-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Regulation of Flowering by the Histone Mark Readers MRG1/2 via Interaction with CONSTANS to Modulate Expression
The photoperiodic flowering in Arabidopsis requires the key regulator CO and its target gene FT. However, how CO regulates FT expression in the context of chromatin remains largely obscure. In this work, we present Arabidopsis MRG1/2 as novel chromatin effectors directly involved in the CO-FT photoperiodic flowering. Firstly, MRG1/2 proteins are identified as recognition factors of H3K4 and H3K36 methylation via their chromodomains. The mrg1 mrg2 double mutant shows a late-flowering phenotype only under long-day conditions through down-regulation of FT but not of CO. MRG2 can directly target in vivo the FT promoter chromatin in a H3K4me3/H3K36me3-level dependent manner. More importantly, MRG2 and CO physically interact and enhance each other's binding to the FT promoter in planta. Determination of co-crystal structures of MRG2 with H3K4me3/H3K36me3 peptides and mutagenesis of a key amino acid residue involved in structural interaction demonstrate that MRG2 reader activity is essential for in planta function. Taken together, our findings uncover a novel mechanism of FT activation in flowering promotion and provide a striking example of mutual interplay between a transcription factor and a histone methylation reader in transcription regulation.
Vyšlo v časopise: Regulation of Flowering by the Histone Mark Readers MRG1/2 via Interaction with CONSTANS to Modulate Expression. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004617
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004617Souhrn
The photoperiodic flowering in Arabidopsis requires the key regulator CO and its target gene FT. However, how CO regulates FT expression in the context of chromatin remains largely obscure. In this work, we present Arabidopsis MRG1/2 as novel chromatin effectors directly involved in the CO-FT photoperiodic flowering. Firstly, MRG1/2 proteins are identified as recognition factors of H3K4 and H3K36 methylation via their chromodomains. The mrg1 mrg2 double mutant shows a late-flowering phenotype only under long-day conditions through down-regulation of FT but not of CO. MRG2 can directly target in vivo the FT promoter chromatin in a H3K4me3/H3K36me3-level dependent manner. More importantly, MRG2 and CO physically interact and enhance each other's binding to the FT promoter in planta. Determination of co-crystal structures of MRG2 with H3K4me3/H3K36me3 peptides and mutagenesis of a key amino acid residue involved in structural interaction demonstrate that MRG2 reader activity is essential for in planta function. Taken together, our findings uncover a novel mechanism of FT activation in flowering promotion and provide a striking example of mutual interplay between a transcription factor and a histone methylation reader in transcription regulation.
Zdroje
1. AmasinoR (2010) Seasonal and developmental timing of flowering. Plant J 61 : 1001–1013.
2. IetswaartR, WuZ, DeanC (2012) Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet 28 : 445–453.
3. AndresF, CouplandG (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13 : 627–639.
4. TurckF, FornaraF, CouplandG (2008) Regulation and Identity of Florigen: FLOWERING LOCUS T Moves Center Stage. Annual Review of Plant Biology 59 : 573–594.
5. TiwariSB, ShenY, ChangHC, HouY, HarrisA, et al. (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187 : 57–66.
6. WenkelS, TurckF, SingerK, GissotL, Le GourrierecJ, et al. (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18 : 2971–2984.
7. HeY (2012) Chromatin regulation of flowering. Trends in Plant Science 17 : 556–562.
8. JiangD, WangY, HeY (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS One 3: e3404.
9. FarronaS, ThorpeFL, EngelhornJ, AdrianJ, DongX, et al. (2011) Tissue-specific expression of FLOWERING LOCUS T in Arabidopsis is maintained independently of polycomb group protein repression. Plant Cell 23 : 3204–3214.
10. Lopez-VernazaM, YangS, MullerR, ThorpeF, de LeauE, et al. (2012) Antagonistic roles of SEPALLATA3, FT and FLC genes as targets of the polycomb group gene CURLY LEAF. PLoS One 7: e30715.
11. LuF, CuiX, ZhangS, JenuweinT, CaoX (2011) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43 : 715–719.
12. JeongJH, SongHR, KoJH, JeongYM, KwonYE, et al. (2009) Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS One 4: e8033.
13. LuF, CuiX, ZhangS, LiuC, CaoX (2010) JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res 20 : 387–390.
14. YangW, JiangD, JiangJ, HeY (2010) A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. Plant J 62 : 663–673.
15. GuX, WangY, HeY (2013) Photoperiodic Regulation of Flowering Time through Periodic Histone Deacetylation of the Florigen Gene FT. PLoS Biology 11: e1001649.
16. ShafiqS, BerrA, ShenW-H (2014) Combinatorial functions of diverse histone methylations inArabidopsis thalianaflowering time regulation. New Phytologist 201 : 312–322.
17. LiuC, LuF, CuiX, CaoX (2010) Histone Methylation in Higher Plants. Annual Review of Plant Biology 61 : 395–420.
18. BerrA, ShafiqS, ShenWH (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809 : 567–576.
19. de la Paz SanchezM, GutierrezC (2009) Arabidopsis ORC1 is a PHD-containing H3K4me3 effector that regulates transcription. Proc Natl Acad Sci U S A 106 : 2065–2070.
20. LeeWY, LeeD, ChungWI, KwonCS (2009) Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J 58 : 511–524.
21. MolitorAM, BuZ, YuY, ShenWH (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10: e1004091.
22. JiangD, GuX, HeY (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21 : 1733–1746.
23. HoppmannV, ThorstensenT, KristiansenPE, VeisethSV, RahmanMA, et al. (2011) The CW domain, a new histone recognition module in chromatin proteins. EMBO J 30 : 1939–1952.
24. HeF, UmeharaT, SaitoK, HaradaT, WatanabeS, et al. (2010) Structural insight into the zinc finger CW domain as a histone modification reader. Structure 18 : 1127–1139.
25. TurckF, RoudierF, FarronaS, Martin-MagnietteML, GuillaumeE, et al. (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3: e86.
26. ZhangX, GermannS, BlusBJ, KhorasanizadehS, GaudinV, et al. (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14 : 869–871.
27. ZhangH, BishopB, RingenbergW, MuirWM, OgasJ (2012) The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol 159 : 418–432.
28. HuY, LiuD, ZhongX, ZhangC, ZhangQ, et al. (2012) CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc Natl Acad Sci U S A 109 : 5773–5778.
29. SunB, HongJ, ZhangP, DongX, ShenX, et al. (2008) Molecular Basis of the Interaction of Saccharomyces cerevisiae Eaf3 Chromo Domain with Methylated H3K36. Journal of Biological Chemistry 283 : 36504–36512.
30. ZhangP, DuJ, SunB, DongX, XuG, et al. (2006) Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3. Nucleic Acids Research 34 : 6621–6628.
31. LarschanE, AlekseyenkoAA, GortchakovAA, PengS, LiB, et al. (2007) MSL Complex Is Attracted to Genes Marked by H3K36 Trimethylation Using a Sequence-Independent Mechanism. Molecular Cell 28 : 121–133.
32. EisenA, UtleyRT, NouraniA, AllardS, SchmidtP, et al. (2001) The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation. J Biol Chem 276 : 3484–3491.
33. ReidJL, MoqtaderiZ, StruhlK (2004) Eaf3 regulates the global pattern of histone acetylation in Saccharomyces cerevisiae. Mol Cell Biol 24 : 757–764.
34. GormanM, FrankeA, BakerBS (1995) Molecular characterization of the male-specific lethal-3 gene and investigations of the regulation of dosage compensation in Drosophila. Development 121 : 463–475.
35. BertramMJ, BerubeNG, Hang-SwansonX, RanQ, LeungJK, et al. (1999) Identification of a gene that reverses the immortal phenotype of a subset of cells and is a member of a novel family of transcription factor-like genes. Mol Cell Biol 19 : 1479–1485.
36. RobinsonSJ, TangLH, MooneyBA, McKaySJ, ClarkeWE, et al. (2009) An archived activation tagged population of Arabidopsis thaliana to facilitate forward genetics approaches. BMC Plant Biol 9 : 101.
37. Suarez-LopezP, WheatleyK, RobsonF, OnouchiH, ValverdeF, et al. (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410 : 1116–1120.
38. WiggePA, KimMC, JaegerKE, BuschW, SchmidM, et al. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309 : 1056–1059.
39. ZhaoZ, YuY, MeyerD, WuC, ShenW-H (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nature Cell Biology 7 : 1256–1260.
40. PienS, FleuryD, MylneJS, CrevillenP, InzeD, et al. (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20 : 580–588.
41. SongYH, SmithRW, ToBJ, MillarAJ, ImaizumiT (2012) FKF1 Conveys Timing Information for CONSTANS Stabilization in Photoperiodic Flowering. Science 336 : 1045–1049.
42. ValverdeF (2004) Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering. Science 303 : 1003–1006.
43. VermeulenM, MulderKW, DenissovS, PijnappelWWMP, van SchaikFMA, et al. (2007) Selective Anchoring of TFIID to Nucleosomes by Trimethylation of Histone H3 Lysine 4. Cell 131 : 58–69.
44. CarrozzaMJ, LiB, FlorensL, SuganumaT, SwansonSK, et al. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123 : 581–592.
45. PardoPS, LeungJK, LucchesiJC, Pereira-SmithOM (2002) MRG15, a novel chromodomain protein, is present in two distinct multiprotein complexes involved in transcriptional activation. J Biol Chem 277 : 50860–50866.
46. ZhangP, DuJ, SunB, DongX, XuG, et al. (2006) Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3. Nucleic Acids Res 34 : 6621–6628.
47. LiD, LiuC, ShenL, WuY, ChenH, et al. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15 : 110–120.
48. ZuoZ, LiuH, LiuB, LiuX, LinC (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21 : 841–847.
49. YaoX, FengH, YuY, DongA, ShenW-H (2013) SDG2-Mediated H3K4 Methylation Is Required for Proper Arabidopsis Root Growth and Development. PLoS ONE 8: e56537.
50. ZuoJ, NiuQW, ChuaNH (2000) Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24 : 265–273.
51. LiZ, LiB, ShenW-H, HuangH, DongA (2012) TCP transcription factors interact with AS2 in the repression of class-I KNOX genes in Arabidopsis thaliana. The Plant Journal 71 : 99–107.
52. SunL, YangZT, SongZT, WangMJ, LuSJ, et al. (2013) The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J 76 : 274–286.
53. LiuH, WangJY, HuangY, LiZ, GongW, et al. (2010) Structural basis for methylarginine-dependent recognition of Aubergine by Tudor. Genes Dev 24 : 1876–1881.
54. LeslieAG, PowellHR, WinterG, SvenssonO, SpruceD, et al. (2002) Automation of the collection and processing of X-ray diffraction data — a generic approach. Acta Crystallogr D Biol Crystallogr 58 : 1924–1928.
55. EmsleyP, LohkampB, ScottWG, CowtanK (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66 : 486–501.
56. AdamsPD, AfoninePV, BunkocziG, ChenVB, DavisIW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66 : 213–221.
Štítky
Genetika Reprodukčná medicína
Článek An Evolutionarily Conserved Role for the Aryl Hydrocarbon Receptor in the Regulation of MovementČlánek Requirement for Drosophila SNMP1 for Rapid Activation and Termination of Pheromone-Induced ActivityČlánek Co-regulated Transcripts Associated to Cooperating eSNPs Define Bi-fan Motifs in Human Gene NetworksČlánek Identification of a Regulatory Variant That Binds FOXA1 and FOXA2 at the Type 2 Diabetes GWAS LocusČlánek tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa CellsČlánek Derlin-1 Regulates Mutant VCP-Linked Pathogenesis and Endoplasmic Reticulum Stress-Induced ApoptosisČlánek A Genetic Assay for Transcription Errors Reveals Multilayer Control of RNA Polymerase II FidelityČlánek The Proprotein Convertase KPC-1/Furin Controls Branching and Self-avoidance of Sensory Dendrites inČlánek Regulation of p53 and Rb Links the Alternative NF-κB Pathway to EZH2 Expression and Cell SenescenceČlánek BMPs Regulate Gene Expression in the Dorsal Neuroectoderm of and Vertebrates by Distinct MechanismsČlánek Unkempt Is Negatively Regulated by mTOR and Uncouples Neuronal Differentiation from Growth Control
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2014 Číslo 9- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- Translational Regulation of the Post-Translational Circadian Mechanism
- An Evolutionarily Conserved Role for the Aryl Hydrocarbon Receptor in the Regulation of Movement
- Eliminating Both Canonical and Short-Patch Mismatch Repair in Suggests a New Meiotic Recombination Model
- Requirement for Drosophila SNMP1 for Rapid Activation and Termination of Pheromone-Induced Activity
- Co-regulated Transcripts Associated to Cooperating eSNPs Define Bi-fan Motifs in Human Gene Networks
- Targeted H3R26 Deimination Specifically Facilitates Estrogen Receptor Binding by Modifying Nucleosome Structure
- Role for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis
- The Tandem Repeats Enabling Reversible Switching between the Two Phases of β-Lactamase Substrate Spectrum
- The Association of the Vanin-1 N131S Variant with Blood Pressure Is Mediated by Endoplasmic Reticulum-Associated Degradation and Loss of Function
- Identification of a Regulatory Variant That Binds FOXA1 and FOXA2 at the Type 2 Diabetes GWAS Locus
- Regulation of Flowering by the Histone Mark Readers MRG1/2 via Interaction with CONSTANS to Modulate Expression
- The Actomyosin Machinery Is Required for Retinal Lumen Formation
- Plays a Conserved Role in Assembly of the Ciliary Motile Apparatus
- Hidden Diversity in Honey Bee Gut Symbionts Detected by Single-Cell Genomics
- Ribosome Rescue and Translation Termination at Non-Standard Stop Codons by ICT1 in Mammalian Mitochondria
- tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa Cells
- Causal Variation in Yeast Sporulation Tends to Reside in a Pathway Bottleneck
- Tissue-Specific RNA Expression Marks Distant-Acting Developmental Enhancers
- WC-1 Recruits SWI/SNF to Remodel and Initiate a Circadian Cycle
- Clonal Expansion of Early to Mid-Life Mitochondrial DNA Point Mutations Drives Mitochondrial Dysfunction during Human Ageing
- Methylation QTLs Are Associated with Coordinated Changes in Transcription Factor Binding, Histone Modifications, and Gene Expression Levels
- Differential Management of the Replication Terminus Regions of the Two Chromosomes during Cell Division
- Obesity-Linked Homologues and Establish Meal Frequency in
- Derlin-1 Regulates Mutant VCP-Linked Pathogenesis and Endoplasmic Reticulum Stress-Induced Apoptosis
- Stress-Induced Nuclear RNA Degradation Pathways Regulate Yeast Bromodomain Factor 2 to Promote Cell Survival
- The MAPK p38c Regulates Oxidative Stress and Lipid Homeostasis in the Intestine
- Widespread Genome Reorganization of an Obligate Virus Mutualist
- Trans-kingdom Cross-Talk: Small RNAs on the Move
- The Vip1 Inositol Polyphosphate Kinase Family Regulates Polarized Growth and Modulates the Microtubule Cytoskeleton in Fungi
- Myosin Vb Mediated Plasma Membrane Homeostasis Regulates Peridermal Cell Size and Maintains Tissue Homeostasis in the Zebrafish Epidermis
- GLD-4-Mediated Translational Activation Regulates the Size of the Proliferative Germ Cell Pool in the Adult Germ Line
- Genome Wide Association Studies Using a New Nonparametric Model Reveal the Genetic Architecture of 17 Agronomic Traits in an Enlarged Maize Association Panel
- Translational Regulation of the DOUBLETIME/CKIδ/ε Kinase by LARK Contributes to Circadian Period Modulation
- Positive Selection and Multiple Losses of the LINE-1-Derived Gene in Mammals Suggest a Dual Role in Genome Defense and Pluripotency
- Out of Balance: R-loops in Human Disease
- A Genetic Assay for Transcription Errors Reveals Multilayer Control of RNA Polymerase II Fidelity
- Altered Behavioral Performance and Live Imaging of Circuit-Specific Neural Deficiencies in a Zebrafish Model for Psychomotor Retardation
- Nipbl and Mediator Cooperatively Regulate Gene Expression to Control Limb Development
- Meta-analysis of Mutations in Autism Spectrum Disorders: A Gradient of Severity in Cognitive Impairments
- The Proprotein Convertase KPC-1/Furin Controls Branching and Self-avoidance of Sensory Dendrites in
- Hydroxymethylated Cytosines Are Associated with Elevated C to G Transversion Rates
- Memory and Fitness Optimization of Bacteria under Fluctuating Environments
- Regulation of p53 and Rb Links the Alternative NF-κB Pathway to EZH2 Expression and Cell Senescence
- Interspecific Tests of Allelism Reveal the Evolutionary Timing and Pattern of Accumulation of Reproductive Isolation Mutations
- PRO40 Is a Scaffold Protein of the Cell Wall Integrity Pathway, Linking the MAP Kinase Module to the Upstream Activator Protein Kinase C
- Low Levels of p53 Protein and Chromatin Silencing of p53 Target Genes Repress Apoptosis in Endocycling Cells
- SPDEF Inhibits Prostate Carcinogenesis by Disrupting a Positive Feedback Loop in Regulation of the Foxm1 Oncogene
- RRP6L1 and RRP6L2 Function in Silencing Regulation of Antisense RNA Synthesis
- BMPs Regulate Gene Expression in the Dorsal Neuroectoderm of and Vertebrates by Distinct Mechanisms
- Unkempt Is Negatively Regulated by mTOR and Uncouples Neuronal Differentiation from Growth Control
- Atkinesin-13A Modulates Cell-Wall Synthesis and Cell Expansion in via the THESEUS1 Pathway
- Dopamine Signaling Leads to Loss of Polycomb Repression and Aberrant Gene Activation in Experimental Parkinsonism
- Histone Methyltransferase MMSET/NSD2 Alters EZH2 Binding and Reprograms the Myeloma Epigenome through Global and Focal Changes in H3K36 and H3K27 Methylation
- Bipartite Recognition of DNA by TCF/Pangolin Is Remarkably Flexible and Contributes to Transcriptional Responsiveness and Tissue Specificity of Wingless Signaling
- The Olfactory Transcriptomes of Mice
- Muscular Dystrophy-Associated and Variants Disrupt Nuclear-Cytoskeletal Connections and Myonuclear Organization
- Interplay of dFOXO and Two ETS-Family Transcription Factors Determines Lifespan in
- Evidence for Widespread Positive and Negative Selection in Coding and Conserved Noncoding Regions of
- Genome-Wide Association Meta-analysis of Neuropathologic Features of Alzheimer's Disease and Related Dementias
- Rejuvenation of Meiotic Cohesion in Oocytes during Prophase I Is Required for Chiasma Maintenance and Accurate Chromosome Segregation
- Admixture in Latin America: Geographic Structure, Phenotypic Diversity and Self-Perception of Ancestry Based on 7,342 Individuals
- Local Effect of Enhancer of Zeste-Like Reveals Cooperation of Epigenetic and -Acting Determinants for Zygotic Genome Rearrangements
- Differential Responses to Wnt and PCP Disruption Predict Expression and Developmental Function of Conserved and Novel Genes in a Cnidarian
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Admixture in Latin America: Geographic Structure, Phenotypic Diversity and Self-Perception of Ancestry Based on 7,342 Individuals
- Nipbl and Mediator Cooperatively Regulate Gene Expression to Control Limb Development
- Genome Wide Association Studies Using a New Nonparametric Model Reveal the Genetic Architecture of 17 Agronomic Traits in an Enlarged Maize Association Panel
- Histone Methyltransferase MMSET/NSD2 Alters EZH2 Binding and Reprograms the Myeloma Epigenome through Global and Focal Changes in H3K36 and H3K27 Methylation
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy