DNA Methylation Signatures of the Plant Chromomethyltransferases

Gouil, Quentin; Baulcombe, David C.

doi:10.1371/journal.pgen.1006526

Cited by 165 publications

(247 citation statements)

References 42 publications

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“…AtROS1 antagonizes RdDM in Arabidopsis (20). A recent study reported that RdDM targets in tomato are located in gene-rich euchromatin regions (37), which is similar to the distribution of SlDML2 targets (Fig. 3B), suggesting a potential antagonism between SlDML2 and RdDM in tomato as well.…”

Section: Discussionsupporting

confidence: 67%

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

Lang

YiHai

Tang

et al. 2017

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

374

409

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DNA methylation is a conserved epigenetic mark important for genome integrity, development, and environmental responses in plants and mammals. Active DNA demethylation in plants is initiated by a family of 5-mC DNA glycosylases/lyases (i.e., DNA demethylases). Recent reports suggested a role of active DNA demethylation in fruit ripening in tomato. In this study, we generated loss-of-function mutant alleles of a tomato gene, SlDML2, which is a close homolog of the Arabidopsis DNA demethylase gene ROS1. In the fruits of the tomato mutants, increased DNA methylation was found in thousands of genes. These genes included not only hundreds of ripening-induced genes but also many ripening-repressed genes. Our results show that SlDML2 is critical for tomato fruit ripening and suggest that active DNA demethylation is required for both the activation of ripeninginduced genes and the inhibition of ripening-repressed genes.DNA demethylase | 5-mC DNA glycosylase | DNA methylation | epigenetic regulation | gene silencing D NA methylation is a conserved epigenetic modification that is generally associated with inactive transcription in plants and mammals. As such, DNA methylation plays important roles in many biological processes, such as genome stability, gene imprinting, development, and response to the environment (1-3). In contrast to mammals, in which DNA methylation predominantly occurs at cytosines in the symmetric CG sequence context, plants commonly have methylation in the asymmetrical CHH sequence context (H = A, C, or T), as well as in the symmetrical CG and CHG contexts (1, 2). In plants, cytosines in all sequence contexts can be de novo methylated through the well-known RNA-directed DNA methylation pathway (RdDM), in which 24-nt siRNAs guide the DNA methyltransferase domains rearranged methyltransferase 2 (DRM2) to methylate target loci (4). DNA methylation can be maintained during replication; mCG and mCHG are maintained by the DNA methyltransferases DNA methyltransferase 1 (MET1) and chromomethylase 3 (CMT3), respectively, whereas mCHH is maintained by CMT2 and RdDM (4, 5).Cytosine methylation levels are dynamically regulated by DNA methylation and demethylation reactions (3, 6). DNA methylation can be lost either because of failure in maintaining methylation after replication (i.e., passive DNA demethylation) or because of active removal by enzymes (i.e., active DNA demethylation). Previous studies have identified and characterized several enzymes important for active DNA demethylation in Arabidopsis (7-11). The ROS1 family of bifunctional 5-methylcytosine DNA glycosylases/lyases, often referred to as DNA demethylases, initiate active DNA demethylation by removing the methylcytosine base from the DNA backbone, resulting in a single nucleotide gap that can be filled with an unmethylated cytosine through a base excision repair pathway (7,8,12,13). Several enzymes acting downstream of ROS1, such as the 3′ DNA phosphatase ZDP, AP endonuclease-like protein APE1L, and DNA ligase I (AtLIG1), have also been identified ...

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Section: Discussionsupporting

confidence: 67%

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

Lang

YiHai

Tang

et al. 2017

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

374

409

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“…Consistent with a previous report (Gouil and Baulcombe 2016), we observed that tomato methylation level is lower in the CCG subcontext than CAG and CTG at heterochromatins ( Figure S18). It was also reported that Arabidopsis met1 mutation specifically caused the loss of CCG methylation across the chromosomes, and that this effect is more pronounced in heterochromatic regions, which may be caused by MET1-mediated mCGG and CmCG that recruit SUVH5/6 that would catalyze H3K9me2, resulting in subsequent recruitment of CMT3 to methylate the first cytosine of CCG (Gouil and Baulcombe 2016). Yet it is still unclear whether tomato slmet1 mutation can cause such an effect.…”

Section: Discussionmentioning

confidence: 99%

“…On the other hand, the DNA demethylase ROS1 can antagonize methylation at both RdDM‐dependent and RdDM–independent loci (Tang et al ). In tomato plants, it has been suggested that CMT2‐dependent CHH methylation exists independently of the RdDM pathway (Gouil and Baulcombe ), and that at least one functional ROS1 homolog is present (Liu et al ; Lang et al ). In this study, we observed that in the slmet1 mutants, CHH methylation was increased in both pericentromeric regions and chromosome arms (Figure B), and that all the CHH subcontexts exhibited similar hypermethylation patterns (Figures S4–S6), suggesting that both RdDM‐dependent and CMT2‐dependent CHH methylation was affected in the slmet1 mutants.…”

Section: Discussionmentioning

confidence: 99%

Critical function of DNA methyltransferase 1 in tomato development and regulation of the DNA methylome and transcriptome

Tang

Datsenka

et al. 2019

JIPB

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DNA methylation confers epigenetic regulation on gene expression and thereby on various biological processes. Tomato has emerged as an excellent system to study the function of DNA methylation in plant development. To date, regulation and function of DNA methylation maintenance remains unclear in tomato plants. Here, we report the critical function of tomato (Solanum lycopersicum) Methyltransferase 1 (SlMET1) in plant development and DNA methylome and transcriptome regulation. Using CRISPR‐Cas9 gene editing, we generated slmet1 mutants and observed severe developmental defects with a frame‐shift mutation, including small and curly leaves, defective inflorescence, and parthenocarpy. In leaf tissues, mutations in SlMET1 caused CG hypomethylation and CHH hypermethylation on a whole‐genome scale, leading to a disturbed transcriptome including ectopic expression of many RIN target genes such as ACC2 in leaf tissues, which are normally expressed in fruits. Neither the CG hypomethylation nor CHH hypermethylation in the slmet1 mutants is related to tissue culture. Meanwhile, tissue culture induces non‐CG hypomethylation, which occurs more frequently at gene regions than at TE regions. Our results depict SlMET1‐ and tissue culture‐dependent tomato DNA methylomes, and that SlMET1 is required for maintaining a normal transcriptome and normal development of tomato.

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“…RNA interference (RNAi) leads to the accumulation of 21–24 nucleotide homologous small interfering RNAs (siRNAs) at plant TE 5′ and 3′ repeats which play a role in establishing and maintaining DNA cytosine methylation (Figure 1) [7–10]. DNA cytosine methylation of TEs occurs in CG, CHG and CHH (where H = A, C or T) sequence contexts, and the nature of bases represented by H can influence methylation frequency [11,12]. CHG and CHH methylation are largely interdependent with dimethylation of histone H3 on lysine 9 (H3K9me2) (Figure 1) [13].…”

Section: Introductionmentioning

confidence: 99%

Genetic and epigenetic variation of transposable elements in Arabidopsis

Underwood

Henderson

Martienssen

2017

Current Opinion in Plant Biology

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Transposable elements are mobile genetic elements that are prevalent in plant genomes and are silenced by epigenetic modification. Different epigenetic modification pathways play distinct roles in the control of transposable element transcription, replication and recombination. The Arabidopsis genome contains families of all of the major transposable element classes, which are differentially enriched in particular genomic regions. Whole genome sequencing and DNA methylation profiling of hundreds of natural Arabidopsis accessions has revealed that transposable elements exhibit significant intraspecific genetic and epigenetic variation, and that genetic variation often underlies epigenetic variation. Together, epigenetic modification and the forces of selection define the scope within which transposable elements can contribute to, and control, genome evolution.

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DNA Methylation Signatures of the Plant Chromomethyltransferases

Cited by 165 publications

References 42 publications

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

Critical function of DNA methyltransferase 1 in tomato development and regulation of the DNA methylome and transcriptome

Genetic and epigenetic variation of transposable elements in Arabidopsis

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