A histone methyltransferase-independent function of PRC2 controls small RNA dynamics during programmed DNA elimination in Paramecium

To limit transposable element (TE) mobilization, most eukaryotes have evolved small RNAs to silence TE activity via homology-dependent mechanisms. Small RNAs, 20–30 nucleotides in length, bind to PIWI proteins and guide them to nascent transcripts by sequence complementarity, triggering the recruitment of histone methyltransferase enzymes on chromatin to repress the transcriptional activity of TEs and other repeats. In the ciliate Paramecium tetraurelia, 25-nt scnRNAs corresponding to TEs recruit Polycomb Repressive Complex 2 (PRC2), and trigger their elimination during the formation of the somatic nucleus. Here, we sequenced sRNAs during the entire sexual cycle with unprecedented resolution. Our data confirmed that scnRNAs are produced from the entire germline genome, from TEs and non-TE sequences, during meiosis. Non-TE scnRNAs are selectively degraded, which results in the specific selection of TE-scnRNAs. We demonstrate that PRC2 is essential for the selective degradation of non-TE-scnRNAs, independently of its histone methyltransferase activity. We further show that the PRC2 cofactor Rf4 is required for the physical interaction between the scnRNA-binding protein Ptiwi09 and the zinc finger protein Gtsf1, pointing to an architectural role of PRC2 in scnRNA degradation.