Dataset Information

TET-mediated epimutagenesis of the Arabidopsis thaliana methylome.

ABSTRACT: DNA methylation in the promoters of plant genes sometimes leads to transcriptional repression, and the loss of DNA methylation in methyltransferase mutants results in altered gene expression and severe developmental defects. However, many cases of naturally occurring DNA methylation variations have been reported, whereby altered expression of differentially methylated genes is responsible for agronomically important traits. The ability to manipulate plant methylomes to generate epigenetically distinct individuals could be invaluable for breeding and research purposes. Here, we describe "epimutagenesis," a method to rapidly generate DNA methylation variation through random demethylation of the Arabidopsis thaliana genome. This method involves the expression of a human ten-eleven translocation (TET) enzyme, and results in widespread hypomethylation that can be inherited to subsequent generations, mimicking mutants in the maintenance of DNA methyltransferase met1. Application of epimutagenesis to agriculturally significant plants may result in differential expression of alleles normally silenced by DNA methylation, uncovering previously hidden phenotypic variations.

SUBMITTER: Ji L

PROVIDER: S-EPMC5832761 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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TET-mediated epimutagenesis of the Arabidopsis thaliana methylome.

Ji Lexiang L Jordan William T WT Shi Xiuling X Hu Lulu L He Chuan C Schmitz Robert J RJ

Nature communications 20180301 1

DNA methylation in the promoters of plant genes sometimes leads to transcriptional repression, and the loss of DNA methylation in methyltransferase mutants results in altered gene expression and severe developmental defects. However, many cases of naturally occurring DNA methylation variations have been reported, whereby altered expression of differentially methylated genes is responsible for agronomically important traits. The ability to manipulate plant methylomes to generate epigenetically di ...[more]

PMID: 29497035

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Project description:Salt stress threatens plant growth, development and crop yields, and has become a critical global environmental issue. Increasing evidence has suggested that the epigenetic mechanism such as DNA methylation can mediate plant response to salt stress through transcriptional regulation and transposable element (TE) silencing. However, studies exploring genome-wide methylation dynamics under salt stress remain limited, in particular, for studies on multiple genotypes. Here, we adopted four natural accessions of the model species Arabidopsis thaliana and investigated the phenotypic and genome-wide methylation responses to salt stress through whole-genome bisulfite sequencing (WGBS). We found that salt stress significantly changed plant phenotypes, including plant height, rosette diameter, fruit number, and aboveground biomass, and the change in biomass tended to depend on accessions. Methylation analysis revealed that genome-wide methylation patterns depended primarily on accessions, and salt stress caused significant methylation changes in ∼ 0.1% cytosines over the genomes. About 33.5% of these salt-induced differential methylated cytosines (DMCs) were located to transposable elements (TEs). These salt-induced DMCs were mainly hypermethylated and accession-specific. TEs annotated to have DMCs (DMC-TEs) across accessions were found mostly belonged to the superfamily of Gypsy, a type II transposon, indicating a convergent DMC dynamic on TEs across different genetic backgrounds. Moreover, 8.0% of salt-induced DMCs were located in gene bodies and their proximal regulatory regions. These DMCs were also accession-specific, and genes annotated to have DMCs (DMC-genes) appeared to be more accession-specific than DMC-TEs. Intriguingly, both accession-specific DMC-genes and DMC-genes shared by multiple accessions were enriched in similar functions, including methylation, gene silencing, chemical homeostasis, polysaccharide catabolic process, and pathways relating to shifts between vegetative growth and reproduction. These results indicate that, across different genetic backgrounds, methylation changes may have convergent functions in post-transcriptional, physiological, and phenotypic modulation under salt stress. These convergent methylation dynamics across accession may be autonomous from genetic variation or due to convergent genetic changes, which requires further exploration. Our study provides a more comprehensive picture of genome-wide methylation dynamics under salt stress, and highlights the importance of exploring stress response mechanisms from diverse genetic backgrounds.

Project description:The nucleosome positioning regulates the gene expression and many other DNA-related processes in eukaryotes. Genome-wide mapping of nucleosome positions and correlation of genome-wide nucleosomal remodeling with the changes in the gene expression can help us understanding gene regulation on genome level.In the present study, we correlate the gene expression and the genomic nucleosomal remodeling in response to salicylic acid (SA) treatment in A. thaliana. We have mapped genome-wide nucleosomes by performing tiling microarray using 146 bp mononucleosomal template DNA. The average nucleosomal coverage is approximately 346 bp per nucleosome both under the control and the SA-treated conditions. The nucleosomal coverage is more in the coding region than in the 5' regulatory regions. We observe approximately 50% nucleosomal remodeling on SA treatment where significant nucleosomal depletion and nucleosomal enrichment around the transcription start site (TSS) occur in SA induced genes and SA repressed genes respectively in response to SA treatment. Especially in the case of the SA-induced group, the nucleosomal remodeling over the minimal promoter in response to SA is especially significant in the Non-expresser of PR1 (NPR1)-dependent genes. A detailed investigation of npr1-1 mutant confirms a distinct role of NPR1 in the nucleosome remodeling over the core promoter. We have also identified several motifs for various hormonal responses; including ABRE elements in the remodeled nucleosomal regions around the promoter region in the SA regulated genes. We have further identified that the W-box and TGACG/C motif, reported to play an important role in SA-mediated induction, are enriched in nucleosome free regions (NFRs) of the promoter region of the SA induced genes.This is the first study reporting genome-wide effects of SA treatment on the chromatin architecture of A. thaliana. It also reports significant role of NPR1 in genome-wide nucleosomal remodeling in response to SA.

Dataset Information

TET-mediated epimutagenesis of the Arabidopsis thaliana methylome.

Publications

TET-mediated epimutagenesis of the Arabidopsis thaliana methylome.

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