A small RNA-guided PRC2 complex eliminates DNA as an extreme form of transposon silencing

• Published in: Cell reports (Cambridge) Vol. 40; no. 8; p. 111263
• Main Authors: Wang, Chundi, Solberg, Therese, Maurer-Alcalá‬, Xyrus X., Swart, Estienne C., Gao, Feng, Nowacki, Mariusz
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 23.08.2022; Cell Press
• Subjects: Animals; Argonaute Proteins - genetics; Argonaute Proteins - metabolism; ciliates; DNA - metabolism; DNA elimination; DNA Transposable Elements - genetics; Drosophila melanogaster - metabolism; Drosophila Proteins - metabolism; Gene Silencing; H3K27me3; H3K9me3; heterochromatin; piRNA; Piwi; Polycomb Repressive Complex 2 - metabolism; PRC; RNA, Small Interfering - genetics; RNA, Small Interfering - metabolism; transposable elements; transposons; PRC; DNA elimination; H3K9me3; piRNA; ciliates; CP: Molecular biology; transposons; transposable elements; Piwi; H3K27me3; heterochromatin
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.111263

In animal germlines, transposons are silenced at the transcriptional or post-transcriptional level to prevent deleterious expression. Ciliates employ a more direct approach by physically eliminating transposons from their soma, utilizing piRNAs to recognize transposons and imprecisely excise them. Ancient, mutated transposons often do not require piRNAs and are precisely eliminated. Here, we characterize the Polycomb Repressive Complex 2 (PRC2) in Paramecium and demonstrate its involvement in the removal of transposons and transposon-derived DNA. Our results reveal a striking difference between the elimination of new and ancient transposons at the chromatin level and show that the complex may be guided by Piwi-bound small RNAs (sRNAs). We propose that imprecise elimination in ciliates originates from an ancient transposon silencing mechanism, much like in plants and metazoans, through sRNAs, repressive methylation marks, and heterochromatin formation. However, it is taken a step further by eliminating DNA as an extreme form of transposon silencing. [Display omitted] •PRC2 couples Piwi-bound small RNAs to transposon elimination in the new soma•Elimination of new and ancient transposon sequences depends on PRC2•Loss of PRC2 leads to retention and de-repression of transposons•Only new transposons require heterochromatin and small RNAs for their removal In animal germlines, the piRNA pathway silences transposons at the transcriptional level by deposition of repressive methylation marks. Wang et al. identify a PRC2 complex as the link between Piwi-bound small RNAs and DNA elimination as an extreme form of transposon silencing.