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

ABSTRACT: 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 mediates the physical interaction between the scnRNA-binding protein Ptiwi09 and the zinc finger protein Gtsf1, pointing to an archirectural role of PRC2 in scnRNA degradation.

INSTRUMENT(S):

ORGANISM(S): Paramecium Tetraurelia

SUBMITTER: Guillaume CHEVREUX

LAB HEAD: Sandra Duharcourt

PROVIDER: PXD063336 | Pride | 2025-09-22

REPOSITORIES: Pride

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			Action	DRS
	2405003_WT_ICL7_DDA_1_S4-A9_1_11451.d.refined.mgf	Mgf
	2405003_WT_ICL7_DDA_1_S4-A9_1_11451.d.zip	Other
	2405003_WT_ICL7_DDA_2_S4-B1_1_11455.d.refined.mgf	Mgf
	2405003_WT_ICL7_DDA_2_S4-B1_1_11455.d.zip	Other
	2405003_WT_ICL7_DDA_3_S4-B5_1_11459.d.refined.mgf	Mgf

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Project description:Background: Transposable elements (TEs) represent a substantial fraction of the genomes, playing a major role in evolution, as sources of genetic variability. To fully appraise the role of TE in the acquisition of genetic novelty in genome evolution, we must also consider the impact of their own transcriptional activity. Results: We studied impact of TE transcriptional activity on gene using high-throughput RNA-Seq sequencing in Drosophila melanogaster. TEs, which turn out to be expressed in euchromatin as well as in heterochromatin, interact with genes at different levels. The observed transcription from TEs involve canonical or non-canonical transcription start sites (TSSs) distributed along their sequence. We also find evidences for potential bidirectional transcription from the TE promoter regions where the antisense transcript is co-opted by the host genome as TSSs of a gene. We found that active TEs seem to accumulate in the 5' upstream regions of the genes, and possibly provide an alternative transcript of the nearby gene. Indeed, predominantly, the TE transcript is collinear and overlapping the gene. Apart from the 5' upstream regions, we also found that most active TEs are transcribed on the gene transcript strand. Conversely, few transcripts from TE are anti sense with respect to the gene. This suggests that they have a disruptive action and are counter-selected. The only exceptions are for TEs located into introns, where they could provide another complex way of gene regulation, and in the 3' downstream region, where other mechanisms akin to siRNAs could take place. Finally, we noted several cases where the cryptic TSS is located on TE fragments corresponding to a low complexity sequence. Frequently these TE fragments appear to be over-represented when close to genes, suggesting a possible selected role. Conclusion: Altogether, these results suggest that active transposable elements influence host gene transcription. It is likely that some features of transposable elements have been exaptated in order to enrich the genes repertoire by opening routes to sub- or neo-functionalization. Examination of the transcription produced by transposable elements in D. melanogaster

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

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