An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites

Miura, Ai; Nakamura, Miyuki; Inagaki, Soichi; Kobayashi, Akie; Saze, Hidetoshi; Kakutani, Tetsuji

doi:10.1038/emboj.2009.59

Cited by 197 publications

(209 citation statements)

References 38 publications

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“…The MET1 pathway would then maintain rare methylation of CG sites in an H3K9me2-independent manner. Consistent with this possibility, gbM-containing genes are preferred targets for hypermethylation in the ibm1 mutant (16). Last, in support of a role for CMT3 in this model, CMT3 is only present in angiosperms, which coincides with the emergence of gbM in the plant kingdom (6,17).…”

supporting

confidence: 51%

On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

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

285

418

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In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, to our knowledge the first instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum. Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM, supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z, and various histone modifications in E. salsugineum and in Arabidopsis thaliana epigenetic recombinant inbred lines found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modification of chromatin over evolutionary timescales.DNA methylation | gene body methylation | epigenetics | histone modifications | CHROMOMETHYLASE 3 I n angiosperms, cytosine DNA methylation occurs in three sequence contexts: Methylated CG (mCG) is catalyzed by METHYLTRANSFERASE 1 (MET1), mCHG (where H is A/C/T) by CHROMOMETHYLASE 3 (CMT3), and mCHH by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) or CHROMOMETHYLASE 2 (CMT2) (1). MET1 performs a maintenance function and is targeted by VARIANT IN METHYLATION 1 (VIM1), which binds preexisting hemimethylated CG sites. In contrast, DRM2 is targeted by RNA-directed DNA methylation (RdDM) for the de novo establishment of mCHH. CMT3 forms a self-reinforcing loop with the H3K9me2 pathway to maintain mCHG; however, considering that transformation of CMT3 into the cmt3 background can rescue DNA methylation defects, it is reasonable to also consider CMT3 a de novo methyltransferase (2). Two main lines of evidence suggest that DNA methylation plays an important role in the transcriptional silencing of transposable elements (TEs): that TEs are usually methylated, and that the loss of DNA methylation (e.g., in methyltransferase mutants) is often accompanied by TE reactivation.A large number of plant genes (e.g., ∼13.5% of all Arabidopsis thaliana genes) also contain exclusively mCG in the transcribed region and a depletion of mCG from both the transcriptional start and stop sites (referred to as "gene body DNA methylation"; gbM) ( Fig. 1A) (3)(4)(5). A survey of plant methylome data showed that the emergence of gbM in the plant kingdom is specific to angiosperms (6), whereas nonflowering plants (such as mosses and green algae) have much more diverse genic methylation patterns (7,8). Similar to mCG at TEs, the maintenance of gbM requires MET1. In contrast to DNA methylation at TEs, however, gbM does not appear to be associated with transcriptional repression. Rather, genes containing gbM are ubiquitously expressed at moderate to high levels compared with non-gbM genes (4, 5, 9), and within gbM genes there is a correlation between transcript abundance and methylation levels (10, 11).It has been proposed ...

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supporting

confidence: 51%

On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

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

285

418

View full text Add to dashboard Cite

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“…This could be due to only partial removal of the repressive modification(s) and subsequently weaker transcriptional change as observed for several histone demethylase mutants in Arabidopsis (Yu et al, 2008;Miura et al, 2009;Searle et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Six-Rowed Spike3 (VRS3) Is a Histone Demethylase That Controls Lateral Spikelet Development in Barley

et al. 2017

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The complex nature of crop genomes has long prohibited the efficient isolation of agronomically relevant genes. However, recent advances in next-generation sequencing technologies provide new ways to accelerate fine-mapping and gene isolation in crops. We used RNA sequencing of allelic six-rowed spike3 (vrs3) mutants with altered spikelet development for gene identification and functional analysis in barley (Hordeum vulgare). Variant calling in two allelic vrs3 mutants revealed that VRS3 encodes a putative histone Lys demethylase with a conserved zinc finger and Jumonji C and N domain. Sanger sequencing of this candidate gene in independent allelic vrs3 mutants revealed a series of mutations in conserved domains, thus confirming our candidate as the VRS3 gene and suggesting that the row type in barley is determined epigenetically. Global transcriptional profiling in developing shoot apical meristems of vrs3 suggested that VRS3 acts as a transcriptional activator of the row-type genes VRS1 (Hv.HOMEOBOX1) and INTERMEDIUM-C (INT-C; Hv.TEOSINTE BRANCHED1). Comparative transcriptome analysis of the row-type mutants vrs3, vrs4 (Hv.RAMOSA2), and int-c confirmed that all three genes act as transcriptional activators of VRS1 and quantitative variation in the expression levels of VRS1 in these mutants correlated with differences in the number of developed lateral spikelets. The identification of genes and pathways affecting seed number in small grain cereals will enable to further unravel the transcriptional networks controlling this important yield component.

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“…Similarly, we observed a negative correlation of de novo recruited CHG methylation and gene expression. Mutations in the JmjC H3K9m2 demethylase INCREASE IN BONSAI METHYLATION1 (IBM1) gene cause increased CHG methylation within gene bodies, which is associated with severe developmental abnormalities (Miura et al, 2009). Expression of IBM1 was not significantly changed in hypomethylated diploid and triploid seeds (Supplemental Data Set 1), making it unlikely that reduced IBM1 function is causally responsible for increased CHG methylation in hypomethylated seeds.…”

Section: Discussionmentioning

confidence: 99%

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

et al. 2014

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Plants of different ploidy levels are separated by a strong postzygotic hybridization barrier that is established in the endosperm. Deregulated parent-of-origin specific genes cause the response to interploidy hybridizations, revealing an epigenetic basis of this phenomenon. In this study, we present evidence that paternal hypomethylation can bypass the interploidy hybridization barrier by alleviating the requirement for the Polycomb Repressive Complex 2 (PRC2) in the endosperm. PRC2 epigenetically regulates gene expression by applying methylation marks on histone H3. Bypass of the barrier is mediated by suppressed expression of imprinted genes. We show that the hypomethylated pollen genome causes de novo CHG methylation directed to FIS-PRC2 target genes, suggesting that different epigenetic modifications can functionally substitute for each other. Our work presents a method for the generation of viable triploids, providing an impressive example of the potential of epigenome manipulations for plant breeding.

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An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites

Cited by 197 publications

References 38 publications

On the origin and evolutionary consequences of gene body DNA methylation

On the origin and evolutionary consequences of gene body DNA methylation

Six-Rowed Spike3 (VRS3) Is a Histone Demethylase That Controls Lateral Spikelet Development in Barley

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

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