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, guide PIWI proteins to which they bind, to nascent transcript by sequence complementary, recruit histone methyltransferase enzymes on chromatin and 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 precision. Our data confirmed that scnRNAs are produced from the entire germline genome, from TEs and non-TE sequences, during meiosis. Non-TE sRNAs are selectively degraded, which results in the specific selection of TE-scnRNAs. We provided important mechanistic insight into the scnRNA selection pathway by identifying PRC2 and its cofactors as essential for the selective degradation of non TE-scnRNAs. Our findings indicate a new mechanism for PRC2 that involves a non-methyltransferase function for regulating small RNA dynamics during development.

This work was supported by the Centre National de la Recherche Scientifique, the Agence Nationale pour la Recherche (ANR) [project "LaMarque" ANR-18-CE12-0005 to SD] and [project "POLYCHROME" ANR-19-CE12-0015 to SD and OA]; the LABEX Who Am I? to SD (ANR-11-LABX-0071; ANR-11-IDEX-0005-02); the Fondation de la Recherche Médicale "Equipe FRM EQU202203014643" to SD. CMP was recipient of PhD fellowships from Université Paris Cité and Fondation ARC, and a LABEX Who Am I? transition postdoc fellowship, OC was recipient of PhD fellowships from Université Paris Cité and Fondation de la Recherche Médicale and of a EUR GENE transition postdoc fellowship.