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VAL1 acts as an assembly platform co-ordinating co-transcriptional repression and chromatin regulation at Arabidopsis FLC

ABSTRACT: Polycomb (PcG) silencing is crucial for development, but how targets are specified remains incompletely understood. The cold-induced Polycomb Repressive Complex 2 (PRC2) silencing of Arabidopsis thaliana FLOWERING LOCUS C (FLC) provides an excellent system to elucidate PcG regulation. Association of the DNA binding protein VAL1 to the PcG nucleationregion at FLC is an important step. VAL1 interacts with APOPTOSIS AND SPLICING ASSOCIATED PROTEIN (ASAP) complex and PRC1. Here, we show that ASAP and PRC1 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 accumulates at FLC nucleation region during cold, but unlike the PRC2-delivered H3K27me3 does not spread across the locus. H2Aub thus marks the transition to epigenetic silencing, while H3K27me3 is necessary for long-term epigenetic memory. Overall, our work highlights the importance of VAL1 as an assembly platform co-ordinating the co-transcriptional repression and chromatin regulation necessary for the epigenetic silencing of FLC.

ORGANISM(S): Arabidopsis Thaliana

SUBMITTER: Caroline Dean

PROVIDER: PXD036057 | iProX | Mon Aug 15 00:00:00 BST 2022

REPOSITORIES: iProX

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VAL1 acts as an assembly platform co-ordinating co-transcriptional repression and chromatin 2 regulation at Arabidopsis FLC

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.

2022-10-13 | PXD036548 | Pride

piRNA-guided co-transcriptional silencing coopts nuclear export factors

Project description:The PIWI-interacting RNA (piRNA) pathway is a small RNA-based immune system that controls the expression of transposons and maintains genome integrity in animal germlines1,2. In Drosophila, piRNA-guided silencing is achieved, in part, via co-transcriptional repression of transposons by Piwi. This depends on Panoramix (Panx)3,4; however, precisely how an RNA binding event silences transcription remains to be determined. Here we show that Nuclear Export Factor 2 (Nxf2) and its co-factor, Nxt1, form a complex with Panx, and are required for co-transcriptional silencing of transposons in somatic and germline cells of the ovary. Tethering of Nxf2 to either RNA or DNA results in silencing of target loci and the concomitant accumulation of repressive chromatin marks. Nxf2 and Panx proteins are mutually required for proper localization and stability. We mapped the protein domains crucial for the Nxf2/Panx complex formation and show that the amino-terminal portion of Panx is sufficient to induce transcriptional silencing. Loss of Nxf2 or Panx results in nuclear accumulation of transposon transcripts, which is for some transposons Piwi-dependent.

2019-06-20 | PXD011415 | Pride

Dimerisation of the PICTS complex via LC8/Cut-up drives co-transcriptional transposon silencing in Drosophila

Project description:In animal gonads, the PIWI-interacting RNA (piRNA) pathway guards genome integrity in part through the co-transcriptional gene silencing of transposon insertions. In Drosophila ovaries, piRNA-loaded Piwi detects nascent transposon transcripts and instructs heterochromatin formation through the Panoramix-induced co-transcriptional silencing (PICTS) complex, containing Panoramix, Nxf2 and Nxt1. Here, we report that the highly conserved dynein light chain LC8/Cut-up (Ctp) is an essential component of the PICTS complex. Loss of Ctp results in transposon de-repression and a reduction in repressive chromatin marks specifically at transposon loci. In turn, Ctp can enforce transcriptional silencing when artificially recruited to RNA and DNA reporters. We show that Ctp drives dimerisation of the PICTS complex through its interaction with conserved motifs within Panoramix. Artificial dimerisation of Panoramix bypasses the necessity for its interaction with Ctp, demonstrating that conscription of a protein from a ubiquitous cellular machinery has fulfilled a fundamental requirement for a transposon silencing complex.

2021-01-26 | PXD022105 | Pride

Dimerisation of the PICTS complex via LC8/Cut-up drives co-transcriptional transposon silencing in Drosophila

2021-01-26 | PXD022103 | Pride

The dimeric SFiNX complex enables piRNA-guided co-transcriptional silencing through molecular condensate formation

Project description:Nuclear Argonaute proteins, guided by their bound small RNAs, orchestrate heterochromatin formation at transposon insertions and repetitive genomic loci. The molecular mechanisms that, besides recruiting heterochromatin effector proteins, are required for this silencing process are poorly understood. Here, we show that the SFiNX complex, the central silencing mediator downstream of nuclear Piwi-piRNA complexes in Drosophila, enables co-transcriptional silencing via the formation of molecular condensates. Condensate formation is stimulated by nucleic acid binding and requires SFiNX to form a homodimer. The dynein light chain dLC8, a highly conserved dimerization hub protein, mediates homo-dimerization of SFiNX. Point mutations preventing dLC8-mediated SFiNX dimerization result in transposon de-repression and sterility. dLC8’s function can be bypassed with a heterologous dimerization domain, suggesting that dimerization is a constitutive rather than a regulated feature of SFiNX. We propose that nucleic-acid stimulated condensate formation enables co-transcriptional silencing through the retention of the target RNA at chromatin, thereby allowing effector proteins to establish heterochromatin at the target locus.

2021-02-12 | PXD022010 | Pride

piRNA-guided co-transcriptional silencing coopts nuclear export factors

2019-06-20 | GSE121661 | GEO

Panoramix enforces piRNA-dependent co-transcriptional silencing (RNA-Seq)

Project description:The Piwi-interacting RNA (piRNA) pathway is a small RNA-based innate immune system that defends germ cell genomes against transposons. In Drosophila ovaries, the nuclear Piwi protein is required for transcriptional silencing of transposons, though the precise mechanisms by which this occurs are unknown. Here we show that CG9754 is a component of Piwi complexes that functions downstream of Piwi and its binding partner, Asterix, in transcriptional silencing. Enforced tethering of CG9754 protein to nascent mRNA transcripts causes co-transcriptional silencing of the source locus and the deposition of repressive chromatin marks. We have named CG9754 Panoramix, and propose that this protein could act as an adaptor, scaffolding interactions between the piRNA pathway and the general silencing machinery that it recruits to enforce transcriptional repression.

2015-10-15 | GSE71371 | GEO

Panoramix enforces piRNA-dependent co-transcriptional silencing (GRO-Seq)

2015-10-15 | GSE71369 | GEO

Panoramix enforces piRNA-dependent co-transcriptional silencing (ChIP-Seq)

2015-10-15 | GSE71368 | GEO

Nuclear RNA export factor variant initiates piRNA-guided co-transcriptional silencing

Project description:PIWI-interacting RNAs (piRNAs) are germline-specific small RNAs that form effector complexes with PIWI proteins (Piwi–piRISC complexes) to preserve genomic integrity by repressing transposable elements (TEs). Among PIWI-clade proteins in Drosophila, Piwi transcriptionally silences its targets via heterochromatin formation characterised by H3K9me3 marks and the linker histone H1. Recent studies have shown that Panoramix (Panx) interacts with Piwi–piRISC complexes to induce transcriptional repression of targets mediated by the recruitment of H3K9me3 marks. Here, we identified Nxf2, a nuclear RNA export factor (NXF) variant, as a protein that forms a complex with Panx and Piwi. Nxf2 further associates with p15 (Nxt1), a co-adaptor for nuclear RNA export. However, unlike Nxf1 that plays a major role in mRNA export, Nxf2–p15 instead transcriptionally regulates TEs in the Piwi–piRNA pathway. Panx–Nxf2–p15 complex formation is necessary in the silencing by stabilizing protein levels of Nxf2 and Panx. Notably, ectopic targeting of Nxf2 initiates co-transcriptional repression of the target reporter in a manner independent of H3K9me3 marks or H1. However, continuous silencing requires HP1a and H1. The amino-terminal domain of Nxf2 harbouring RNA binding activity is essential for recruitment of the Piwi–piRISC complex to target TEs. Indeed, Nxf2 directly interacts with target TE transcripts in a Piwi-dependent manner. These findings suggest a model in which the Nxf2–Panx–p15 complex enforces the association of Piwi with target transcripts to trigger co-transcriptional repression, prior to heterochromatin formation in the nuclear piRNA pathway. Our results provide an unexpected connection between an NXF variant and small RNA-mediated co-transcriptional silencing.

2019-07-09 | GSE131950 | GEO

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