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RNAi-dependent Polycomb repression controls transposable elements in Tetrahymena [RNA-seq]

ABSTRACT: RNA interference (RNAi) and Polycomb repression play evolutionarily conserved and often coordinated roles in transcriptional silencing. Here we show that in the protozoan Tetrahymena thermophila, germ line-specific internally eliminated sequences (IES) - many related to transposable elements (TE) - are transcriptionally activated in mutants deficient in the RNAi-dependent Polycomb repression pathway. Mobilization of recently duplicated TE also dramatically increases in these mutants. Importantly, transcriptional silencing and activation of TE-related sequences are accompanied by switching between noncoding RNA (ncRNA) and mRNA production, which can be affected by co-transcriptional processing as well as RNAi and Polycomb repression. We posit that interplay between RNAi and Polycomb repression is a widespread phenomenon, whose ancestral role is epigenetic silencing of TE.

ORGANISM(S): Tetrahymena thermophila

PROVIDER: GSE118199 | GEO | 2019/03/01

REPOSITORIES: GEO

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RNAi-dependent Polycomb repression controls transposable elements in Tetrahymena [small RNA-seq]

Project description:RNA interference (RNAi) and Polycomb repression play evolutionarily conserved and often coordinated roles in transcriptional silencing. Here we show that in the protozoan Tetrahymena thermophila, germ line-specific internally eliminated sequences (IES)—many related to transposable elements (TE)—are transcriptionally activated in mutants deficient in the RNAi-dependent Polycomb repression pathway. Mobilization of recently duplicated TE also dramatically increases in these mutants. Importantly, transcriptional silencing and activation of TE-related sequences are accompanied by switching between noncoding RNA (ncRNA) and mRNA production, which can be affected by co-transcriptional processing as well as RNAi and Polycomb repression. We posit that interplay between RNAi and Polycomb repression is a widespread phenomenon, whose ancestral role is epigenetic silencing of TE.

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Investigation of the timing of secondary small RNA biogenesis during programmed DNA elimination in Tetrahymena

Project description:Signal amplification of the initial small RNA trigger is important to ensure the silencing of repetitive transposable elements (TEs). Curiously, secondary small RNA biogenesis occurs by various mechanisms that are coupled with distinct steps of TE silencing in different eukaryotes, such as nucleolytic cleavage of TE transcripts, recruitment of RNA-dependent RNA polymerase, and heterochromatin-directed transcription. How such a variety of small RNA amplification mechanisms has evolved has not been thoroughly elucidated to date. Ciliated protozoa perform small RNA-directed programmed DNA elimination of thousands of TE-related internal eliminated sequences (IESs) in the newly developed somatic nucleus. In the ciliate Paramecium, secondary small RNAs are produced after primary small RNAs induce the excision of IESs. To examine whether such post-excision production of secondary small RNAs is conserved, we investigate the causality between the excision of IESs and the biogenesis of secondary small RNAs in another ciliate, Tetrahymena. We show that secondary small RNAs accumulate at least a few hours before their derived IESs are excised and that DNA excision is dispensable for their biogenesis in this ciliate. Therefore, unlike the situation in Paramecium, small RNA amplification occurs prior to IES excision in Tetrahymena. This study reveals remarkable mechanistic diversity of secondary small RNA biogenesis mechanisms, even among ciliates showing similar DNA elimination processes, and thus raises the possibility that the evolution of TE-targeting small RNA amplification can be traced by investigating the DNA elimination mechanisms of ciliates.

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RNAi-dependent Polycomb repression controls transposable elements in Tetrahymena

Project description:RNAi-dependent Polycomb repression controls transposable elements in Tetrahymena

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Project description:• Polycomb (PcG) regulation is crucial for development across eukaryotes, but how PcG targets are specified is still incompletely understood. The slow timescale of cold-induced Polycomb Repressive Complex 2 silencing during vernalization at Arabidopsis thaliana FLOWERING LOCUS C (FLC) provides an excellent system to elucidate the sequence of events. Association of the DNA binding protein VAL1 to an FLC intronic RY motif within the PcG nucleation region is an important step. VAL1 is associated in vivo with APOPTOSIS AND SPLICING ASSOCIATED PROTEIN (ASAP) complex and Polycomb Repressive Complex 1 (PRC1). Here, we show that ASAP and PRC1 functions are necessary for co-transcriptional repression and chromatin regulation during FLC silencing. ASAP mutants affect FLC transcription in warm conditions, but the rate of FLC silencing in the cold is unaffected. PRC1-mediated H2Aub accumulation increases at the nucleation region upon exposure to cold, but unlike the PRC2-delivered H3K27me3 does not spread across the locus. H2Aub is thus involved in the transition to epigenetic silencing at FLC facilitating H3K27me3 accumulation, which in turn is necessary for long-term epigenetic memory. Overall, our work highlights the importance of the DNA sequence-specific binding protein VAL1 as an assembly platform coordinating the co-transcriptional repression and chromatin regulation necessary for the epigenetic silencing of FLC.

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2022-08-15 | PXD036057 |

H2A ubiquitination is essential for Polycomb Repressive Complex 1-mediated gene regulation in Marchantia polymorpha

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