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Piecing together cis ‐regulatory networks: insights from epigenomics studies in plants

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5‐Methylcytosine, a chemical modification of DNA, is a covalent modification found in the genomes of both plants and animals. Epigenetic inheritance of phenotypes mediated by DNA methylation is well established in plants. Most of the known mechanisms of establishing, maintaining and modifying DNA methylation have been worked out in the reference plant Arabidopsis thaliana. Major functions of DNA methylation in plants include regulation of gene expression and silencing of transposable elements (TEs) and repetitive sequences, both of which have parallels in mammalian biology, involve interaction with the transcriptional machinery, and may have profound effects on the regulatory networks in the cell. Methylome and transcriptome dynamics have been investigated in development and environmental responses in Arabidopsis and agriculturally and ecologically important plants, revealing the interdependent relationship among genomic context, methylation patterns, and expression of TE and protein coding genes. Analyses of methylome variation among plant natural populations and species have begun to quantify the extent of genetic control of methylome variation vs. true epimutation, and model the evolutionary forces driving methylome evolution in both short and long time scales. The ability of DNA methylation to positively or negatively modulate binding affinity of transcription factors (TFs) provides a natural link from genome sequence and methylation changes to transcription. Technologies that allow systematic determination of methylation sensitivities of TFs, in native genomic and methylation context without confounding factors such as histone modifications, will provide baseline datasets for building cell‐type‐ and individual‐specific regulatory networks that underlie the establishment and inheritance of complex traits.

This article is categorized under:

  • Laboratory Methods and Technologies > Genetic/Genomic Methods
  • Biological Mechanisms > Regulatory Biology
Typical patterns o DNA methylation in plant genomes, showing examples from Arabidopsis. In the TAIR10 gene model tracks, solid green and solid red rectangles represent exons and UTRs, respectively, and gray arrows represent transposable elements (TEs). In the 5mC tracks, each tick mark corresponds to one methylated cytosine. The color of the tick marks represents cytosine methylation context and the height of the tick marks represents level of methylation. (a) Methylation in gene bodies is typically in a CG context while methylation found in TEs are in all three contexts. (b) The gene on the left (At1g10180) show typical gene body methylation in a CG context. The gene on the right (At1g10190) is an example of a poly‐epiallelic gene, displaying TE‐like methylation in accessions Col‐0 and Ömo1‐7 but gene body methylation in accession Ädal 3.
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Examples of applying DAP‐seq to investigate cis‐effects (blue boxes) and trans‐effects (green boxes) regulating TF binding to the genome.
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Three major groups of TF binding sensitivity to DNA methylation. Examples of TF binding to methylated regions analyzed by DAP‐seq, which retains native DNA methylation, or by ampDAP‐seq, where PCR amplification replaces 5mC in the DAP‐seq input DNA by unmethylated cytosine. In the 5mC track, the color of the tick marks represents methylation context and the tick height represents the level of methylation. In the DAP‐seq and ampDAP‐seq tracks, green and red colors represent pileups of reads mapping to either the Watson or Crick DNA strands, respectively. (a) TF binding is inhibited by 5mC in the binding motif. Arabidopsis TF ABSCISIC ACID INSENSITIVE 5 (ABI5; AT2G36270) belongs to this group. (b) TF binding is unaffected by 5mC in the binding motif. Arabidopsis TF LHY/CCA1‐LIKE 1 (LCL1; AT5G02840) belongs to this group. (c) TF binding is enhanced by 5mC in the binding motif. Arabidopsis TF DP‐E2F‐LIKE 2 (DEL2; AT5G14960) belongs to this group.
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Mechanisms for genome sequence and methylation variation to create different regulatory connections between plant accessions (populations), both in cis (blue rectangles) and in trans (green rectangle).
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Model of cis‐ and trans‐action of DNA methylation in relation to genome context and gene expression. The different colored rectangles represent different genes, while rectangles in solid gray represent transposable elements (TE) and circles represent transcription factor (TF) proteins.
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