate noncoding transcripts at loci silenced by 24-nt siRNAs3. We show that AGO4 physically interacts with these Pol V transcripts and is thereby recruited to the corresponding chromatin. We further show that DEFECTIVE IN MERISTEM SILENCING3 (DMS3), a structural maintenance of chromosomes (SMC) hinge-domain protein4, functions in the assembly of Pol V transcription initiation or elongation complexes. Collectively, our data suggest that AGO4 is guided to target loci through base-pairing of associated siRNAs with nascent Pol V transcripts.