Structural studies on MRG701 chromodomain reveal a novel dimerization interface of MRG proteins in green plants

Liu, Yanchao; Wu, Hen-Ming; Yu, Yu; Huang, Ying

doi:10.1007/s13238-016-0310-5

Cited by 6 publications

(6 citation statements)

References 42 publications

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“…For this, we used 8‐day‐old seedlings of the MRG2 pro :: YFP ‐ MRG2 mrg1 mrg2 line, which express the YFP‐MRG2 fusion protein that fully rescues the mrg1 mrg2 mutant phenotype (Bu et al , 2014; Peng et al , 2018). Our anti‐green fluorescent protein (GFP)/yellow fluorescent protein (YFP) IP‐MS analysis identified MRG2 as a binding protein of YFP‐MRG2 (Table S1), which is consistent with previous findings reporting that plant MRG proteins form homodimers (Liu et al , 2016). Interestingly, AtNAP1;1 was also found to be a binding protein of YFP‐MRG2 in the same analysis (Table S1).…”

Section: Resultssupporting

confidence: 91%

“…In Arabidopsis, it was found that MRG1/MRG2 and NRP1/NRP2 cooperate together in promoting expression of the key floral repressor gene FLC (present study). Considering that the NRP1 and NRP2, as well as MRG1 and MRG2, form both homodimers and heterodimers (Liu et al , 2016; Zhu et al , 2017), it is reasonable to speculate that they may form a higher order complex of multiprotein components. Previous studies showed that the recruitment of MRG1/MRG2 via binding with CO to FT and via binding with PIF7 to YUCCA8 and IAA9 is required for maintaining chromatin H4K5ac levels at the target genes (Bu et al , 2014; Xu et al , 2014; Peng et al , 2018).…”

Section: Discussionmentioning

confidence: 99%

“…By contrast, the readout of the active histone methylation marks by the chromodomain proteins belonging to the MORF4‐related gene (MRG) family is relatively well conserved in eukaryotes. Thus, the yeast EAF3 (Carrozza et al , 2005; Joshi and Struhl, 2005; Keogh et al , 2005), the human MRG15 (Zhang et al , 2006), the Drosophila MSL3/dMRG15 (Larschan et al , 2007), the Arabidopsis MRG1/MRG2 (Bu et al , 2014; Xu et al , 2014) and the rice MRG701/MRG702 (Jin et al , 2015; Liu et al , 2016) were all shown to bind H3K36me3. In Arabidopsis, MRG1/MRG2 physically associates with the transcription factors CONSTANS (CO) and PHYTOCHROME‐INTERACTING FACTOR 7 (PIF7) in specific targeting of FLOWERING LOCUS T ( FT ) and shade‐responsive genes (e.g.…”

Section: Introductionmentioning

confidence: 99%

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The histone methylation readers MRG1/MRG2 and the histone chaperones NRP1/NRP2 associate in fine‐tuning Arabidopsis flowering time

Yin

Wang

et al. 2020

The Plant Journal

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Summary Histones are highly basic proteins involved in packaging DNA into chromatin, and histone modifications are fundamental in epigenetic regulation in eukaryotes. Among the numerous chromatin modifiers identified in Arabidopsis (Arabidopsis thaliana), MORF‐RELATED GENE (MRG)1 and MRG2 have redundant functions in reading histone H3 lysine 36 trimethylation (H3K36me3). Here, we show that MRG2 binds histone chaperones belonging to the NUCLEOSOME ASSEMBLY PROTEIN 1 (NAP1) family, including NAP1‐RELATED PROTEIN (NRP)1 and NRP2. Characterization of the loss‐of‐function mutants mrg1 mrg2, nrp1 nrp2 and mrg1 mrg2 nrp1 nrp2 revealed that MRG1/MRG2 and NRP1/NRP2 regulate flowering time through fine‐tuning transcription of floral genes by distinct molecular mechanisms. In particular, the physical interaction between NRP1/NRP2 and MRG1/MRG2 inhibited the binding of MRG1/MRG2 to the transcription factor CONSTANS (CO), leading to a transcriptional repression of FLOWERING LOCUS T (FT) through impeded H4K5 acetylation (H4K5ac) within the FT chromatin. By contrast, NRP1/NRP2 and MRG1/MRG2 act together, likely in a multiprotein complex manner, in promoting the transcription of FLOWERING LOCUS C (FLC) via an increase of both H4K5ac and H3K9ac in the FLC chromatin. Because the expression pattern of FLC represents the major category of differentially expressed genes identified by genome‐wide RNA‐sequencing analysis in the mrg1 mrg2, nrp1 nrp2 and mrg1 mrg2 nrp1 nrp2 mutants, it is reasonable to speculate that the NRP1/NRP2‐MRG1/MRG2 complex may be involved in transcriptional activation of genes beyond FLC and flowering time control.

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Section: Resultssupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The histone methylation readers MRG1/MRG2 and the histone chaperones NRP1/NRP2 associate in fine‐tuning Arabidopsis flowering time

Yin

Wang

et al. 2020

The Plant Journal

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“…MRG1/MRG2 also can form homodimers and heterodimers (Liu et al, 2016). The tethered PIF-MRG multiprotein complex may contribute to function together for the PIF-binding and MRG-binding sites that are separated with variable distances among different target genes.…”

Section: Discussionmentioning

confidence: 99%

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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“…In higher eukaryotes, changes in pH i have been correlated with cell proliferation [43], differentiation [44], cell cycle progression [45], apoptosis [7] and cancer [46]. In this regard, it is worth noting that His18 of Eaf3 CD is highly conserved (Supplementary Figure S5) and the corresponding histidine of Eaf3 orthologs -namely, His21 in human MRG15, His62 in Arabidopsis MRG2, and His37 in rice MRG701 -actually lies at a structurally equivalent position [47][48][49]. In addition, the interactions between MRG15 CD and methyl-lysine peptides have been found to be strongly sensitive to the pH used for NMR titrations, with little or no interaction between MRG15 CD and H3K36me3 peptide at acidic pH [50].…”

Section: Generality Of the Function Of The Ph I Sensor Activity Of Eamentioning

confidence: 99%

The Eaf3 chromodomain acts as a pH sensor for gene expression by altering its binding affinity for histone methylated-lysine residues

Okuda

Nishimura

2020

Bioscience Reports

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During gene expression, histone acetylation by histone acetyltransferase (HAT) loosens the chromatin structure around the promoter to allow RNA polymerase II (Pol II) to initiate transcription, while de-acetylation by histone deacetylase (HDAC) tightens the structure in the transcribing region to repress false initiation. Histone acetylation is also regulated by intracellular pH (pHi) with global hypoacetylation observed at low pHi, and hyperacetylation, causing proliferation, observed at high pHi. However, the mechanism underlying the pHi-dependent regulation of gene expression remains elusive. Here, we have explored the role of the chromodomain (CD) of budding yeast Eaf3, a common subunit of both HAT and HDAC that is thought to recognize methylated lysine residues on histone H3. We found that Eaf3 CD interacts with histone H3 peptides methylated at Lys4 (H3K4me, a promoter epigenetic marker) and Lys36 (H3K36me, a coding region epigenetic marker), as well as with many dimethyl-lysine peptides and even arginine-asymmetrically dimethylated peptides, but not with unmethylated, phosphorylated or acetylated peptides. The Eaf3 CD structure revealed an unexpected histidine residue in the aromatic cage essential for binding H3K4me and H3K36me. pH titration experiments showed that protonation of the histidine residue around physiological pH controls the charge state of the aromatic cage to regulate binding to H3K4me and H3K36me. Histidine substitution and NMR experiments confirmed the correlation of histidine pKa with binding affinity. Collectively, our findings suggest that Eaf3 CD functions as a pHi sensor and a regulator of gene expression via its pHi-dependent interaction with methylated nucleosomes.

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Structural studies on MRG701 chromodomain reveal a novel dimerization interface of MRG proteins in green plants

Cited by 6 publications

References 42 publications

The histone methylation readers MRG1/MRG2 and the histone chaperones NRP1/NRP2 associate in fine‐tuning Arabidopsis flowering time

The histone methylation readers MRG1/MRG2 and the histone chaperones NRP1/NRP2 associate in fine‐tuning Arabidopsis flowering time

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

The Eaf3 chromodomain acts as a pH sensor for gene expression by altering its binding affinity for histone methylated-lysine residues

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