Epigenetic and Genetic Influences on DNA Methylation Variation in Maize Populations

Eichten, Steven R.; Briskine, Roman; Song, Jawon; Li, Qing; Swanson-Wagner, Ruth A.; Hermanson, Peter J.; Waters, Amanda J.; Starr, Evan; West, Patrick T.; Tiffin, Peter; Myers, Chad L.; Vaughn, Matthew; Springer, Nathan M.

doi:10.1105/tpc.113.114793

Cited by 213 publications

(230 citation statements)

References 68 publications

(108 reference statements)

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“…These events may be a common result of hybridization and could have implications for the transcriptome of the hybrid plant. Although paramutation was initially described at only a small number of loci in maize, recent evidence indicates it occurs more frequently, with both m C and gene expression in maize hybrids being altered in many genes through paramutation-like events (35)(36)(37). The two loci examined here maintained the F1 m C patterns into the F2 generation, whereas other TCM events may show variable penetrance in subsequent generations.…”

Section: Discussionmentioning

confidence: 86%

Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

Greaves

Groszmann

Wang

et al. 2014

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

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Hybridization in plants leads to transinteractions between the parental genomes and epigenomes that can result in changes to both 24 nt siRNA and cytosine methylation ( m C) levels in the hybrid. In Arabidopsis the principle processes altering the hybrid methylome are Trans Chromosomal Methylation (TCM) and Trans Chromosomal deMethylation (TCdM) in which the m C pattern of a genomic segment attains the same m C pattern of the corresponding segment on the other parental chromosome. We examined two loci that undergo TCM/TCdM in the Arabidopsis C24/Landsberg erecta (Ler) F1 hybrids, which show patterns of inheritance dependent on the properties of the particular donor and recipient chromosomal segments. At At1g64790 the TCM-and TCdMderived m C patterns are maintained in the F2 generation but are transmitted in outcrosses or backcrosses only by the C24 genomic segment. At a region between and adjacent to At3g43340 and At3g43350, the originally unmethylated Ler genomic segment receives the C24 m C pattern in the F1, which is then maintained in backcross plants independent of the presence of the parental C24 segment. In backcrosses to an unmethylated Ler allele, the newly methylated F1 Ler segment may act as a TCM source in a process comparable to paramutation in maize. TCM-derived m C patterns are associated with reduced expression of both At3g43340 and At3g43350 in F1 and F2 plants, providing support for such events influencing the transcriptome. The inheritance of the F1 m C patterns and the segregation of other genetic and epigenetic determinants may contribute to the reduced hybrid vigor in the F2 and subsequent generations.heterosis | chromatin | histones | RdDM

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Section: Discussionmentioning

confidence: 86%

Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

Greaves

Groszmann

Wang

et al. 2014

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

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“…Whole-genome bisulfite sequencing (WGBS) data from the third leaf of B73 seedlings (16) were used to determine the coverage and level of DNA methylation in each sequence context for nonoverlapping 100-bp tiles across the entire maize genome. There are 29,922 maize genes with coverage for at least 50% of the tiles in the 2-kb region immediately upstream of maize genes and 25,973 genes with at least 50% coverage for the 2-kb region downstream of maize genes.…”

Section: Resultsmentioning

confidence: 99%

“…WGBS and RNA-seq data for B73 shoot apex, immature ear and anther tissue, H3K4me3 ChIP-seq for B73 seedling leaf tissue, RNA-seq data for mop1, mop3, and wild-type siblings earshoot/seedling leaf, and WGBS data for PH207 seedling leaf were generated for experiments described in this paper. In addition the analyses in this study used previously published WGBS data for B73 seedling leaf and RNA-seq data for B73, Mo17, Oh43, Tx303, and CML322 seedling leaf from Eichten et al (16), H3K9me2 ChIP-seq data for B73 seedling from West et al (10), WGBS data for Mo17, Oh43, Tx303, and CML322 seedling leaf from Li et al (19), WGBS data for mop1 earshoot and targeted bisulfite sequencing data for mop1 earshoot, B73, mop2, and mop3 seedling leaf from Li et al (22), and chromatin accessibility data for B73 earshoot from Gent et al (13).…”

Section: Methodsmentioning

confidence: 99%

RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome

Gent

Zynda

et al. 2015

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

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The maize genome is relatively large (∼2.3 Gb) and has a complex organization of interspersed genes and transposable elements, which necessitates frequent boundaries between different types of chromatin. The examination of maize genes and conserved noncoding sequences revealed that many of these are flanked by regions of elevated asymmetric CHH (where H is A, C, or T) methylation (termed mCHH islands). These mCHH islands are quite short (∼100 bp), are enriched near active genes, and often occur at the edge of the transposon that is located nearest to genes. The analysis of DNA methylation in other sequence contexts and several chromatin modifications revealed that mCHH islands mark the transition from heterochromatin-associated modifications to euchromatin-associated modifications. The presence of an mCHH island is fairly consistent in several distinct tissues that were surveyed but shows some variation among different haplotypes. The presence of insertion/ deletions in promoters often influences the presence and position of an mCHH island. The mCHH islands are dependent upon RNA-directed DNA methylation activities and are lost in mop1 and mop3 mutants, but the nearby genes rarely exhibit altered expression levels. Instead, loss of an mCHH island is often accompanied by additional loss of DNA methylation in CG and CHG contexts associated with heterochromatin in nearby transposons. This suggests that mCHH islands and RNA-directed DNA methylation near maize genes may act to preserve the silencing of transposons from activity of nearby genes.T he cytosine bases in a genome can be modified to 5-methylcytosine by adding a methyl group at the 5′ position. This process, called DNA methylation, is conserved from algae to animals and plants (1, 2). DNA methylation can be separated into different types based on the local sequence context. In plants DNA methylation is found at the symmetric CG or CHG (where H = A, C, or T) sites or at nonsymmetric CHH sites. CG and CHG methylation are maintained at high fidelity following DNA replication due to activity of maintenance methyltransferases such as MET1 or chromomethylase (CMT) 3 (3, 4), whereas CHH methylation (mCHH) requires targeting by either domains rearranged methylase 2 (DRM2) or CMT2 (3-6). The DRM2 targeting occurs via RNAdirected DNA methylation (RdDM) and requires the activity of polymerase IV (PolIV) and polymerase V (PolV) complexes (3, 4). There is evidence that recruitment of PolIV and PolV may require the presence of dimethylation of lysine 9 of histone H3 (H3K9me2) or DNA methylation at the targeted genomic regions (7,8). The specific mechanisms that recruit CMT2 are not well characterized but may require specific histone modifications (5, 6).Much of our knowledge of DNA methylation in plants is derived from studies of the model plant Arabidopsis thaliana, which has a relatively small genome and relatively few examples of genes with nearby transposons (36.3%; ref. 9). The maize genome is much more complex, with the majority (85.5%) of genes positioned within 1...

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“…Insertions of DNA transposons or retrotransposons within or near genes have been reported to negatively affect the expression of genes by decreasing or abolishing transcription (Kumar and Bennetzen, 1999;Hollister and Gaut, 2009;Ahmed et al, 2011;Eichten et al, 2012Eichten et al, , 2013. For example, the null wx-ml allele originated from the insertion of the 409-bp DNA transposon Dissociation 1 in the 9th exon of the waxy (wx) gene in maize (Wessler, 1991).…”

Section: Discussionmentioning

confidence: 99%

Transposable Element Insertion and Epigenetic Modification Cause the Multiallelic Variation in the Expression of FAE1 in Sinapis alba

Zeng

Cheng

2014

The Plant Cell

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Naturally occurring heritable variation provides a fundamental resource to reveal the genetic and molecular bases of traits in forward genetic studies. Here, we report the molecular basis of the differences in the four alleles E 1 , E 2 , E 3 , and e of the FATTY ACID ELONGATION1 (FAE1) gene controlling high, medium, low, and zero erucic content in yellow mustard (Sinapis alba). E 1 represents a fully functional allele with a coding DNA sequence (CDS) of 1521 bp and a promoter adjacent to the CDS. The null allele e resulted from an insertional disruption in the CDS by Sal-PIF, a 3100-bp PIF/Harbinger-like DNA transposon, whereas E 2 and E 3 originated from the insertion of Sal-T1, a 4863-bp Copia-like retrotransposon, in the 59 untranslated region. E 3 was identical to E 2 but showed cytosine methylation in the promoter region and was thus an epiallele having a further reduction in expression. The coding regions of E 2 and E 3 also contained five single-nucleotide polymorphisms (SNPs) not present in E 1 , but expression studies in Saccharomyces cerevisiae indicated that these SNPs did not affect enzyme functionality. These results demonstrate a comprehensive molecular framework for the interplay of transposon insertion, SNP/indel mutation, and epigenetic modification influencing the broad range of natural genetic variation in plants.

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Epigenetic and Genetic Influences on DNA Methylation Variation in Maize Populations

Cited by 213 publications

References 68 publications

Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome

Transposable Element Insertion and Epigenetic Modification Cause the Multiallelic Variation in the Expression of FAE1 in Sinapis alba

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