Genetic Perturbation of the Maize Methylome

Li, Qing; Eichten, Steven R.; Hermanson, Peter J.; Zaunbrecher, Virginia; Song, Jawon; Wendt, Jennifer; Rosenbaum, Heidi; Madzima, Thelma F.; Sloan, Amy E.; Huang, Ji; Burgess, Daniel L.; Richmond, Todd; McGinnis, Karen M.; Meeley, Robert B.; Danilevskaya, Olga N.; Vaughn, Matthew; Kaeppler, Shawn M.; Jeddeloh, Jeffrey A.; Springer, Nathan M.

doi:10.1105/tpc.114.133140

Cited by 172 publications

(206 citation statements)

References 71 publications

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“…The average percentages of methylation of CG, CHG and CHH contexts in leaf were 89.7%, 59.1% and 2.1%, respectively (Supplementary Table 24). The genome CG and CHG methylation levels are about the same as those in maize (86.4%, 70.9%) 33 , and are much higher than those in B. distachyon (56.5%, 35.3%) 34 and rice (44%, 24%) 35 . This is consistent with previous observations indicating a positive correlation between genome size, TE content and genomic methylation levels 36 .…”

Section: −13mentioning

confidence: 64%

The Aegilops tauschii genome reveals multiple impacts of transposons

Zhao¹,

Zou²,

et al. 2017

Nature Plants

173

112

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Wheat is an important global crop with an extremely large and complex genome that contains more transposable elements (TEs) than any other known crop species. Here, we generated a chromosome-scale, high-quality reference genome of Aegilops tauschii, the donor of the wheat D genome, in which 92.5% sequences have been anchored to chromosomes. Using this assembly, we accurately characterized genic loci, gene expression, pseudogenes, methylation, recombination ratios, microRNAs and especially TEs on chromosomes. In addition to the discovery of a wave of very recent gene duplications, we detected that TEs occurred in about half of the genes, and found that such genes are expressed at lower levels than those without TEs, presumably because of their elevated methylation levels. We mapped all wheat molecular markers and constructed a high-resolution integrated genetic map corresponding to genome sequences, thereby placing previously detected agronomically important genes/ quantitative trait loci (QTLs) on the Ae. tauschii genome for the first time. NaTuRe PLaNTs

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Section: −13mentioning

confidence: 64%

The Aegilops tauschii genome reveals multiple impacts of transposons

Zhao¹,

Zou²,

et al. 2017

Nature Plants

173

112

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“…Assuming that TE RNA levels accurately reflect transcription rates, this difference in experimental results indicates that the mechanisms of TE repression among meristematic and differentiated cell types are distinct. Consistent with the limited cytosine methylation changes seen in the absence of maize RPD1 (Parkinson et al 2007;Erhard et al 2013;Li et al 2014), Pol IV plays a potentially redundant role in repressing most TE transcription in whole seedlings although a fraction appear to be directly controlled by Pol IV action(s). The genomic and/or molecular features that distinguish these two general classes remain to be identified.…”

Section: Pol IV Affects Gene Regulationmentioning

confidence: 74%

“…The disparate impacts of rpd1/NRPD1A mutations in maize vs. Brassicaceae representatives are potentially related to different genomic TE contents as TE sequences are greatly expanded in maize compared to both Arabidopsis ) and B. rapa (Wang et al 2011). However, recently reported cytosine methylome profiles (Li et al 2014) indicate maize TEs are as equally well methylated in the absence of Pol IV as their Arabidopsis counterparts (Stroud et al 2013), predicting that Pol IV-dependent cytosine methylation is not required to maintain TE silencing. The developmental defects observed in rpd1 mutants are both distinct and nonheritable (Parkinson et al 2007) and therefore unlikely to be related to TE-derived mutations.…”

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confidence: 96%

Nascent Transcription Affected by RNA Polymerase IV inZea mays

et al. 2015

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All eukaryotes use three DNA-dependent RNA polymerases (RNAPs) to create cellular RNAs from DNA templates. Plants have additional RNAPs related to Pol II, but their evolutionary role(s) remain largely unknown. Zea mays (maize) RNA polymerase D1 (RPD1), the largest subunit of RNA polymerase IV (Pol IV), is required for normal plant development, paramutation, transcriptional repression of certain transposable elements (TEs), and transcriptional regulation of specific alleles. Here, we define the nascent transcriptomes of rpd1 mutant and wild-type (WT) seedlings using global run-on sequencing (GRO-seq) to identify the broader targets of RPD1-based regulation. Comparisons of WT and rpd1 mutant GRO-seq profiles indicate that Pol IV globally affects transcription at both transcriptional start sites and immediately downstream of polyadenylation addition sites. We found no evidence of divergent transcription from gene promoters as seen in mammalian GRO-seq profiles. Statistical comparisons identify genes and TEs whose transcription is affected by RPD1. Most examples of significant increases in genic antisense transcription appear to be initiated by 3ʹ-proximal long terminal repeat retrotransposons. These results indicate that maize Pol IV specifies Pol II-based transcriptional regulation for specific regions of the maize genome including genes having developmental significance.KEYWORDS RNA polymerase IV; transcription; gene regulation; transposons; paramutation E UKARYOTES use at least three DNA-dependent RNA polymerases (RNAPs) to transcribe their genomes into functional RNAs. RNAP Pol II generates messenger RNAs (mRNAs) and noncoding RNAs involved in various RNA-mediated regulatory pathways (reviewed by Sabin et al. 2013). Flowering plant genomes encode additional RNAP subunits comprising Pol IV and Pol V, which are central to a small interfering RNA (siRNA)-based silencing pathway primarily targeting repetitive sequences such as transposable elements (TEs) (Matzke and Mosher 2014;Matzke et al. 2015). These additional RNAPs derive from duplications of specific Pol II subunits followed by subfunctionalization during plant evolution (Tucker et al. 2011), yet the holoenzyme complexes still share some Pol II subunits (Ream et al. 2009;Haag et al. 2014).Zea mays (maize) has distinct largest subunits for Pol IV and V and, unlike Arabidopsis thaliana, three second-largest subunits Sidorenko et al. 2009;Stonaker et al. 2009) that in distinct combinations form two Pol IV and three Pol V isoforms (Haag et al. 2014). Genetic analyses of rna polymerase d/e 2a (rpd/e2a) encoding one of the secondlargest subunits (Sidorenko et al. 2009;Stonaker et al. 2009) together with recent proteomic data showing association of a putative RNA-dependent RNA polymerase (RDR2) with only RPD/E2a-containing isoforms (Haag et al. 2014) indicate that maize Pol IV isoforms have diverse functional roles in managing genome homeostasis.Loss of Pol IV function has different consequences in Arabidopsis, Brassica rapa (a close relative of Arabidops...

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“…The ectopic CHH methylation may be caused by an internal balancing mechanism to compensate for the extensive loss of CHG and CG methylation found in heterochromatic TEs due to the loss of OsDDM1 function. Considering that DRM2 or RdDM seems not to be required for CHH methylation of heterochromatic or long TEs in Arabidopsis and maize (Zemach et al, 2013;Li et al, 2014), the ectopic CHH methylation in heterochromatic TEs may be mediated by a CMT2-like activity that was shown to methylate CHH in heterochromatic regions in Arabidopsis (Zemach et al, 2013). However, the osddm1a/1b mutation clearly reduced CHH methylation of small TEs (i.e.…”

Section: Function Of Osddm1 In Te and Teg Methylationmentioning

confidence: 99%

Analysis of Chromatin Regulators Reveals Specific Features of Rice DNA Methylation Pathways

Tan

Zhou²,

Zhou³

et al. 2016

Plant Physiol.

115

157

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Plant DNA methylation that occurs at CG, CHG, and CHH sites (H = A, C, or T) is a hallmark of the repression of repetitive sequences and transposable elements (TEs). The rice (Oryza sativa) genome contains about 40% repetitive sequence and TEs and displays specific patterns of genome-wide DNA methylation. The mechanism responsible for the specific methylation patterns is unclear. Here, we analyzed the function of OsDDM1 (Deficient in DNA Methylation 1) and OsDRM2 (Deficient in DNA Methylation 1) in genome-wide DNA methylation, TE repression, small RNA accumulation, and gene expression. We show that OsDDM1 is essential for high levels of methylation at CHG and, to a lesser extent, CG sites in heterochromatic regions and also is required for CHH methylation that mainly locates in the genic regions of the genome. In addition to a large member of TEs, loss of OsDDM1 leads to hypomethylation and up-regulation of many protein-coding genes, producing very severe growth phenotypes at the initial generation. Importantly, we show that OsDRM2 mutation results in a nearly complete loss of CHH methylation and derepression of mainly small TE-associated genes and that OsDDM1 is involved in facilitating OsDRM2-mediated CHH methylation. Thus, the function of OsDDM1 and OsDRM2 defines distinct DNA methylation pathways in the bulk of DNA methylation of the genome, which is possibly related to the dispersed heterochromatin across chromosomes in rice and suggests that DNA methylation mechanisms may vary among different plant species.DNA methylation in flowering plants occurs in three sequence contexts: the so-called symmetric CG and CHG and the asymmetric CHH, where H is any nucleotide except G. Methylation in each context is believed to be catalyzed primarily by a specific family of DNA methyltransferases: MET1 (homologous to animal Dnmt1) for CG, plant-specific chromomethylases (CMT3 and CMT2) for CHG, and DRM2 (homologous to animal Dnmt3) for CHH (Law and Jacobsen, 2010).Recently, it was shown that CMT2 is a major CHH methyltransferase in Arabidopsis (Arabidopsis thaliana; Zemach et al., 2013;Stroud et al., 2014). The majority of plant methylation is found in transposable elements (TEs) and transcribed TE genes (known as transposable element-related genes [TEGs]) and is crucial for the repression of TE expression and transposition (Law and Jacobsen, 2010). Substantial methylation also is found in the bodies of active genes, where methylation is generally restricted to the CG context (Law and Jacobsen, 2010;Zemach et al., 2010). Methylation in all sequence contexts also is found in the promoter regions of many genes, which represses gene expression.In Arabidopsis, the maintenance of CHH methylation is mediated by RNA-directed DNA methylation (RdDM) involving the methyltransferase activity of DRM2 (Law and Jacobsen, 2010). DNA methylation also is influenced by chromatin factors. For instance, the Arabidopsis Snf2 family nucleosome remodeler DDM1, which can shift nucleosomes in vitro (Brzeski and Jerzmanowski, 2003), is essential fo...

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Genetic Perturbation of the Maize Methylome

Cited by 172 publications

References 71 publications

The Aegilops tauschii genome reveals multiple impacts of transposons

The Aegilops tauschii genome reveals multiple impacts of transposons

Nascent Transcription Affected by RNA Polymerase IV inZea mays

Analysis of Chromatin Regulators Reveals Specific Features of Rice DNA Methylation Pathways

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