An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation

Gao, Zhihuan; Liu, Hailiang; Daxinger, Lucia; Pontes, Olga; He, Xin‐Jian; Qian, Weiqiang; Lin, Huixin; Xie, Mingtang; Lorković, Zdravko J.; Zhang, Shoudong; Miki, Daisuke; Zhan, Xiangqiang; Pontier, Dominique; Lagrange, Thierry; Jin, Hailing; Matzke, A. J. M.; Matzke, Marjori; Pikaard, Craig S.; Zhu, Jian‐Kang

doi:10.1038/nature09025

Cited by 225 publications

(242 citation statements)

References 29 publications

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“…However, further studies showed that Pol II and not Pol V is responsible for transcribing the noncoding RNA scaffold required for assembling the TGS complex (46). This alternative model is supported by a recent report showing that Pol II is associated with Ago4 at the TGS target sites in the nucleus (47). The same study also identified a new protein, RDM1, which binds single strands of methylated DNA that are unwound during Pol V-or Pol II-mediated transcription.…”

Section: Molecular Interaction Network Centered On Argonaute Proteinsupporting

confidence: 71%

Phylogenetic Comparison of Small RNA-triggered Transcriptional Gene Silencing

Zhang

Rossi

2011

Journal of Biological Chemistry

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The discovery of RNA interference has revealed complex roles for small RNAs in regulating gene expression and cellular physiology. Small RNAs have been demonstrated to be involved in post-transcriptional suppression of translation, targeted degradation of messenger RNAs, and transcriptional suppression via epigenetic modifications of histones and DNA. In fission yeast, RNAi mediates suppression of centromeric transcripts, whereas in plants, transcriptional gene silencing appears to be primarily an antiviral mechanism. In mammals, the well annotated functional role of RNAi is primarily post-transcriptional, but there is increasing evidence that this mechanism can also work to suppress or modulate gene transcription, although it is not clear what primary function this serves. We overview, compare, and contrast the transcriptional silencing pathways in yeast, plants, and mammals in this article. This minireview is intended to provide the reader with a framework of how the RNAi machinery appears to be universally involved in various aspects of transcriptional regulation with discussions of similarities and differences in the components and mechanisms of achieving transcriptional silencing.The phenomenon of siRNA-triggered transcriptional gene silencing (TGS) 2 is conserved across different phyla. In the fission yeast Schizosaccharomyces pombe, siRNA TGS is associated closely with heterochromatin-related gene silencing (1). In the plant Arabidopsis thaliana, siRNA-mediated TGS is associated with the establishment and maintenance of DNA methylation (RNA-directed DNA methylation) (2). In mammalian cells, studies of siRNA-triggered TGS have thus far focused only on the transcriptional silencing of protein-encoding genes via the application of promoter-targeted siRNAs (3). Although different organisms have developed diversified protein players in this process, some commonly shared features exist, especially the argonaute proteins. In general, the mechanism of siRNA TGS is composed of three mutually related parts: 1) the biogenesis and amplification of siRNA triggers, 2) molecular interactions involving an Argonaute Protein and a noncoding or coding RNA, and 3) the accompanied epigenetic changes such as histone modifications and DNA methylation. Biogenesis and Amplification of siRNA TriggersGenetic studies have contributed to establishing a correlation between RNAi and TGS (1, 2). Post-TGS (PTGS) and TGS share some of the same machinery to produce the siRNA triggers (4). In S. pombe, the major RNAi proteins for siRNA production during PTGS and TGS are identical, including the argonaute protein Ago1, the RNase III enzyme Dicer (Dcr1), and an RNA-dependent RNA polymerase (Rdp1), all of which are derived from single-copy genes (5). In contrast, the plant A. thaliana has developed a more complex system in which the argonaute proteins Ago4 and Ago6, the nuclear Dicer enzyme DCL2-4, and the RNA-dependent RNA polymerase Rdr2 are all required for TGS (6 -9). The siRNA triggers for TGS in plants are mainly 24 nucleotides in leng...

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Section: Molecular Interaction Network Centered On Argonaute Proteinsupporting

confidence: 71%

Phylogenetic Comparison of Small RNA-triggered Transcriptional Gene Silencing

Zhang

Rossi

2011

Journal of Biological Chemistry

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“…Correlation of CCA1 repression with growth vigor is confirmed in Arabidopsis hybrids (Miller et al, 2012;Shen et al, 2012). This repression of the CCA1 expression peak is established during embryo development, which requires AGO4 and other components such as NRPD1a in RdDM (Gao et al, 2010;Law and Jacobsen, 2010). Quantitative variation of CHH methylation levels in the regulatory motif (GTBS) of the CCA1 promoter region correlates with CCA1 expression amplitudes and depends on the NRPD1a-and AGO4-mediated pathway, possibly through interactions with 24-nucleotide siRNAs.…”

Section: A Model For Parent-of-origin Effects On Altered Circadian Rhmentioning

confidence: 83%

“…In the RdDM pathway (Law and Jacobsen, 2010;Haag and Pikaard, 2011), AGO4 controls locus-specific methylation of CHH and CHG sites (Zilberman et al, 2004;Gao et al, 2010). We first tested if CCA1:LUC expression is altered in the ago4-1 mutant.…”

Section: Chh Methylation and Ago4 Affect Parent-of-origin Effects On mentioning

confidence: 99%

“…Double-stranded siRNAs are amplified through RNA-DEPENDENT RNA POLYMERASE2 and cleaved by the endoribonuclease DICER-LIKE3. These siRNAs are then loaded onto ARGONAUTE4 (AGO4), and AGO4-associated siRNAs are predicted to guide the de novo methyltransferase activity of DOMAINS REARRANGED METHYLASE2 (Zilberman et al, 2004;Gao et al, 2010), leading to RdDM (Haag and Pikaard, 2011;Law et al, 2013). The maintenance of DNA methylation requires METHYLTRANSFERASE1 (MET1), which encodes a DNA methyltransferase, as well as DECREASE IN DNA METHYLATION1 (DDM1), which is a SWI/SNF2-like chromatin-remodeling protein (Jeddeloh et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

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A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis inArabidopsisIntraspecific Hybrids

Miller

et al. 2014

The Plant Cell

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Hybrid plants and animals often show increased levels of growth and fitness, a phenomenon known as hybrid vigor or heterosis. Circadian rhythms optimize physiology and metabolism in plants and animals. In plant hybrids and polyploids, expression changes of the genes within the circadian regulatory network, such as CIRCADIAN CLOCK ASSOCIATED1 (CCA1), lead to heterosis. However, the relationship between allelic CCA1 expression and heterosis has remained elusive. Here, we show a parent-of-origin effect on altered circadian rhythms and heterosis in Arabidopsis thaliana F1 hybrids. This parent-of-origin effect on biomass heterosis correlates with altered CCA1 expression amplitudes, which are associated with methylation levels of CHH (where H = A, T, or C) sites in the promoter region. The direction of rhythmic expression and hybrid vigor is reversed in reciprocal F1 crosses involving mutants that are defective in the RNA-directed DNA methylation pathway (argonaute4 and nuclear RNA polymerase D1a) but not in the maintenance methylation pathway (methyltransferase1 and decrease in DNA methylation1). This parent-of-origin effect on circadian regulation and heterosis is established during early embryogenesis and maintained throughout growth and development.

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“…The secondary siRNAs are produced from methylated loci, which are associated predominately with short repetitive sequences in intergenic regions (Lee et al, 2012), for reinforcement and possibly spreading of methylation (Pontier et al, 2005;Matzke et al, 2009;Kanno et al, 2010). RDM1 was found to bind single-stranded methylated DNA and help the recruitment of the silencing complex to methylated DNA (Gao et al, 2010). AGO4 in the complex cuts Pol II and Pol V transcripts that are complementary to the initial trigger siRNAs.…”

Section: Protein Cellmentioning

confidence: 99%

siRNA-mediated DNA methylation and H3K9 dimethylation in plants

2013

Protein Cell

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Heterochromatic siRNAs regulate transcriptional gene silencing by inducing DNA methylation and histone H3K9 dimethylation. Recent advances have revealed the distinct phases involved in siRNA mediated silencing pathway, although the precise functions of a number of factors remain undesignated, putative mechanisms for the connection between DNA and histone methylation have been investigated, and much effort has been invested to understand the biological functions of siRNA-mediated epigenetic modifi cation. In this review, we summarize the mechanism of siRNA-mediated epigenetic modification, which involves the production of siRNA and the recruitments of DNA and histone methytransferases to the target sequences assisted by complementary pairing between 24-nt siRNAs and nascent scaffold RNAs, the roles of siRNAmediated epigenetic modifi cation in maintaining genome stability and regulating gene expression have been discussed, newly identified players of the siRNA mediated silencing pathway have also been introduced.

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An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation

Cited by 225 publications

References 29 publications

Phylogenetic Comparison of Small RNA-triggered Transcriptional Gene Silencing

Phylogenetic Comparison of Small RNA-triggered Transcriptional Gene Silencing

A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis inArabidopsisIntraspecific Hybrids

siRNA-mediated DNA methylation and H3K9 dimethylation in plants

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