Widespread natural variation of DNA methylation within angiosperms

Niederhuth, Chad E.; Bewick, Adam J.; Ji, Lexiang; Alabady, Magdy S.; Kim, Kyung Do; Page, Justin T.; Li, Qing; Rohr, Nicholas A.; Rambani, Aditi; Burke, John M.; Udall, Josh A.; Egesi, Chiedozie; Schmutz, Jeremy; Grimwood, Jane; Jackson, Scott A.; Springer, Nathan M.; Schmitz, Robert J.

doi:10.1101/045880

Cited by 111 publications

(258 citation statements)

References 134 publications

(218 reference statements)

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“…Previous studies have shown that gbM genes tend to be expressed at moderate to high levels in A. thaliana (4,5,9). Similar results were found in all other plant species that contained gbM (19). These results indicated that the CMT3/KYP pathway might preferentially target moderately to highly transcribed genes.…”

supporting

confidence: 76%

“…The methylomes of the vast majority of the plant species are similar to A. thaliana, with high levels of mCG/mCHG/mCHH colocalized to repetitive sequences and gbM in moderately expressed genes (19). The only exception was Eutrema salsugineum (accession Shandong), a member of the Brassicaceae family that shares a common ancestor with A. thaliana and Brassica spp.…”

mentioning

confidence: 97%

“…It is possible that H3K9me2-containing H3 may be occasionally misincorporated into active genes during transcription-coupled nucleosome turnover. Alternatively, nucleosome movement during transcription may lead to the spreading of mCHG/H3K9me2 in flanking regions into active genes, as was described at the A. thaliana BONSAI gene (19).…”

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confidence: 99%

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On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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266

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In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, to our knowledge the first instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum. Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM, supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z, and various histone modifications in E. salsugineum and in Arabidopsis thaliana epigenetic recombinant inbred lines found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modification of chromatin over evolutionary timescales.DNA methylation | gene body methylation | epigenetics | histone modifications | CHROMOMETHYLASE 3 I n angiosperms, cytosine DNA methylation occurs in three sequence contexts: Methylated CG (mCG) is catalyzed by METHYLTRANSFERASE 1 (MET1), mCHG (where H is A/C/T) by CHROMOMETHYLASE 3 (CMT3), and mCHH by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) or CHROMOMETHYLASE 2 (CMT2) (1). MET1 performs a maintenance function and is targeted by VARIANT IN METHYLATION 1 (VIM1), which binds preexisting hemimethylated CG sites. In contrast, DRM2 is targeted by RNA-directed DNA methylation (RdDM) for the de novo establishment of mCHH. CMT3 forms a self-reinforcing loop with the H3K9me2 pathway to maintain mCHG; however, considering that transformation of CMT3 into the cmt3 background can rescue DNA methylation defects, it is reasonable to also consider CMT3 a de novo methyltransferase (2). Two main lines of evidence suggest that DNA methylation plays an important role in the transcriptional silencing of transposable elements (TEs): that TEs are usually methylated, and that the loss of DNA methylation (e.g., in methyltransferase mutants) is often accompanied by TE reactivation.A large number of plant genes (e.g., ∼13.5% of all Arabidopsis thaliana genes) also contain exclusively mCG in the transcribed region and a depletion of mCG from both the transcriptional start and stop sites (referred to as "gene body DNA methylation"; gbM) ( Fig. 1A) (3)(4)(5). A survey of plant methylome data showed that the emergence of gbM in the plant kingdom is specific to angiosperms (6), whereas nonflowering plants (such as mosses and green algae) have much more diverse genic methylation patterns (7,8). Similar to mCG at TEs, the maintenance of gbM requires MET1. In contrast to DNA methylation at TEs, however, gbM does not appear to be associated with transcriptional repression. Rather, genes containing gbM are ubiquitously expressed at moderate to high levels compared with non-gbM genes (4, 5, 9), and within gbM genes there is a correlation between transcript abundance and methylation levels (10, 11).It has been proposed ...

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supporting

confidence: 76%

mentioning

confidence: 97%

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On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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412

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“…Methylome studies for crops like rice, maize and soybean, which have larger genomes with expanded TE families, have higher mCG and mCHG levels but similar mCHH levels compared to Arabidopsis (Niederhuth et al, 2016; Seymour et al, 2014; Takuno et al, 2016). Since TE transposition greatly impacts epigenomic diversity among A. thaliana accessions, crops are likely to show much more local epigenomic diversity within a species.…”

Section: Resultsmentioning

confidence: 99%

Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions

Kawakatsu

Huang

Jupe

et al. 2016

Cell

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SUMMARY The epigenome orchestrates genome accessibility, functionality and three-dimensional structure. Because epigenetic variation can impact transcription and thus phenotypes, it may contribute to adaptation. Here we report 1,107 high-quality single-base resolution methylomes and 1,203 transcriptomes from the 1001 Genomes collection of Arabidopsis thaliana. Although the genetic basis of methylation variation is highly complex, geographic origin is a major predictor of genome-wide DNA methylation levels and of altered gene expression caused by epialleles. Comparison to cistrome and epicistrome datasets identifies associations between transcription factor binding sites, methylation, nucleotide variation and co-expression modules. Physical maps for nine of the most diverse genomes reveals how transposons and other structural variants shape the epigenome, with dramatic effects on immunity genes. The 1001 Epigenomes Project provides a comprehensive resource for understanding how variation in DNA methylation contributes to molecular and non-molecular phenotypes in natural populations of the most studied model plant.

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“…Within A. thaliana , methylation levels in all three contexts varied among accessions, differing as much as ~2× for mCG, ~6× for mCHG, and ~11× for mCHH [72]. Methylation levels differ by even greater degrees between plant species, with mCG varying ~3×, mCHG ~9×, and mCHH ~16× [74, 75, 77, 78]. Underlying these genome-wide variations are dissimilarities in both the percentage of sites methylated and how highly those sites are methylated [75, 76].…”

Section: Genome-wide Patterns Of Methylation In Flowering Plant Genomesmentioning

confidence: 99%

Putting DNA methylation in context: from genomes to gene expression in plants

Niederhuth

Schmitz

2017

Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanism

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130

110

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Plant DNA methylation is its own language, interpreted by the cell to maintain silencing of transposons, facilitate chromatin structure, and to ensure proper expression of some genes. Just as in any language, context is important. Rather than being a simple “on-off switch”, DNA methylation has a range of “meanings” dependent upon the underlying sequence and its location in the genome. Differences in the sequence context of individual sites are established, maintained, and interpreted by differing molecular pathways. Varying patterns of methylation within genes and surrounding sequences are associated with a continuous range of expression differences, from silencing to constitutive expression. These often-subtle differences have been pieced together from years of effort, but have taken off with the advent of methods for assessing methylation across entire genomes. Recognizing these patterns and identifying underlying causes is essential for understanding the function of DNA methylation and its systems-wide contribution to a range of processes in plant genomes.

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Widespread natural variation of DNA methylation within angiosperms

Cited by 111 publications

References 134 publications

On the origin and evolutionary consequences of gene body DNA methylation

On the origin and evolutionary consequences of gene body DNA methylation

Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions

Putting DNA methylation in context: from genomes to gene expression in plants

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