Paramecium Polycomb repressive complex 2 physically interacts with the small RNA-binding PIWI protein to repress transposable elements

Miró-Pina, Caridad; Charmant, Olivia; Kawaguchi, Takayuki; Holoch, Daniel; Michaud, Audrey; Cohen, Isadora S.; Humbert, Adeline; Jaszczyszyn, Yan; Chevreux, Guillaume; Maestro, Laurence Del; Ait‐Si‐Ali, Slimane; Arnaiz, Olivier; Margueron, Raphaël; Duharcourt, Sandra

doi:10.1016/j.devcel.2022.03.014

Cited by 36 publications

(66 citation statements)

References 79 publications

(143 reference statements)

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“…PRC2 also silences TEs in ciliates 7 and is associated with TEs in stramenopiles and fungi 16 allowing us to propose that PRC2 targeted TEs for silencing in LECA, the common ancestors of these groups. In the ciliate Paramecium aureliae the recruitment of PRC2, which deposits both H3K9me3 and H3K27me3 7 involves non-coding RNAs 8 in a manner reminiscent of the recruitment of the machinery that deposits H3K9me3 in fungi and animals 38 . In red algae H3K27me3-silenced TEs are associated with the telomeres which is reminiscent of PRC2 recruitment by TELOMERE REPEAT BINDING FACTORs (TRBs) at telobox motifs in angiosperms 39 .…”

Section: Discussionmentioning

confidence: 99%

“…TEs are marked with DNA and H3K9 methylation that are associated with silencing in flowering plants 5 , animals, and fungi 6 . Yet, in distantly related eukaryotes TEs are instead marked by H3K27me3 deposited by the Polycomb Repressive Complex 2 (PRC2) [7][8][9][10][11] , an epigenetic mark associated with gene silencing in multicellular eukaryotes [12][13][14][15] . It was therefore proposed that the ancestral activity of PRC2 was the deposition of H3K27me3 to silence TEs 16 .To test this hypothesis we obtained mutants deprived of PRC2 activity and used genomics to analyze the role of PRC2 in extant species along the lineage of Archaeplastida.…”

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confidence: 99%

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Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

Hisanaga

Romani

et al. 2022

Preprint

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The mobility of transposable elements (TEs) contributes to evolution of genomes. Meanwhile, their uncontrolled activity causes genomic instability and therefore expression of TEs is silenced by host genomes. TEs are marked with DNA and H3K9 methylation that are associated with silencing in flowering plants, animals, and fungi. Yet, in distantly related eukaryotes TEs are instead marked by H3K27me3 deposited by the Polycomb Repressive Complex 2 (PRC2), an epigenetic mark associated with gene silencing in multicellular eukaryotes. It was therefore proposed that the ancestral activity of PRC2 was the deposition of H3K27me3 to silence TEs. To test this hypothesis we obtained mutants deprived of PRC2 activity and used genomics to analyze the role of PRC2 in extant species along the lineage of Archaeplastida. While in the red alga Cyanidioschyzon merolae more TEs than genes were repressed by PRC2, an opposite trend was observed in bryophytes Marchantia polymorpha and Anthoceros agrestis. In the red alga, TEs silenced by H3K27me3 are in subtelomeres but in bryophytes, TEs and genes marked by H3K27me3 form coregulated transcriptional units. The latter trend was also observed in the flowering plant Arabidopsis thaliana, and we identified cis-elements recognised by transcription factors in TEs flanking genes repressed by PRC2. Together with the silencing of TEs by PRC2 in ciliates that diverged early from an ancestor common with Archaeplastida, our findings support the hypothesis that PRC2 deposited H3K27me3 to silence TEs in early lineages of eukaryotes. During evolution, TE fragments marked with H3K27me3 were selected to shape transcriptional regulation that control networks of genes regulated by PRC2.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

Hisanaga

Romani

et al. 2022

Preprint

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“…They act on TEs by triggering histone modifications via P-element Induced WImpy testis (PIWI) proteins or triggering transcript degradation through Argonaute proteins ( Dechaud et al, 2019 ). A recent study unearthed further details of this interaction in Paramecium whereby PIWI proteins regulate TEs through Polycomb Repressive Complex 2 ( Miró-Pina et al, 2022 ).…”

Section: Transposable Elements and Epigeneticsmentioning

confidence: 99%

The Role of Transposable Elements in Sexual Development

Chiang

DeRosa

Park

et al. 2022

Front. Behav. Neurosci.

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Up to 50% of most mammalian genomes are made up of transposable elements (TEs) that have the potential to mobilize around the genome. Despite this prevalence, research on TEs is only beginning to gain traction within the field of neuroscience. While TEs have long been regarded as “junk” or parasitic DNA, it has become evident that they are adaptive DNA and RNA regulatory elements. In addition to their vital role in normal development, TEs can also interact with steroid receptors, which are key elements to sexual development. In this review, we provide an overview of the involvement of TEs in processes related to sexual development- from TE activity in the germline to TE accumulation in sex chromosomes. Moreover, we highlight sex differences in TE activity and their regulation of genes related to sexual development. Finally, we speculate on the epigenetic mechanisms that may govern TEs’ role in sexual development. In this context, we emphasize the need to further the understanding of sexual development through the lens of TEs including in a variety of organs at different developmental stages, their molecular networks, and evolution.

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“…Similarly, in Paramecium tetraurelia , H3K27 and H3K9 methyl marks coexist in multiple TE families, and the ortholog of Ezh2, Ezl1, is implicated in their silencing [ 150 ]. Ezl1 interaction with components of small RNA/RNAi machinery appears to be responsible for its targeting of TEs [ 151 ]. It has been hypothesized that H3K27 methylation is an ancestral mechanism of TE silencing that has been largely replaced by a more stable silencing by H3K9 methylation and DNA methylation at the onset of multicellularization when the disadvantages of TE activation outweigh their possible advantages, especially in the germline.…”

Section: Chromatinmentioning

confidence: 99%

All Quiet on the TE Front? The Role of Chromatin in Transposable Element Silencing

Stefano

2022

Cells

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Transposable elements (TEs) are mobile genetic elements that constitute a sizeable portion of many eukaryotic genomes. Through their mobility, they represent a major source of genetic variation, and their activation can cause genetic instability and has been linked to aging, cancer and neurodegenerative diseases. Accordingly, tight regulation of TE transcription is necessary for normal development. Chromatin is at the heart of TE regulation; however, we still lack a comprehensive understanding of the precise role of chromatin marks in TE silencing and how chromatin marks are established and maintained at TE loci. In this review, I discuss evidence documenting the contribution of chromatin-associated proteins and histone marks in TE regulation across different species with an emphasis on Drosophila and mammalian systems.

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Paramecium Polycomb repressive complex 2 physically interacts with the small RNA-binding PIWI protein to repress transposable elements

Cited by 36 publications

References 79 publications

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

The Role of Transposable Elements in Sexual Development

All Quiet on the TE Front? The Role of Chromatin in Transposable Element Silencing

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