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Spontaneous epigenetic variation in the Arabidopsis thaliana methylome.
Nature. 2011 Dec 8; 480(7376):245-9
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15 Nov 2011
Confirmation, New Finding
DOI: 10.3410/f.13361059.14731207
This study establishes rates of appearance and stability of DNA methylation epialleles in multiple Arabidopsis thaliana strains derived by single seed descent {1} for about 30 generations of selfing under greenhouse conditions. The study, therefore, provides insights into the dynamics of heritable epialleles...Continue reading
This study establishes rates of appearance and stability of DNA methylation epialleles in multiple Arabidopsis thaliana strains derived by single seed descent {1} for about 30 generations of selfing under greenhouse conditions. The study, therefore, provides insights into the dynamics of heritable epialleles that have the potential to underlie phenotypic variation.
As ascertained by deep sequencing, single cytosine epimutations occurred at a rate about 1000-fold higher than expected for DNA mutations. Nonetheless, the frequency of changes in larger regions (concerted changes across adjacent sites) was much lower, with a rate similar to that of DNA mutations as measured for a subset of the strains in an earlier study (pls see {2}, on which I am a co-author). There was no evidence that de novo DNA mutations were associated in cis with heritable changes in cytosine methylation. Across the genome, transgenerational variation in cytosine methylation was lowest for transposable elements that are known to be effectively methylated (and silenced) by short interfering RNAs (siRNAs). In a small number of cases, differences in gene expression were correlated with epialleles, consistent with a causal role for epialleles in phenotypic variation. However, the appearance of such alleles was restricted to a subset of genomic locations, and reversion rates were high. The extent to which these factors limit the evolutionary impact of epialleles requires further study.
The design of this study is similar to that of Schmitz et al. {3}, who used similar methods and biological material to reach some of the same conclusions.
As ascertained by deep sequencing, single cytosine epimutations occurred at a rate about 1000-fold higher than expected for DNA mutations. Nonetheless, the frequency of changes in larger regions (concerted changes across adjacent sites) was much lower, with a rate similar to that of DNA mutations as measured for a subset of the strains in an earlier study (pls see {2}, on which I am a co-author). There was no evidence that de novo DNA mutations were associated in cis with heritable changes in cytosine methylation. Across the genome, transgenerational variation in cytosine methylation was lowest for transposable elements that are known to be effectively methylated (and silenced) by short interfering RNAs (siRNAs). In a small number of cases, differences in gene expression were correlated with epialleles, consistent with a causal role for epialleles in phenotypic variation. However, the appearance of such alleles was restricted to a subset of genomic locations, and reversion rates were high. The extent to which these factors limit the evolutionary impact of epialleles requires further study.
The design of this study is similar to that of Schmitz et al. {3}, who used similar methods and biological material to reach some of the same conclusions.
References
1.
Spontaneous mutational effects on reproductive traits of arabidopsis thaliana.
Genetics 2000 May; 1(155):369-78
PMID: 10790410
2.
The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana.
Science 2010 Jan 1; 5961(327):92-4
PMID: 20044577
3.
Transgenerational epigenetic instability is a source of novel methylation variants.
Science 2011 Oct 21; 6054(334):369-73
PMID: 21921155
Disclosures
Richard Clark notes that he has been a recent collaborator, on unrelated studies, with two of the authors (D. Weigel and O. Stegel).
Add Comment
Clark R: F1000Prime Recommendation of [Becker C et al., Nature 2011, 480(7376):245-9]. In F1000Prime, 15 Nov 2011; DOI: 10.3410/f.13361059.14731207. F1000Prime.com/13361059#eval14731207
31 Jan 2012
New Finding
DOI: 10.3410/f.13361059.14866241
This landmark study provides an important basis to understand how DNA methylation patterns change over time, and how these changes might contribute to phenotypic and genomic evolution.
Perhaps anticipating game-changing improvements in DNA sequencing technology, this study has been able to present...Continue reading
Perhaps anticipating game-changing improvements in DNA sequencing technology, this study has been able to present...Continue reading
This landmark study provides an important basis to understand how DNA methylation patterns change over time, and how these changes might contribute to phenotypic and genomic evolution.
Perhaps anticipating game-changing improvements in DNA sequencing technology, this study has been able to present a detailed sequence-based summary of changes in the DNA methylome that have accumulated over 30 generations among 10 separate lines of Arabidopsis. Marked regional differences are described with respect to the stability of DNA methylation marks. Methylation was most stable in regions that were associated with transposable element-type sequences, with infrequent changes on par with spontaneous DNA mutation rates. By contrast, genic regions were much less stable, with some showing especially high rates of change. Although the bases for these differences remain largely unclear, the level of detail provided by this study offers an essential foundation for future work, including how environmental inputs might contribute to evolutionary processes at the genome level.
Perhaps anticipating game-changing improvements in DNA sequencing technology, this study has been able to present a detailed sequence-based summary of changes in the DNA methylome that have accumulated over 30 generations among 10 separate lines of Arabidopsis. Marked regional differences are described with respect to the stability of DNA methylation marks. Methylation was most stable in regions that were associated with transposable element-type sequences, with infrequent changes on par with spontaneous DNA mutation rates. By contrast, genic regions were much less stable, with some showing especially high rates of change. Although the bases for these differences remain largely unclear, the level of detail provided by this study offers an essential foundation for future work, including how environmental inputs might contribute to evolutionary processes at the genome level.
Disclosures
None declared
Veit B: F1000Prime Recommendation of [Becker C et al., Nature 2011, 480(7376):245-9]. In F1000Prime, 31 Jan 2012; DOI: 10.3410/f.13361059.14866241. F1000Prime.com/13361059#eval14866241
28 Feb 2012
New Finding
DOI: 10.3410/f.13361059.15405119
This landmark paper provides insight into how DNA methylation patterns change over time by bisulfite sequencing a number of mutation accumulation lines, as well as the founders. The rates observed are sufficiently high for epialleles to be a significant contribution to variation. This paper should be...Continue reading
This landmark paper provides insight into how DNA methylation patterns change over time by bisulfite sequencing a number of mutation accumulation lines, as well as the founders. The rates observed are sufficiently high for epialleles to be a significant contribution to variation. This paper should be read in parallel with Schmitz et al. {1}, which reaches similar conclusions with similar data.
References
1.
Transgenerational epigenetic instability is a source of novel methylation variants.
Science 2011 Oct 21; 6054(334):369-73
PMID: 21921155
Disclosures
None declared
Nordborg M: F1000Prime Recommendation of [Becker C et al., Nature 2011, 480(7376):245-9]. In F1000Prime, 28 Feb 2012; DOI: 10.3410/f.13361059.15405119. F1000Prime.com/13361059#eval15405119
F1000Prime Recommendations, Dissents and Comments for [Becker C et al., Nature 2011, 480(7376):245-9]. In F1000Prime, 20 May 2013; F1000Prime.com/13361059
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Heritable epigenetic polymorphisms, such as differential cytosine methylation, can underlie phenotypic variation. Moreover, wild strains of the plant Arabidopsis thaliana differ in many epialleles, and these can influence the expression of nearby genes. However, to understand their role in evolution, it is imperative to ascertain the emergence rate and stability of epialleles, including those that are not due to structural variation. We have compared genome-wide DNA methylation among 10 A. thaliana lines, derived 30 generations ago from a common ancestor. Epimutations at individual positions were easily detected, and close to 30,000 cytosines in each strain were differentially methylated. In contrast, larger regions of contiguous methylation were much more stable, and the frequency of changes was in the same low range as that of DNA mutations. Like individual positions, the same regions were often affected by differential methylation in independent lines, with evidence for recurrent cycles of forward and reverse mutations. Transposable elements and short interfering RNAs have been causally linked to DNA methylation. In agreement, differentially methylated sites were farther from transposable elements and showed less association with short interfering RNA expression than invariant positions. The biased distribution and frequent reversion of epimutations have important implications for the potential contribution of sequence-independent epialleles to plant evolution.
DOI: 10.1038/nature10555
PMID: 22057020
