Hidden genetic nature of epigenetic natural variation in plants

Pečinka, Aleš; Abdelsamad, Ahmed; Vu, Giang T. H.

doi:10.1016/j.tplants.2013.07.005

Cited by 43 publications

(28 citation statements)

References 87 publications

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“…The number of mutated genes reported in Table 3 was based on DNA sequence changes, and we did not consider the number of genes that may have undergone changes in their expression owing to epigenetic variation. It has been reported that epigenetic variation is a result of genomic alterations such as CNV, genetic rearrangement, or transposon insertion; and that it affects the function of protein-coding genes (reviewed in Pecinka et al, 2013). Therefore, we cannot rule out the possibility that the expression of genes in the vicinity of the genomic rearrangements may be affected through alterations in epigenetic status or chromatin modifications.…”

Section: Discussionmentioning

confidence: 96%

Comprehensive identification of mutations induced by heavy‐ion beam irradiation in Arabidopsis thaliana

et al. 2015

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SUMMARYHeavy-ion beams are widely used for mutation breeding and molecular biology. Although the mutagenic effects of heavy-ion beam irradiation have been characterized by sequence analysis of some restricted chromosomal regions or loci, there have been no evaluations at the whole-genome level or of the detailed genomic rearrangements in the mutant genomes. In this study, using array comparative genomic hybridization (array-CGH) and resequencing, we comprehensively characterized the mutations in Arabidopsis thaliana genomes irradiated with Ar or Fe ions. We subsequently used this information to investigate the mutagenic effects of the heavy-ion beams. Array-CGH demonstrated that the average number of deleted areas per genome were 1.9 and 3.7 following Ar-ion and Fe-ion irradiation, respectively, with deletion sizes ranging from 149 to 602 180 bp; 81% of the deletions were accompanied by genomic rearrangements. To provide a further detailed analysis, the genomes of the mutants induced by Ar-ion beam irradiation were resequenced, and total mutations, including base substitutions, duplications, in/dels, inversions, and translocations, were detected using three algorithms. All three resequenced mutants had genomic rearrangements. Of the 22 DNA fragments that contributed to the rearrangements, 19 fragments were responsible for the intrachromosomal rearrangements, and multiple rearrangements were formed in the localized regions of the chromosomes. The interchromosomal rearrangements were detected in the multiply rearranged regions. These results indicate that the heavy-ion beams led to clustered DNA damage in the chromosome, and that they have great potential to induce complicated intrachromosomal rearrangements. Heavy-ion beams will prove useful as unique mutagens for plant breeding and the establishment of mutant lines.

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Section: Discussionmentioning

confidence: 96%

Comprehensive identification of mutations induced by heavy‐ion beam irradiation in Arabidopsis thaliana

et al. 2015

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“…Genetic variation has been suggested to be associated with epigenetic variation, such as differential DNA methylation (26,27). We asked whether genetic variation is also associated with methylation interactions in F1 hybrids.…”

Section: Genetic Variations Between Col and C24 Associate With Methylmentioning

confidence: 99%

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

Zhang

Wang

Lang

et al. 2016

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

110

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DNA methylation is a conserved epigenetic mark in plants and many animals. How parental alleles interact in progeny to influence the epigenome is poorly understood. We analyzed the DNA methylomes of Arabidopsis Col and C24 ecotypes, and their hybrid progeny. Hybrids displayed nonadditive DNA methylation levels, termed methylation interactions, throughout the genome. Approximately 2,500 methylation interactions occurred at regions where parental DNA methylation levels are similar, whereas almost 1,000 were at differentially methylated regions in parents. Methylation interactions were characterized by an abundance of 24-nt small interfering RNAs. Furthermore, dysfunction of the RNA-directed DNA methylation pathway abolished methylation interactions but did not affect the increased biomass observed in hybrid progeny. Methylation interactions correlated with altered genetic variation within the genome, suggesting that they may play a role in genome evolution.D NA methylation is a conserved epigenetic mark in many eukaryotes (1-6). In plants and mammals, DNA methylation plays important roles in genome stability, genomic imprinting, paramutation, and gene regulation during development and diseases (1-6). Parental genetic alleles interact in the filial 1 (F1) progeny in a Mendelian manner. DNA methylation may affect this interaction such that methylated epialleles may show nonadditive interactions. This notion is supported by recent observations that hybridization results in nonadditive changes in the F1 plant DNA methylome (7,8). It has been proposed that genome-wide interactions between parental epialleles in F1 hybrids are critical for hybrid vigor, the superior performance of hybrids compared with their parents (8-13). Epigenome interactions may confer nonadditive transcriptional and epigenetic activities in hybrid offspring compared with the parental lines. In contrast to additive regulation, which leads to midparent value (MPV) levels equal to the average of the two parental lines, nonadditive regulation results in a deviation from the MPV, such that the F1 hybrid resembles the high-or low-expression parent. In addition, nonadditive regulation can be transgressive, which is beyond the range of the parental levels (14).Studies in rice and Arabidopsis have identified nonadditive changes in DNA methylation levels at loci where parental methylation levels are different [differentially methylated regions (DMRs)] (7,8,11,12,15,16). These "methylation interactions" were attributed to two mechanisms, transchromosomal methylation (TCM) and transchromosomal demethylation (TCdM), whereby the methylation level of one parental allele is altered to resemble the methylation level of the other parental allele (7,8,17). At some genomic loci, the transmethylation events in F1 were shown to be inherited to the next generation, as observed for paramutation (17). Nonetheless, a thorough profile of DNA methylation interactions across the whole Arabidopsis genome has yet to be determined. In particular, it remains unclear whether DNA m...

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“…Calculating the insertion times of TEs responsible for the hypermethylation of genes may help to determine whether these insertions were contemporaneous to the WGD events, perhaps due to genomic shock. Also, highly methylated genes could be a path to pseudogenization followed by gene loss, but they may also serve as backup copies that may become demethylated and, under certain conditions, transcriptionally active (Pecinka et al, 2013). Collectively, genetic and epigenetic variation triggered by TEs may play an important role in the functional divergence of duplicated genes in soybean and common bean.…”

Section: Differential Methylation Among Duplicated Genes Can Serve Asmentioning

confidence: 99%

A Comparative Epigenomic Analysis of Polyploidy-Derived Genes in Soybean and Common Bean

et al. 2015

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Soybean (Glycine max) and common bean (Phaseolus vulgaris) share a paleopolyploidy (whole-genome duplication [WGD]) event, approximately 56.5 million years ago, followed by a genus Glycine-specific polyploidy, approximately 10 million years ago. Cytosine methylation is an epigenetic mark that plays an important role in the regulation of genes and transposable elements (TEs); however, the role of DNA methylation in the fate/evolution of genes following polyploidy and speciation has not been fully explored. Whole-genome bisulfite sequencing was used to produce nucleotide resolution methylomes for soybean and common bean. We found that, in soybean, CG body-methylated genes were abundant in WGD genes, which were, on average, more highly expressed than single-copy genes and had slower evolutionary rates than unmethylated genes, suggesting that WGD genes evolve more slowly than single-copy genes. CG body-methylated genes were also enriched in shared single-copy genes (single copy in both species) that may be responsible for the broad and high expression patterns of this class of genes. In addition, diverged methylation patterns in non-CG contexts between paralogs were due mostly to TEs in or near genes, suggesting a role for TEs and non-CG methylation in regulating gene expression post polyploidy. Reference methylomes for both soybean and common bean were constructed, providing resources for investigating epigenetic variation in legume crops. Also, the analysis of methylation patterns of duplicated and single-copy genes has provided insights into the functional consequences of polyploidy and epigenetic regulation in plant genomes.

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Hidden genetic nature of epigenetic natural variation in plants

Cited by 43 publications

References 87 publications

Comprehensive identification of mutations induced by heavy‐ion beam irradiation in Arabidopsis thaliana

Comprehensive identification of mutations induced by heavy‐ion beam irradiation in Arabidopsis thaliana

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

A Comparative Epigenomic Analysis of Polyploidy-Derived Genes in Soybean and Common Bean

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