Gene body DNA methylation in plants.
TL;DR: The recent findings on the evolutionary origin and molecular mechanism of gbM are highlighted and studies describing the possible roles for this enigmatic epigenetic phenotype are synthesized.
About: This article is published in Current Opinion in Plant Biology.The article was published on 2017-04-01 and is currently open access. It has received 294 citations till now. The article focuses on the topics: RNA-Directed DNA Methylation & DNA methylation.
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Norwich Research Park1, Bayer2, University of Toronto3, Agriculture and Agri-Food Canada4, University of Saskatchewan5, Paris Diderot University6, Institut national de la recherche agronomique7, National Research Council8, Technische Universität München9, University of Melbourne10, University of Maryland, College Park11
TL;DR: This study leverages 850 wheat RNA-sequencing samples, alongside the annotated genome, to determine the similarities and differences between homoeolog expression across a range of tissues, developmental stages, and cultivars and suggests that the transposable elements in promoters relate more closely to the variation in the relative expression of homoeologicals across tissues than to a ubiquitous effect across all tissues.
Abstract: The coordinated expression of highly related homoeologous genes in polyploid species underlies the phenotypes of many of the world's major crops. Here we combine extensive gene expression datasets to produce a comprehensive, genome-wide analysis of homoeolog expression patterns in hexaploid bread wheat. Bias in homoeolog expression varies between tissues, with ~30% of wheat homoeologs showing nonbalanced expression. We found expression asymmetries along wheat chromosomes, with homoeologs showing the largest inter-tissue, inter-cultivar, and coding sequence variation, most often located in high-recombination distal ends of chromosomes. These transcriptionally dynamic genes potentially represent the first steps toward neo- or subfunctionalization of wheat homoeologs. Coexpression networks reveal extensive coordination of homoeologs throughout development and, alongside a detailed expression atlas, provide a framework to target candidate genes underpinning agronomic traits in wheat.
609 citations
TL;DR: The extent of variation in DNA methylation in angiosperms is revealed and patterns are shown to be broadly a reflection of the evolutionary and life histories of plant species.
Abstract: DNA methylation is an important feature of plant epigenomes, involved in the formation of heterochromatin and affecting gene expression. Extensive variation of DNA methylation patterns within a species has been uncovered from studies of natural variation. However, the extent to which DNA methylation varies between flowering plant species is still unclear. To understand the variation in genomic patterning of DNA methylation across flowering plant species, we compared single base resolution DNA methylomes of 34 diverse angiosperm species. By analyzing whole-genome bisulfite sequencing data in a phylogenetic context, it becomes clear that there is extensive variation throughout angiosperms in gene body DNA methylation, euchromatic silencing of transposons and repeats, as well as silencing of heterochromatic transposons. The Brassicaceae have reduced CHG methylation levels and also reduced or loss of CG gene body methylation. The Poaceae are characterized by a lack or reduction of heterochromatic CHH methylation and enrichment of CHH methylation in genic regions. Furthermore, low levels of CHH methylation are observed in a number of species, especially in clonally propagated species. These results reveal the extent of variation in DNA methylation in angiosperms and show that DNA methylation patterns are broadly a reflection of the evolutionary and life histories of plant species.
403 citations
Cites background from "Gene body DNA methylation in plants..."
...Species in gold belong to the Brassicaceae and illustrate the decreased levels and loss of mCG. d gbM genes are more highly expressed, whereas mCG over the TSS (mCG-TSS) has reduced gene expression known to occur, especially in intronic sequences due in part to the presence of transposons [80]....
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...1b), which is a natural cmt3 mutant, whereas CMT3 is under relaxed selection in other Brassicaceae [61, 62]....
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...Seymour DK, Koenig D, Hagmann J, Becker C, Weigel D. Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization....
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...In contrast, mCHG genes were relatively rare in the Brassicaceae where mCHH genes were the predominant type of non-CG genes....
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...Here, too, the decay and loss of gbM in the Brassicaceae is observed as B. rapa and B. oleracea have the second and third lowest DNA methylation levels, respectively, in gbM genes; and E. salsugineum shows no canonical gbM having only a few genes that passed statistical tests for having enrichment of mCG in gene bodies....
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TL;DR: In this article, de novo genome assemblies, transcriptomes, annotations, and methylomes for the 26 inbreds that serve as the founders for the maize nested association mapping population were reported.
Abstract: We report de novo genome assemblies, transcriptomes, annotations, and methylomes for the 26 inbreds that serve as the founders for the maize nested association mapping population. The number of pan-genes in these diverse genomes exceeds 103,000, with approximately a third found across all genotypes. The results demonstrate that the ancient tetraploid character of maize continues to degrade by fractionation to the present day. Excellent contiguity over repeat arrays and complete annotation of centromeres revealed additional variation in major cytological landmarks. We show that combining structural variation with single-nucleotide polymorphisms can improve the power of quantitative mapping studies. We also document variation at the level of DNA methylation and demonstrate that unmethylated regions are enriched for cis-regulatory elements that contribute to phenotypic variation.
183 citations
TL;DR: It will be important to understand the sources of epigenetic variation and the stability of newly formed epigenetic variants over generations to fully use the potential of epigenetics to improve crops.
Abstract: Plant breeding has traditionally relied on combining the genetic diversity present within a species to develop combinations of alleles that provide desired traits. Epigenetic diversity may provide additional sources of variation within a species that could be captured or created for crop improvement. It will be important to understand the sources of epigenetic variation and the stability of newly formed epigenetic variants over generations to fully use the potential of epigenetic variation to improve crops. The development and application of methods for widespread epigenome profiling and engineering may generate new avenues for using the full potential of epigenetics in crop improvement.
173 citations
TL;DR: Methylation in the bodies of active genes is common in animals and vascular plants and evolutionary patterns indicate homeostatic functions for this type of methylation.
Abstract: Methylation in the bodies of active genes is common in animals and vascular plants. Evolutionary patterns indicate homeostatic functions for this type of methylation.
132 citations
Cites background from "Gene body DNA methylation in plants..."
...In addition to transposons, DNA methylation frequently occurs in active plant genes [2, 3, 5]....
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...expressed genes and away from the 5′ and 3′ gene ends [2, 3, 5, 6]....
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...Several homeostatic GbM functions have been proposed [2, 5]....
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...Some or all of the proposed hypotheses may turn out to be wrong, but it is premature to conclude that any of them have been disproven [5] until they are tested with techniques that measure transcription rather than mRNA levels and are able to analyze small numbers of cells....
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..., housekeeping) genes, and least frequent in the genes with the most variable expression [2, 5]....
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References
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TL;DR: Drawing on insights from both plants and animals should deepen the understanding of the regulation and biological significance of DNA methylation.
Abstract: Cytosine DNA methylation is a stable epigenetic mark that is crucial for diverse biological processes, including gene and transposon silencing, imprinting and X chromosome inactivation. Recent findings in plants and animals have greatly increased our understanding of the pathways used to accurately target, maintain and modify patterns of DNA methylation and have revealed unanticipated mechanistic similarities between these organisms. Key roles have emerged for small RNAs, proteins with domains that bind methylated DNA and DNA glycosylases in these processes. Drawing on insights from both plants and animals should deepen our understanding of the regulation and biological significance of DNA methylation.
3,180 citations
TL;DR: An in-depth investigation of the human SHANK3 locus and its mouse homologue demonstrated that this tissue-specific DNA methylation regulates intragenic promoter activity in vitro and in vivo.
Abstract: Although it is known that the methylation of DNA in 5' promoters suppresses gene expression, the role of DNA methylation in gene bodies is unclear. In mammals, tissue- and cell type-specific methylation is present in a small percentage of 5' CpG island (CGI) promoters, whereas a far greater proportion occurs across gene bodies, coinciding with highly conserved sequences. Tissue-specific intragenic methylation might reduce, or, paradoxically, enhance transcription elongation efficiency. Capped analysis of gene expression (CAGE) experiments also indicate that transcription commonly initiates within and between genes. To investigate the role of intragenic methylation, we generated a map of DNA methylation from the human brain encompassing 24.7 million of the 28 million CpG sites. From the dense, high-resolution coverage of CpG islands, the majority of methylated CpG islands were shown to be in intragenic and intergenic regions, whereas less than 3% of CpG islands in 5' promoters were methylated. The CpG islands in all three locations overlapped with RNA markers of transcription initiation, and unmethylated CpG islands also overlapped significantly with trimethylation of H3K4, a histone modification enriched at promoters. The general and CpG-island-specific patterns of methylation are conserved in mouse tissues. An in-depth investigation of the human SHANK3 locus and its mouse homologue demonstrated that this tissue-specific DNA methylation regulates intragenic promoter activity in vitro and in vivo. These methylation-regulated, alternative transcripts are expressed in a tissue- and cell type-specific manner, and are expressed differentially within a single cell type from distinct brain regions. These results support a major role for intragenic methylation in regulating cell context-specific alternative promoters in gene bodies.
1,610 citations
TL;DR: The data suggest that land plants and vertebrates are under strong selective pressure to repress TEs, because of their sexual mode of reproduction, and indicate that gene body methylation is an ancient property of eukaryotic genomes.
Abstract: Eukaryotic cytosine methylation represses transcription but also occurs in the bodies of active genes, and the extent of methylation biology conservation is unclear. We quantified DNA methylation in 17 eukaryotic genomes and found that gene body methylation is conserved between plants and animals, whereas selective methylation of transposons is not. We show that methylation of plant transposons in the CHG context extends to green algae and that exclusion of histone H2A.Z from methylated DNA is conserved between plants and animals, and we present evidence for RNA-directed DNA methylation of fungal genes. Our data demonstrate that extant DNA methylation systems are mosaics of conserved and derived features, and indicate that gene body methylation is an ancient property of eukaryotic genomes.
1,529 citations
TL;DR: DNA methylation is mapped in the entire Arabidopsis thaliana genome at high resolution, indicating that genic transcription and DNA methylation are closely interwoven processes.
Abstract: Cytosine methylation, a common form of DNA modification that antagonizes transcription, is found at transposons and repeats in vertebrates, plants and fungi. Here we have mapped DNA methylation in the entire Arabidopsis thaliana genome at high resolution. DNA methylation covers transposons and is present within a large fraction of A. thaliana genes. Methylation within genes is conspicuously biased away from gene ends, suggesting a dependence on RNA polymerase transit. Genic methylation is strongly influenced by transcription: moderately transcribed genes are most likely to be methylated, whereas genes at either extreme are least likely. In turn, transcription is influenced by methylation: short methylated genes are poorly expressed, and loss of methylation in the body of a gene leads to enhanced transcription. Our results indicate that genic transcription and DNA methylation are closely interwoven processes.
1,321 citations
TL;DR: The isolation of KRYPTONITE, a methyltransferase gene specific to H3 Lys 9, identified in a mutant screen for suppressors of gene silencing at the Arabidopsis thaliana SUPERMAN (SUP) locus is reported, which suggests that CpNpG DNA methylation is controlled by histone H 3 Lys 9 methylation, through interaction of CMT3 with methylated chromatin.
Abstract: Gene silencing in eukaryotes is associated with the formation of heterochromatin, a complex of proteins and DNA that block transcription. Heterochromatin is characterized by the methylation of cytosine nucleotides of the DNA, the methylation of histone H3 at lysine 9 (H3 Lys 9), and the specific binding of heterochromatin protein 1 (HP1) to methylated H3 Lys 9 (refs 1-7). Although the relationship between these chromatin modifications is generally unknown, in the fungus Neurospora crassa, DNA methylation acts genetically downstream of H3 Lys 9 methylation. Here we report the isolation of KRYPTONITE, a methyltransferase gene specific to H3 Lys 9, identified in a mutant screen for suppressors of gene silencing at the Arabidopsis thaliana SUPERMAN (SUP) locus. Loss-of-function kryptonite alleles resemble mutants in the DNA methyltransferase gene CHROMOMETHYLASE3 (CMT3), showing loss of cytosine methylation at sites of CpNpG trinucleotides (where N is A, C, G or T) and reactivation of endogenous retrotransposon sequences. We show that CMT3 interacts with an Arabidopsis homologue of HP1, which in turn interacts with methylated histones. These data suggest that CpNpG DNA methylation is controlled by histone H3 Lys 9 methylation, through interaction of CMT3 with methylated chromatin.
1,205 citations