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

Zhang, Qingzhu; Wang, Dong; Lang, Zhaobo; He, Li; Zeng, Liang; Li, Yanqiang; Zhao, Cheng; Huang, Huan; Zhang, Heng; Zhang, Huiming; Zhu, Jian‐Kang

doi:10.1073/pnas.1607851113

Cited by 87 publications

(119 citation statements)

References 50 publications

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“…Both analyses conclude that 24nt siRNAs are important for the initiation of TCM and TCdM events. Zhang et al showed that hybrid vigor is not affected by the abolition of the POLIV/POLV-directed TCM and TCdM events (42). We showed that the altered m C states can affect gene expression but had no evidence that hybrid vigor was affected.…”

Section: Discussionmentioning

confidence: 58%

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Greaves

Eichten

Groszmann

et al. 2016

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

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Hybrid Arabidopsis plants undergo epigenetic reprogramming producing decreased levels of 24-nt siRNAs and altered patterns of DNA methylation that can affect gene expression. Driving the changes in methylation are the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM). In TCM/TCdM the methylation state of one allele is altered to resemble the other allele. We show that Pol IV-dependent sRNAs are required to establish TCM events. The changes in DNA methylation and the associated changes in sRNA levels in the F1 hybrid can be maintained in subsequent generations and affect hundreds of regions in the F2 epigenome. The inheritance of these altered epigenetic states varies in F2 individuals, resulting in individuals with genetically identical loci displaying different epigenetic states and gene expression profiles. The change in methylation at these regions is associated with the presence of sRNAs. Loci without any sRNA activity can have altered methylation states, suggesting that a sRNA-independent mechanism may also contribute to the altered methylation state of the F1 and F2 generations.H ybrid vigor, heterosis, is important in agriculture due to the increased performance of hybrid plants over parental lines. The increase in performance is attributable to changes in gene expression (1, 2) but how these changes result in the increased performance of the hybrid is still not known. The level of hybrid vigor is believed to correlate with the genetic distance between parental lines; however, hybrid vigor can occur in progeny derived from crosses of genetically similar parents. An example is found in intraspecific crosses between Arabidopsis thaliana accessions. In crosses between C24 and Landsberg erecta (Ler), up to a 100% increase in plant biomass and seed yield is observed (3). The different epigenomes of the two parental accessions could provide the diversity required to initiate gene expression changes and vigor-related characteristics. A number of laboratories have investigated whether there are epigenetic changes in Arabidopsis hybrids, whether they affect gene expression, and whether they contribute to the hybrid vigor phenotype (1, 3-6).We have previously established that F1 hybrids between Arabidopsis accessions undergo some epigenetic reprogramming. We found that the abundance of 24-nt siRNAs is reduced in F1 hybrids and that a second epigenetic system, DNA methylation ( m C), is also altered in the hybrid genome (1, 3, 5). The altered m C patterns in the hybrids involve the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM), where the m C state of one parental allele is altered to resemble the other allele (reviewed in ref. 7). Due to the presence of siRNAs at regions that undergo TCM/TCdM, we have suggested that siRNAs are the initiating molecules that establish these TCM/TCdM events (reviewed in ref. 8). In the hybrid nucleus, the complement of 24-nt siRNAs can interact with homologous sequences from either parent.The TCM and TCdM...

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Section: Discussionmentioning

confidence: 58%

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Greaves

Eichten

Groszmann

et al. 2016

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

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“…Therefore, we cannot exclude their importance in establishing a new epigenetic state near TAD3-1 in F1s, leading to the progressive methylation of the Col-0 allele (Fig 5A). Indeed, several reports point toward drastic modifications of sRNA populations between hybrids and their parents, associated with changes in DNA methylation patterns [32–35]. Interestingly, regions localized in the vicinity of TEs seem to be particularity prone to changes in sRNA contents [36] and DNA methylation [35] in hybrids.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, several reports point toward drastic modifications of sRNA populations between hybrids and their parents, associated with changes in DNA methylation patterns [32–35]. Interestingly, regions localized in the vicinity of TEs seem to be particularity prone to changes in sRNA contents [36] and DNA methylation [35] in hybrids. Nevertheless, while sRNAs could initiate the spreading of methylation toward TAD3-1 in an initial step, none of the genes involved in 24-nt sRNA synthesis tested in our study (Table 2) are important to maintain the tad3-1 epiallele.…”

Section: Discussionmentioning

confidence: 99%

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An Arabidopsis Natural Epiallele Maintained by a Feed-Forward Silencing Loop between Histone and DNA

et al. 2017

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The extent of epigenetic variation is currently well documented, but the number of natural epialleles described so far remains very limited. Determining the relevance of epigenetic changes for natural variation is an important question of research that we investigate by isolating natural epialleles segregating in Arabidopsis recombinant populations. We previously described a genetic incompatibility among Arabidopsis strains based on the silencing of a gene involved in fitness. Here, we isolated a new epiallele resulting from the silencing of a transfer-RNA editing gene in an Arabidopsis accession from the Netherlands (Nok-1). Crosses with the reference accession Col-0 show a complete incompatibility between this epiallele and another locus localized on a different chromosome. We demonstrate that conversion of an unmethylated version of this allele occurs in hybrids, associated with modifications of small RNA populations. These epialleles can also spontaneously revert within the population. Furthermore, we bring evidence that neither METHYLTRANSFERASE 1, maintaining methylation at CGs, nor components of RNA-directed DNA methylation, are key factors for the transmission of the epiallele over generations. This depends only on the self-reinforcing loop between CHROMOMETHYLASE 3 and KRYPTONITE, involving DNA methylated in the CHG context and histone H3 lysine 9 methylation. Our findings reveal a predominant role of this loop in maintaining a natural epiallele.

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“…In hybrid plants, DNA methylation and histone modifications on one chromosome can be transferred to other homologous regions, likely via siRNAs, which can sometimes induce heritable changes of gene expression and phenotypes404142. Paramutation is one such well-known phenomenon, where allelic transfer of epigenetic states occurs in hybrid plants43, and indeed paramutation-like effects have been observed between two T-DNA sequences in Arabidopsis F1 plants1244.…”

Section: Discussionmentioning

confidence: 99%

Epigenetic Regulation of Intronic Transgenes in Arabidopsis

Osabe

Harukawa

Miura

et al. 2017

Sci Rep

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Defense mechanisms of plant genomes can epigenetically inactivate repetitive sequences and exogenous transgenes. Loss of mutant phenotypes in intronic T-DNA insertion lines by interaction with another T-DNA locus, termed T-DNA suppression, has been observed in Arabidopsis thaliana, although the molecular basis of establishment and maintenance of T-DNA suppression is poorly understood. Here we show that maintenance of T-DNA suppression requires heterochromatinisation of T-DNA sequences and the nuclear proteins, INCREASED IN BONSAI METHYLATION 2 (IBM2) and ENHANCED DOWNY MILDEW 2 (EDM2), which prevent ectopic 3′ end processing of mRNA in atypically long introns containing T-DNA sequences. Initiation of T-DNA suppression is mediated by the canonical RdDM pathway after hybridisation of two T-DNA strains, accompanied by DNA hypermethylation of T-DNA sequences in the F1 generation. Our results reveal the presence of a genome surveillance mechanism through genome hybridisation that masks repetitive DNAs intruding into transcription units.

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

Cited by 87 publications

References 50 publications

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

An Arabidopsis Natural Epiallele Maintained by a Feed-Forward Silencing Loop between Histone and DNA

Epigenetic Regulation of Intronic Transgenes in Arabidopsis

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