Dual Binding of Chromomethylase Domains to H3K9me2-Containing Nucleosomes Directs DNA Methylation in Plants

Du, Jiamu; Zhong, Xuehua; Bernatavichute, Yana V.; Stroud, Hume; Feng, Suhua; Caro, Elena; Vashisht, Ajay A.; Terragni, Jolyon; Chin, Hang Gyeong; Tu, Andy; Hetzel, Jonathan; Wohlschlegel, James A.; Pradhan, Sriharsa; Patel, Dinshaw J.; Jacobsen, Steven E.

doi:10.1016/j.cell.2012.07.034

Cited by 447 publications

(535 citation statements)

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“…1B and 2C). It has been proposed that CMT3 could have some de novo methyltransferase activity in vivo (8). In addition, the drm1 drm2 cmt3 mutant still retains a substantial amount of CHH methylation in pericentromeric regions (34), indicating a yet unidentified DNA methyltransferase for CHH methylation.…”

Section: Discussionmentioning

confidence: 97%

“…An example of cross-talk between histone H3 lysine 9 dimethylation (H3K9me2) and CHG methylation is implemented by a positive feedback loop involving the DNA methyltransferase CMT3 and histone methyltransferase KYP (KRYPTONITE). CMT3 contains bromo adjacent homology and chromo domains that bind to H3K9me2 and catalyzes CHG methylation (8), whereas KYP harbors SET-and RING-associated domains that bind to CHG and CHH methylation and methylates histone H3K9 (9). Several histone-modifying enzymes including the histone deacetylase HDA6 (10), the putative histone demethylase JMJ14 (JUMONJI 14) (11,12) and histone H2B deubiquitination enzyme UBP26/SUP32 (UBIQUITIN PROTEASE 26, also known as SUP32) (13) have been shown to affect DNA methylation and/or transcriptional silencing of RdDM target loci.…”

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confidence: 99%

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DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV

Zhang

Yang

Zeng

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

164

179

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DNA methylation is an important epigenetic mark in many eukaryotic organisms. De novo DNA methylation in plants can be achieved by the RNA-directed DNA methylation (RdDM) pathway, where the plant-specific DNA-dependent RNA polymerase IV (Pol IV) transcribes target sequences to initiate 24-nt siRNA production and action. The putative DNA binding protein DTF1/SHH1 of Arabidopsis has been shown to associate with Pol IV and is required for 24-nt siRNA accumulation and transcriptional silencing at several RdDM target loci. However, the extent and mechanism of DTF1 function in RdDM is unclear. We show here that DTF1 is necessary for the accumulation of the majority of Pol IV-dependent 24-nt siRNAs. It is also required for a large proportion of Pol IV-dependent de novo DNA methylation. Interestingly, there is a group of RdDM target loci where 24-nt siRNA accumulation but not DNA methylation is dependent on DTF1. DTF1 interacts directly with the chromatin remodeling protein CLASSY 1 (CLSY1), and both DTF1 and CLSY1 are associated in vivo with Pol IV but not Pol V, which functions downstream in the RdDM effector complex. DTF1 and DTF2 (a DTF1-like protein) contain a SAWADEE domain, which was found to bind specifically to histone H3 containing H3K9 methylation. Taken together, our results show that DTF1 is a core component of the RdDM pathway, and suggest that DTF1 interacts with CLSY1 to assist in the recruitment of Pol IV to RdDM target loci where H3K9 methylation may be an important feature. Our results also suggest the involvement of DTF1 in an important negative feedback mechanism for DNA methylation at some RdDM target loci.histone modifications | small RNA | gene silencing | transposon D NA cytosine methylation is a conserved epigenetic mark that plays important roles in maintaining genome stability, transcriptional gene silencing, and developmental regulation (1, 2). In plants, DNA methylation occurs in three sequence contexts: CG, CHG, and CHH (H = A, C, T). CG and CHG methylation are symmetric in sequence and are maintained through a semiconservative mechanism that requires the DNA methyltransferases (METHYLTRANSFERASE 1) (MET1) and CHROMOMETHYLASE 3 (CMT3), respectively. In contrast, the asymmetric CHH methylation needs to be established during each cell cycle (1, 2). In plants a 24-nt small interfering RNA (siRNA)-dependent DNA methylation pathway is involved in recruiting the de novo DNA methyltransferase DOMAINS REARRANGED METHYLASE 2 (DRM2) and is responsible for DNA methylation at many transposable elements and repetitive sequences (3, 4).Two plant-specific homologs of RNA polymerase II play important roles in the RNA-directed DNA methylation (RdDM) pathway (5). RNA polymerase IV presumably initiates 24-nt siRNA biogenesis by specifically transcribing RdDM target loci to produce single-stranded RNA (ssRNA) transcripts, which serve as templates for RNA-dependent RNA polymerase 2 (RDR2) to generate double-stranded RNAs (dsRNAs). CLASSY 1 (CLSY1), a putative ATP-dependent chromatin remodeling protein, is prop...

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Section: Discussionmentioning

confidence: 97%

mentioning

confidence: 99%

DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV

Zhang

Yang

Zeng

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

164

179

View full text Add to dashboard Cite

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“…CHG methylation is tightly linked to histone methylation and is maintained by a positive feedback loop. The histone methyltransferases KYP, SUVH5 and SUVH6 bind to methylated CHG and catalyze methylation on histone H3 lysine 9 (H3K9me2) [7][8][9]; the plant-specific DNA methyltransferase CMT3 binds to this mark and promotes CHG methylation [10,11]. The asymmetric CHH methylation is maintained by two different DNA methyltransferases, CMT2 and DRM2.…”

Section: Introductionmentioning

confidence: 99%

Dicer-independent RNA-directed DNA methylation in Arabidopsis

et al. 2015

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RNA-directed DNA methylation (RdDM) is an important de novo DNA methylation pathway in plants. Small interfering RNAs (siRNAs) generated by Dicers from RNA polymerase IV (Pol IV) transcripts are thought to guide sequence-specific DNA methylation. To gain insight into the mechanism of RdDM, we performed whole-genome bisulfite sequencing of a collection of Arabidopsis mutants, including plants deficient in Pol IV (nrpd1) or Dicer (dcl1/2/3/4) activity. Unexpectedly, of the RdDM target loci that required Pol IV and/or Pol V, only 16% were fully dependent on Dicer activity. DNA methylation was partly or completely independent of Dicer activity at the remaining Pol IV-and/ or Pol V-dependent loci, despite the loss of 24-nt siRNAs. Instead, DNA methylation levels correlated with the accumulation of Pol IV-dependent 25-50 nt RNAs at most loci in Dicer mutant plants. Our results suggest that RdDM in plants is largely guided by a previously unappreciated class of Dicer-independent non-coding RNAs, and that siRNAs are required to maintain DNA methylation at only a subset of loci.

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“…CG methylation is maintained by the Dnmt1/MET1 subfamily of DNA methyltransferases, CHG methylation is mediated by the plant-specific chromomethylases (CMTs), and CHH methylation is introduced by the Dnmt3/DRM (Domains Rearranged Methyltransferase) enzymes (Goll and Bestor, 2005;Law and Jacobsen, 2010;Zhong et al, 2014). Interestingly, in a clear interplay between silencing mechanisms, chromomethylases appear to be targeted to chromosomal regions with H3K9 methylated nucleosomes via their bromo adjacent homology (BAH) and chromo domains (Du et al, 2012), whereas DRMs seem to be guided to target loci by small RNAs and certain components of the RNAi machinery (Law and Jacobsen, 2010;Zhong et al, 2014).…”

Section: Phylogenetic Analysis and Domain Organization Of Dna Methyltmentioning

confidence: 99%

“…For instance, di-or trimethylation of histone H3 lysine 9 (H3K9) or of histone H3 lysine 27 (H3K27) is often associated with silenced chromatin (Krauss, 2008;Shaver et al, 2010;Bannister and Kouzarides, 2011;Saze and Kakutani, 2011;Derkacheva and Hennig, 2014). DNA cytosine methylation also plays a role in repression and in some organisms there appears to be a complex interplay between histone tail modifications and DNA methylation in establishing a silent chromatin structure (Law and Jacobsen, 2010;Saze and Kakutani, 2011;Du et al, 2012;Zhong et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Gene silencing in microalgae: Mechanisms and biological roles

Kim

Cerutti³

2015

Bioresource Technology

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Microalgae exhibit enormous diversity and can potentially contribute to the production of biofuels and high value compounds. However, for most species, our knowledge of their physiology, metabolism, and gene regulation is fairly limited. In eukaryotes, gene silencing mechanisms play important roles in both the reversible repression of genes that are required only in certain contexts and the suppression of genome invaders such at transposons. The recent sequencing of several algal genomes is providing insights into the complexity of these mechanisms in microalgae. Collectively, glaucophyte, red, and green microalgae contain the machineries involved in repressive histone H3 lysine methylation, DNA cytosine methylation, and RNA interference. However, individual species often only have subsets of these gene-silencing mechanisms. Moreover, current evidence suggests that algal silencing systems function in transposon and transgene repression but their role(s) in gene regulation or other cellular processes remains virtually unexplored, hindering rational genetic engineering efforts.

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Dual Binding of Chromomethylase Domains to H3K9me2-Containing Nucleosomes Directs DNA Methylation in Plants

Cited by 447 publications

References 47 publications

DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV

DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV

Dicer-independent RNA-directed DNA methylation in Arabidopsis

Gene silencing in microalgae: Mechanisms and biological roles

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