Arabidopsis MRG domain proteins bridge two histone modifications to elevate expression of flowering genes

Xu, Yifeng; Gan, Eng‐Seng; Zhou, Jie; Wee, Wan-Yi; Zhang, Xiaoyu; Ito, Toshiro

doi:10.1093/nar/gku781

Cited by 69 publications

(97 citation statements)

References 65 publications

(132 reference statements)

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“…4, D and E), which overlaps MRG2 binding regions (Fig. 4C) and thereby is in agreement with MRG1/MRG2 acting as readers of H3K4me3 and H3K36me3 Xu et al, 2014). Strikingly, significant difference was undetected at either H3K4me3 levels (Fig.…”

Section: Mrg2 and Pif7 Bind Chromatin At Shade-responsive Genessupporting

confidence: 83%

“…6). This proposed mechanistic model is based on numerous points of evidence: (1) PIF7 and MRG2 physically interact in vitro and in vivo; (2) PIF7 is dephosphorylated (Li et al, 2012) when plants are exposed to shade, and it is this shade-induced PIF7 form that binds MRG2; (3) both pif7-1 and mrg1mrg2 mutants display impaired hypocotyl elongation and reduced expression levels of a common set of shade-responsive genes under shade treatment; (4) pif7-1 is epistatic to mrg1mrg2 in both hypocotyl elongation and gene expression regulation; (5) PIF7 recognizes the G-box in the promoter (Li et al, 2012) and binds chromatin around it, whereas MRG2 binds H3K4me3/ H3K36me3 Xu et al, 2014) and is enriched together with H3K4me3/H3K36me3 at the 59-end of gene body; (6) shade-induced binding of MRG2 at chromatin is PIF7-dependent and is enhanced by basal level of H3K4me3/H3K36me3; (7) H4K5ac/H3K9ac/H3K27ac are induced under shade treatment, although H3K4me3/ H3K36me3 levels remain unchanged; and (8) MRG2 physically interacts with the H4K5-acetyltransferase HAM1/HAM2 (Xu et al, 2014), and a consistently shade-induced H4K5ac elevation is dependent on PIF7 and MRG1/MRG2.…”

Section: Discussionmentioning

confidence: 99%

“…MRG2 interacts with HAM1/HAM2, which has been proposed to bridge H3K36me3 to H4K5 acetylation (H4K5ac) in transcription activation of FT in flowering time control (Xu et al, 2014). To examine whether a similar mechanism exists in shade response, we analyzed histone acetylation levels at YUCCA8.…”

Section: Pif7/mrg2-mediated Shade-induction Of Gene Expression Is Assmentioning

confidence: 99%

“…In general, methylation on H3K9 or H3K27 is related to gene silencing, whereas methylation on H3K4 or H3K36 is associated with transcription activation (Berr et al, 2011). Interestingly, recent studies demonstrate that the Morf Related Gene (MRG) family proteins MRG1 and MRG2 bind H3K4/H3K36 trimethylation (H3K4me3/ H3K36me3) and physically interact with the transcription factor CONSTANS (CO; Bu et al, 2014) as well as with the HAT-family proteins HAM1 and HAM2 (Xu et al, 2014), pointing to a mechanistic connection of CO with histone methylation and acetylation in activation of Arabidopsis FLOWERING LOCUS T (FT) transcription.…”

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confidence: 99%

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Linking PHYTOCHROME-INTERACTING FACTOR to Histone Modification in Plant Shade Avoidance

Peng

Zhou

et al. 2017

Plant Physiol.

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Shade avoidance syndrome (SAS) allows a plant grown in a densely populated environment to maximize opportunities to access to sunlight. Although it is well established that SAS is accompanied by gene expression changes, the underlying molecular mechanism needs to be elucidated. Here, we identify the H3K4me3/H3K36me3-binding proteins, Morf Related Gene (MRG) group proteins MRG1 and MRG2, as positive regulators of shade-induced hypocotyl elongation in Arabidopsis (Arabidopsis thaliana). MRG2 binds PHYTOCHROME-INTERACTING FACTOR7 (PIF7) and regulates the expression of several common downstream target genes, including YUCCA8 and IAA19 involved in the auxin biosynthesis or response pathway and PRE1 involved in brassinosteroid regulation of cell elongation. In response to shade, PIF7 and MRG2 are enriched at the promoter and gene-body regions and are necessary for increase of histone H4 and H3 acetylation to promote target gene expression. Our study uncovers a mechanism in which the shade-responsive factor PIF7 recruits MRG1/MRG2 that binds H3K4me3/H3K36me3 and brings histone-acetylases to induce histone acetylations to promote expression of shade responsive genes, providing thus a molecular mechanistic link coupling the environmental light to epigenetic modification in regulation of hypocotyl elongation in plant SAS.

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Section: Mrg2 and Pif7 Bind Chromatin At Shade-responsive Genessupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

Section: Pif7/mrg2-mediated Shade-induction Of Gene Expression Is Assmentioning

confidence: 99%

mentioning

confidence: 99%

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Linking PHYTOCHROME-INTERACTING FACTOR to Histone Modification in Plant Shade Avoidance

Peng

Zhou

et al. 2017

Plant Physiol.

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“…For example, H3K36me3 has been shown to function in suppressing cryptic transcriptional initiation and regulating splicing (26). We therefore created the triple mutant met1 sdg7 sdg8, in which both gbM and H3K36me3 were eliminated (27). RNA-seq experiments from met1 sdg7 sdg8 and wild-type Col-0 again failed to identify significant differences in mRNA expression, antisense transcription, or splicing variants in a comparison between gbM loci and UM loci (SI Appendix, Tables S5-S7).…”

mentioning

confidence: 99%

On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

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

Self Cite

281

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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Phenotypic and genotypic resources for the USDA quinoa (Chenopodium quinoa) genebank accessions

et al. 2023

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Quinoa (Chenopodium quinoa) is a nutritious grain, with balanced composition of amino acids, and a facultative halophyte. Under greenhouse conditions, we assessed 148 quinoa accessions from the USDA genebank for grain weight, phenological, and morphological characteristics. For all traits, the analysis of variance revealed a significant difference among accessions. The accessions matured as late as 146 days after planting and produced grain weight up to 19.6 g/plant. Days to maturity showed negative correlation with grain weight per plant, whereas the number of branches was positively correlated with grain weight per plant. By adopting the NsiI/BfaI combination to enhance the genotyping‐by‐sequencing technique, we were able to generate 59,248 filtered single nucleotide polymorphism markers by mapping to the reference genome. Molecular markers showed an average heterozygosity of 11.76% across the accessions with a range of 4.9%–21.9%. The first two principal component analyses (PCAs) explained nearly 50% of molecular markers. The genetic diversity analysis using PCA revealed the presence of four main groups. Groups A and B consisted of mainly Bolivian and Peruvian accessions with relatively slower maturity and taller plant stature. In contrast, groups C and D were mainly accessions registered from USA and Chile with relatively faster maturity and shorter plant stature. Groups C and D together have shown far more private single nucleotide polymorphisms than accessions in A and B groups, indicating the higher levels of diversity within these groups and more levels of similarities among individuals of A and B groups. Marker‐trait association revealed significant markers for grain weight per plant and days to flowering. We only analyzed linkage disequilibrium on the scaffolds that harbor these marker‐trait associations. LD expressed in r2 persisted as high as 0.2 in ranges greater than 600 kb for scaffold 1992 but dropped more quickly for scaffold 1843. These phenotypic and genotypic resources will serve as a reference for the cataloging and conservation of germplasm and, for the selection of a core collection for the improvement of quinoa to address food security.

show abstract

Arabidopsis MRG domain proteins bridge two histone modifications to elevate expression of flowering genes

Cited by 69 publications

References 65 publications

Linking PHYTOCHROME-INTERACTING FACTOR to Histone Modification in Plant Shade Avoidance

Linking PHYTOCHROME-INTERACTING FACTOR to Histone Modification in Plant Shade Avoidance

On the origin and evolutionary consequences of gene body DNA methylation

Phenotypic and genotypic resources for the USDA quinoa (Chenopodium quinoa) genebank accessions

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