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      The Progeny of Arabidopsis thaliana Plants Exposed to Salt Exhibit Changes in DNA Methylation, Histone Modifications and Gene Expression

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          Abstract

          Plants are able to acclimate to new growth conditions on a relatively short time-scale. Recently, we showed that the progeny of plants exposed to various abiotic stresses exhibited changes in genome stability, methylation patterns and stress tolerance. Here, we performed a more detailed analysis of methylation patterns in the progeny of Arabidopsis thaliana (Arabidopsis) plants exposed to 25 and 75 mM sodium chloride. We found that the majority of gene promoters exhibiting changes in methylation were hypermethylated, and this group was overrepresented by regulators of the chromatin structure. The analysis of DNA methylation at gene bodies showed that hypermethylation in the progeny of stressed plants was primarily due to changes in the 5′ and 3′ ends as well as in exons rather than introns. All but one hypermethylated gene tested had lower gene expression. The analysis of histone modifications in the promoters and coding sequences showed that hypermethylation and lower gene expression correlated with the enrichment of H3K9me2 and depletion of H3K9ac histones. Thus, our work demonstrated a high degree of correlation between changes in DNA methylation, histone modifications and gene expression in the progeny of salt-stressed plants.

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          Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.

          Cytosine DNA methylation is important in regulating gene expression and in silencing transposons and other repetitive sequences. Recent genomic studies in Arabidopsis thaliana have revealed that many endogenous genes are methylated either within their promoters or within their transcribed regions, and that gene methylation is highly correlated with transcription levels. However, plants have different types of methylation controlled by different genetic pathways, and detailed information on the methylation status of each cytosine in any given genome is lacking. To this end, we generated a map at single-base-pair resolution of methylated cytosines for Arabidopsis, by combining bisulphite treatment of genomic DNA with ultra-high-throughput sequencing using the Illumina 1G Genome Analyser and Solexa sequencing technology. This approach, termed BS-Seq, unlike previous microarray-based methods, allows one to sensitively measure cytosine methylation on a genome-wide scale within specific sequence contexts. Here we describe methylation on previously inaccessible components of the genome and analyse the DNA methylation sequence composition and distribution. We also describe the effect of various DNA methylation mutants on genome-wide methylation patterns, and demonstrate that our newly developed library construction and computational methods can be applied to large genomes such as that of mouse.
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            Epigenetic regulation of stress responses in plants.

            Gene expression driven by developmental and stress cues often depends on nucleosome histone post-translational modifications and sometimes on DNA methylation. A number of studies have shown that these DNA and histone modifications play a key role in gene expression and plant development under stress. Most of these stress-induced modifications are reset to the basal level once the stress is relieved, while some of the modifications may be stable, that is, may be carried forward as 'stress memory' and may be inherited across mitotic or even meiotic cell divisions. Epigenetic stress memory may help plants more effectively cope with subsequent stresses. Comparative studies on stress-responsive epigenomes and transcriptomes will enhance our understanding of stress adaptation of plants.
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              Stress-induced DNA methylation changes and their heritability in asexual dandelions.

              *DNA methylation can cause heritable phenotypic modifications in the absence of changes in DNA sequence. Environmental stresses can trigger methylation changes and this may have evolutionary consequences, even in the absence of sequence variation. However, it remains largely unknown to what extent environmentally induced methylation changes are transmitted to offspring, and whether observed methylation variation is truly independent or a downstream consequence of genetic variation between individuals. *Genetically identical apomictic dandelion (Taraxacum officinale) plants were exposed to different ecological stresses, and apomictic offspring were raised in a common unstressed environment. We used methylation-sensitive amplified fragment length polymorphism markers to screen genome-wide methylation alterations triggered by stress treatments and to assess the heritability of induced changes. *Various stresses, most notably chemical induction of herbivore and pathogen defenses, triggered considerable methylation variation throughout the genome. Many modifications were faithfully transmitted to offspring. Stresses caused some epigenetic divergence between treatment and controls, but also increased epigenetic variation among plants within treatments. *These results show the following. First, stress-induced methylation changes are common and are mostly heritable. Second, sequence-independent, autonomous methylation variation is readily generated. This highlights the potential of epigenetic inheritance to play an independent role in evolutionary processes, which is superimposed on the system of genetic inheritance.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                23 January 2012
                : 7
                : 1
                : e30515
                Affiliations
                [1 ]Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, Canada
                [2 ]Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, Ghent University, Ghent, Belgium
                [3 ]Department of Molecular Genetics, Ghent University, Ghent, Belgium
                Temasek Life Sciences Laboratory, Singapore
                Author notes

                Conceived and designed the experiments: AB IK. Performed the experiments: AB YI JH. Analyzed the data: AB YI JH IK. Wrote the paper: AB IK.

                Article
                PONE-D-11-12134
                10.1371/journal.pone.0030515
                3264603
                22291972
                f64b2ce0-5590-47ee-89ef-da8b5e15a440
                Bilichak et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 29 June 2011
                : 16 December 2011
                Page count
                Pages: 15
                Categories
                Research Article
                Biology
                Biochemistry
                Nucleic Acids
                DNA
                Biophysics
                Nucleic Acids
                DNA
                Genetics
                Epigenetics
                Gene Expression
                Model Organisms
                Plant and Algal Models
                Molecular Cell Biology
                Gene Expression
                Nucleic Acids
                DNA
                Plant Science
                Physics
                Biophysics
                Nucleic Acids
                DNA

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                Uncategorized

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