Tug of war: adding and removing histone lysine methylation in Arabidopsis

Xiao, Jun; Lee, Un-Sa; Wagner, Doris

doi:10.1016/j.pbi.2016.08.002

Cited by 125 publications

(110 citation statements)

References 142 publications

(76 reference statements)

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“…H3K4 methylation is catalyzed by COMPASS (Complex Proteins Associated with Set1) complexes to activate target genes transcription in yeast, human, and plants. The core components of COMPASS complexes are conserved and include Ash2, RbBP5, and WDR5 (Miller et al , ; Shilatifard, ; Ding et al , ; Xiao et al , ). In Arabidopsis , an Ash2R‐containing COMPASS‐like complex mediates H3K4me3 in FLC to regulate flowering time (Jiang et al , ).…”

Section: Discussionmentioning

confidence: 99%

“…In addition to down-regulation of H3K4me3, loss of function of SEC also resulted in an increase in H3K27me3 levels in FLC chromatin ( Fig 2D). The PRC2 complex maintains a state of transcriptional repression through deposition of H3K27me3 at specific chromatin region, which is conserved in animals and plants (Cao et al, 2002;Schubert et al, 2005;Whitcomb et al, 2007;Xiao et al, 2016). In Drosophila, the location of O-GlcNAc on chromosomes is coincident with Polycomb group (PcG) response elements (PREs; Gambetta et al, 2009;Sinclair et al, 2009), and PREs and TREs (trithorax response elements) may represent the same regions for regulation of target gene expression (Ringrose & Paro, 2004).…”

Section: Sec Mediates Epigenetic Regulation Of Flowering By Catalyzinmentioning

confidence: 99%

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Arabidopsis O ‐Glc NA c transferase SEC activates histone methyltransferase ATX 1 to regulate flowering

Xing

Liu

et al. 2018

The EMBO Journal

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Post‐translational modification of proteins by O‐linked β‐N‐acetylglucosamine (O‐GlcNAc) is catalyzed by O‐GlcNAc transferases (OGTs). O‐GlcNAc modification of proteins regulates multiple important biological processes in metazoans. However, whether protein O‐GlcNAcylation is involved in epigenetic processes during plant development is largely unknown. Here, we show that loss of function of SECRET AGENT (SEC), an OGT in Arabidopsis, leads to an early flowering phenotype. This results from reduced histone H3 lysine 4 trimethylation (H3K4me3) of FLOWERING LOCUS C (FLC) locus, which encodes a key negative regulator of flowering. SEC activates ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1), a histone lysine methyltransferase (HKMT), through O‐GlcNAc modification to augment ATX1‐mediated H3K4me3 histone modification at FLC locus. SEC transfers an O‐GlcNAc group on Ser947 of ATX1, which resides in the SET domain, thereby activating ATX1. Taken together, these results uncover a novel post‐translational O‐GlcNAc modification‐mediated mechanism for regulation of HKMT activity and establish the function of O‐GlcNAc signaling in epigenetic processes in plants.

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Section: Discussionmentioning

confidence: 99%

Section: Sec Mediates Epigenetic Regulation Of Flowering By Catalyzinmentioning

confidence: 99%

Arabidopsis O ‐Glc NA c transferase SEC activates histone methyltransferase ATX 1 to regulate flowering

Xing

Liu

et al. 2018

The EMBO Journal

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“…PRC2 core subunits do not have sequence-specificity; therefore PRC2 target-specificity relies on its interaction with long non-coding RNAs, transcription factors, or other histone modifications to recognize target sites [87–91]. Overall, molecular mechanisms for PRC2 recruitment are poorly understood [92, 93]. Moreover, little is known about how PRC2’s activity can be modulated.…”

Section: Discussionmentioning

confidence: 99%

Systematic discovery of novel eukaryotic transcriptional regulators using sequence homology independent prediction

et al. 2017

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BackgroundThe molecular function of a gene is most commonly inferred by sequence similarity. Therefore, genes that lack sufficient sequence similarity to characterized genes (such as certain classes of transcriptional regulators) are difficult to classify using most function prediction algorithms and have remained uncharacterized.ResultsTo identify novel transcriptional regulators systematically, we used a feature-based pipeline to screen protein families of unknown function. This method predicted 43 transcriptional regulator families in Arabidopsis thaliana, 7 families in Drosophila melanogaster, and 9 families in Homo sapiens. Literature curation validated 12 of the predicted families to be involved in transcriptional regulation. We tested 33 out of the 195 Arabidopsis putative transcriptional regulators for their ability to activate transcription of a reporter gene in planta and found twelve coactivators, five of which had no prior literature support. To investigate mechanisms of action in which the predicted regulators might work, we looked for interactors of an Arabidopsis candidate that did not show transactivation activity in planta and found that it might work with other members of its own family and a subunit of the Polycomb Repressive Complex 2 to regulate transcription.ConclusionsOur results demonstrate the feasibility of assigning molecular function to proteins of unknown function without depending on sequence similarity. In particular, we identified novel transcriptional regulators using biological features enriched in transcription factors. The predictions reported here should accelerate the characterization of novel regulators.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3853-9) contains supplementary material, which is available to authorized users.

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“…Hence, we conclude that S2Lb and WDR5 can associate within one or more HMW complexes in planta, likely corresponding to AtCOMPASS-like complexes. Association of S2Lb with WDR5a was somehow expected given the high conservation of COMPASS subunits from yeast to plants and mammals [39,60,61].…”

Section: S2lb Co-regulates a Large Set Of Genes With Atcompass-like Cmentioning

confidence: 96%

“…Among them, ATX1 (ARABIDOPSIS TRITHORAX1) [32] and ATXR7 (ARABIDOPSIS TRITHORAX-RELATED7) [33,34] appear to target highly specific genomic loci or to be cell-type specific whereas the plant-specific SET DOMAIN GROUP 2/ARABIDOPSIS TRITHORAX RELATED 3 (SDG2) HMT presumably targets a broad repertoire of genes [35,36]. Notwithstanding, while the influence of H3 Lys-4 trimethylation on transcription activation/elongation in plants have begun to emerge [37][38][39][40], the Arabidopsis genomic loci targeted by SDG2 as well as the mechanisms determining its specificity remain undetermined. ATX1 has been shown to have high affinity for Ser5phosphorylated RNPII, a property enabling this COMPASS-associated HMT to facilitate RNPII exit from to the promoter proximal pause region to favor transcription elongation [37,41].…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in histone H3 Lys-4 trimethylation independently from histone H2B monoubiquitination

Fiorucci

Bourbousse

Concia

et al. 2019

Preprint

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The functional determinants of histone H3 Lys-4 trimethylation (H3K4me3), their potential dependency on histone H2B monoubiquitination (H2Bub) and their contribution to defining transcriptional regimes are poorly defined in plant systems. Unlike in S. cerevisiae, where a single SET1 protein catalyzes H3 Lys-4 trimethylation as part of COMPASS (COMPlex of proteins ASsociated with Set1), in Arabidopsis thaliana this activity involves multiple histone methyltransferases (HMTs). Among these, the plant-specific SDG2 (SET DOMAIN GROUP2) has a prominent role. We report that SDG2 co-regulates hundreds of genes with SWD2-like b (S2Lb), a plant ortholog of the Swd2 axillary subunit of yeast COMPASS. S2Lb co-purifies with the AtCOMPASS core subunit WDR5 from a highmolecular weight complex, and both S2Lb and SDG2 directly influence H3K4me3 enrichment over highly transcribed genes. S2Lb knockout triggers pleiotropic developmental phenotypes at the vegetative and reproductive stages, including reduced fertility and seed dormancy. Notwithstanding, s2lb seedlings display little transcriptomic defects as compared to the large repertoire of genes targeted by S2Lb, SDG2 or H3 Lys-4 trimethylation, suggesting that H3K4me3 enrichment is important for optimal gene induction during cellular transitions rather than for determining on/off transcriptional status. Moreover, unlike in budding yeast, most of the S2Lb and H3K4me3 genomic distribution does not rely on a trans-histone crosstalk with histone H2B monoubiquitination. Collectively, this study unveils that the evolutionarily conserved COMPASS-like complex has been coopted by the plant-specific SDG2 HMT and mediates H3K4me3 deposition through an H2Bub-independent pathway in Arabidopsis.

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Tug of war: adding and removing histone lysine methylation in Arabidopsis

Cited by 125 publications

References 142 publications

Arabidopsis O ‐Glc NA c transferase SEC activates histone methyltransferase ATX 1 to regulate flowering

Arabidopsis O ‐Glc NA c transferase SEC activates histone methyltransferase ATX 1 to regulate flowering

Systematic discovery of novel eukaryotic transcriptional regulators using sequence homology independent prediction

Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in histone H3 Lys-4 trimethylation independently from histone H2B monoubiquitination

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