DNA methylation is a conserved epigenetic modification that is important for gene regulation and genome stability. Aberrant patterns of DNA methylation can lead to plant developmental abnormalities. A specific DNA methylation state is an outcome of dynamic regulation by de novo methylation, maintenance of methylation and active demethylation, which are catalysed by various enzymes that are targeted by distinct regulatory pathways. In this Review, we discuss DNA methylation in plants, including methylating and demethylating enzymes and regulatory factors, and the coordination of methylation and demethylation activities by a so-called methylstat mechanism; the functions of DNA methylation in regulating transposon silencing, gene expression and chromosome interactions; the roles of DNA methylation in plant development; and the involvement of DNA methylation in plant responses to biotic and abiotic stress conditions.
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 ...
Backgroundm6A is a ubiquitous RNA modification in eukaryotes. Transcriptome-wide m6A patterns in Arabidopsis have been assayed recently. However, differential m6A patterns between organs have not been well characterized.ResultsOver two-third of the transcripts in Arabidopsis are modified by m6A. In contrast to a recent observation of m6A enrichment in 5′ mRNA, we find that m6A is distributed predominantly near stop codons. Interestingly, 85 % of the modified transcripts show high m6A methylation extent compared to their transcript level. The 290 highly methylated transcripts are mainly associated with transporters, stress responses, redox, regulation factors, and some non-coding RNAs. On average, the proportion of transcripts showing differential methylation between two plant organs is higher than that showing differential transcript levels. The transcripts with extensively higher m6A methylation in an organ are associated with the unique biological processes of this organ, suggesting that m6A may be another important contributor to organ differentiation in Arabidopsis. Highly expressed genes are relatively less methylated and vice versa, and different RNAs have distinct m6A patterns, which hint at mRNA fate. Intriguingly, most of the transposable element transcripts maintained a fragmented form with a relatively low transcript level and high m6A methylation in the cells.ConclusionsThis is the first study to comprehensively analyze m6A patterns in a variety of RNAs, the relationship between transcript level and m6A methylation extent, and differential m6A patterns across organs in Arabidopsis.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0839-2) contains supplementary material, which is available to authorized users.
SUMMARY DNA methylation is a conserved epigenetic mark that plays important roles in plant and vertebrate development, genome stability, and gene regulation. Canonical Methyl-CpG-Binding Domain (MBD) proteins are important interpreters of DNA methylation that recognize methylated CG sites and recruit chromatin remodelers, histone deacetylases and histone methyltransferases to repress transcription. Here, we show that Arabidopsis MBD7 and Increased DNA Methylation 3 (IDM3) are anti-silencing factors that prevent gene repression and DNA hypermethylation. MBD7 preferentially binds to highly methylated, CG-dense regions and physically associates with other anti-silencing factors, including the histone acetyltransferase IDM1 and the alpha-crystallin domain proteins IDM2 and IDM3. IDM1 and IDM2 were previously shown to facilitate active DNA demethylation by the 5-methylcytosine DNA glycosylase/lyase ROS1. Thus, MBD7 tethers the IDM proteins to methylated DNA, which enables the function of DNA demethylases that in turn limit DNA methylation and prevent transcriptional gene silencing.
DNA methylation is an important epigenetic mark involved in many biological processes. The genome of the climacteric tomato fruit undergoes a global loss of DNA methylation due to active DNA demethylation during the ripening process. It is unclear whether the ripening of other fruits is also associated with global DNA demethylation. We characterized the single-base resolution DNA methylomes of sweet orange fruits. Compared with immature orange fruits, ripe orange fruits gained DNA methylation at over 30,000 genomic regions and lost DNA methylation at about 1,000 genomic regions, suggesting a global increase in DNA methylation during orange fruit ripening. This increase in DNA methylation was correlated with decreased expression of DNA demethylase genes. The application of a DNA methylation inhibitor interfered with ripening, indicating that the DNA hypermethylation is critical for the proper ripening of orange fruits. We found that ripening-associated DNA hypermethylation was associated with the repression of several hundred genes, such as photosynthesis genes, and with the activation of hundreds of genes, including genes involved in abscisic acid responses. Our results suggest important roles of DNA methylation in orange fruit ripening.
The Arabidopsis ROS1/DEMETER family of 5mC DNA glycosylases are the first genetically characterized DNA demethylases in eukaryotes. However, the features of ROS1 targeted genomic loci are not well-understood. In this study, we characterized ROS1 target loci in Arabidopsis Col-0 and C24 ecotypes. We found that ROS1 preferentially targets transposable elements (TEs) and intergenic regions. Compared to most TEs, ROS1-targeted TEs are closer to protein coding genes, suggesting that ROS1 may prevent DNA methylation spreading from TEs to nearby genes. ROS1-targeted TEs are specifically enriched for H3K18Ac and H3K27me3, and depleted of H3K27me and H3K9me2. Importantly, we identified thousands of previously unknown RNA-directed DNA methylation (RdDM) targets upon depletion of ROS1, suggesting that ROS1 strongly antagonizes RdDM at these loci. In addition, we show that ROS1 also antagonizes RdDM-independent DNA methylation at some loci. Our results provide important insights into the genome-wide targets of ROS1 and the crosstalk between DNA methylation and ROS1-mediated active DNA demethylation.
BackgroundRecently, DNA methylation was proposed to regulate fleshy fruit ripening. Fleshy fruits can be distinguished by their ripening process as climacteric fruits, such as tomatoes, or non-climacteric fruits, such as strawberries. Tomatoes undergo a global decrease in DNA methylation during ripening, due to increased expression of a DNA demethylase gene. The dynamics and biological relevance of DNA methylation during the ripening of non-climacteric fruits are unknown.ResultsHere, we generate single-base resolution maps of the DNA methylome in immature and ripe strawberry. We observe an overall loss of DNA methylation during strawberry fruit ripening. Thus, ripening-induced DNA hypomethylation occurs not only in climacteric fruit, but also in non-climacteric fruit. Application of a DNA methylation inhibitor causes an early ripening phenotype, suggesting that DNA hypomethylation is important for strawberry fruit ripening. The mechanisms underlying DNA hypomethylation during the ripening of tomato and strawberry are distinct. Unlike in tomatoes, DNA demethylase genes are not upregulated during the ripening of strawberries. Instead, genes involved in RNA-directed DNA methylation are downregulated during strawberry ripening. Further, ripening-induced DNA hypomethylation is associated with decreased siRNA levels, consistent with reduced RdDM activity. Therefore, we propose that a downregulation of RdDM contributes to DNA hypomethylation during strawberry ripening.ConclusionsOur findings provide new insight into the DNA methylation dynamics during the ripening of non-climacteric fruit and suggest a novel function of RdDM in regulating an important process in plant development.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1587-x) contains supplementary material, which is available to authorized users.
Throughout their lives, plants sense many developmental and environmental stimuli, and activation of optimal responses against these stimuli requires extensive transcriptional reprogramming. To facilitate this activation, plant mRNA contains untranslated regions (UTRs) that significantly increase the coding capacity of the genome by producing multiple mRNA variants from the same gene. In this review we compare UTRs of arabidopsis (Arabidopsis thaliana) and rice (Oryza sativum) at the genome scale to highlight their complexity in crop plants. We discuss different modes of UTR-based regulation with emphasis on genes that regulate multiple plant processes, including flowering, stress responses, and nutrient homeostasis. We demonstrate functional specificity in genes with variable UTR length and propose future research directions.
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