#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Companion Cell–Dominant and Developmentally Regulated H3K4 Demethylase Controls Flowering Time in via the Repression of Expression


Flowering time relies on the integration of intrinsic developmental cues and environmental signals. FLC and its downstream target FT are key players in the floral transition in Arabidopsis. Here, we characterized the expression pattern and function of JMJ18, a novel JmjC domain-containing histone H3K4 demethylase gene in Arabidopsis. JMJ18 was dominantly expressed in companion cells; its temporal expression pattern was negatively and positively correlated with that of FLC and FT, respectively, during vegetative development. Mutations in JMJ18 resulted in a weak late-flowering phenotype, while JMJ18 overexpressors exhibited an obvious early-flowering phenotype. JMJ18 displayed demethylase activity toward H3K4me3 and H3K4me2, and bound FLC chromatin directly. The levels of H3K4me3 and H3K4me2 in chromatins of FLC clade genes and the expression of FLC clade genes were reduced, whereas FT expression was induced and the protein expression of FT increased in JMJ18 overexpressor lines. The early-flowering phenotype caused by the overexpression of JMJ18 was mainly dependent on the functional FT. Our findings suggest that the companion cell–dominant and developmentally regulated JMJ18 binds directly to the FLC locus, reducing the level of H3K4 methylation in FLC chromatin and repressing the expression of FLC, thereby promoting the expression of FT in companion cells to stimulate flowering.


Vyšlo v časopise: A Companion Cell–Dominant and Developmentally Regulated H3K4 Demethylase Controls Flowering Time in via the Repression of Expression. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002664
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002664

Souhrn

Flowering time relies on the integration of intrinsic developmental cues and environmental signals. FLC and its downstream target FT are key players in the floral transition in Arabidopsis. Here, we characterized the expression pattern and function of JMJ18, a novel JmjC domain-containing histone H3K4 demethylase gene in Arabidopsis. JMJ18 was dominantly expressed in companion cells; its temporal expression pattern was negatively and positively correlated with that of FLC and FT, respectively, during vegetative development. Mutations in JMJ18 resulted in a weak late-flowering phenotype, while JMJ18 overexpressors exhibited an obvious early-flowering phenotype. JMJ18 displayed demethylase activity toward H3K4me3 and H3K4me2, and bound FLC chromatin directly. The levels of H3K4me3 and H3K4me2 in chromatins of FLC clade genes and the expression of FLC clade genes were reduced, whereas FT expression was induced and the protein expression of FT increased in JMJ18 overexpressor lines. The early-flowering phenotype caused by the overexpression of JMJ18 was mainly dependent on the functional FT. Our findings suggest that the companion cell–dominant and developmentally regulated JMJ18 binds directly to the FLC locus, reducing the level of H3K4 methylation in FLC chromatin and repressing the expression of FLC, thereby promoting the expression of FT in companion cells to stimulate flowering.


Zdroje

1. LugerKMaderAWRichmondRKSargentDFRichmondTJ 1997 Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 251 260

2. KouzaridesT 2007 Chromatin modifications and their function. Cell 128 693 705

3. LiBCareyMWorkmanJL 2007 The role of chromatin during transcription. Cell 128 707 719

4. BannisterAJZegermanPPartridgeJFMiskaEAThomasJO 2001 Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 120 124

5. KimTBuratowskiS 2009 Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5′ transcribed regions. Cell 137 259 272

6. ZhangXGermannSBlusBJKhorasanizadehSGaudinV 2007 The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14 869 871

7. TurckFRoudierFFarronaSMartin-MagnietteMLGuillaumeE 2007 Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3 e86 doi:10.1371/journal.pgen.0030086

8. WangGGSongJWangZDormannHLCasadioF 2009 Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459 847 851

9. LiuCLuFCuiXCaoX 2010 Histone methylation in higher plants. Annu Rev Plant Biol 61 395 420

10. ZhaoZYuYMeyerDWuCShenWH 2005 Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat Cell Biol 7 1256 1260

11. CaoYDaiYCuiSMaL 2008 Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20 2586 2602

12. BastowRMylneJSListerCLippmanZMartienssenRA 2004 Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427 164 167

13. JiangDWangYHeY 2008 Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3 e3404 doi:10.1371/journal.pone.0003404

14. PasiniDBrackenAPJensenMRLazzerini DenchiEHelinK 2004 Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23 4061 4071

15. RingroseLParoR 2004 Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38 413 443

16. KloseRJKallinEMZhangY 2006 JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7 715 727

17. KloseRJYamaneKBaeYZhangDErdjument-BromageH 2006 The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442 312 316

18. ShiYLanFMatsonCMulliganPWhetstineJR 2004 Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119 941 953

19. AggerKCloosPAChristensenJPasiniDRoseS 2007 UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449 731 734

20. CloosPAChristensenJAggerKMaiolicaARappsilberJ 2006 The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 442 307 311

21. WhetstineJRNottkeALanFHuarteMSmolikovS 2006 Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125 467 481

22. YamaneKToumazouCTsukadaYErdjument-BromageHTempstP 2006 JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125 483 495

23. OkadaYScottGRayMKMishinaYZhangY 2007 Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature 450 119 123

24. HeYMichaelsSDAmasinoRM 2003 Regulation of flowering time by histone acetylation in Arabidopsis. Science 302 1751 1754

25. JiangDYangWHeYAmasinoRM 2007 Arabidopsis relatives of the human lysine-specific Demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19 2975 2987

26. LiuFQuesadaVCrevillenPBaurleISwiezewskiS 2007 The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28 398 407

27. LuFLiGCuiXLiuCWangXJ 2008 Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice. J Integr Plant Biol 50 886 896

28. JeongJHSongHRKoJHJeongYMKwonYE 2009 Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS ONE 4 e8033 doi:10.1371/journal.pone.0008033

29. LuFCuiXZhangSLiuCCaoX 2010 JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res 20 387 390

30. MiuraANakamuraMInagakiSKobayashiASazeH 2009 An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J 28 1078 1086

31. NohBLeeSHKimHJYiGShinEA 2004 Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell 16 2601 2613

32. SazeHShiraishiAMiuraAKakutaniT 2008 Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319 462 465

33. SearleIRPontesOMelnykCWSmithLMBaulcombeDC 2010 JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev 24 986 991

34. YuXLiLGuoMChoryJYinY 2008 Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci U S A 105 7618 7623

35. LiWLiuHChengZJSuYHHanHN 2011 DNA Methylation and Histone Modifications Regulate De Novo Shoot Regeneration in Arabidopsis by Modulating WUSCHEL Expression and Auxin Signaling. PLoS Genet 7 e1002243 doi:10.1371/journal.pgen.1002243

36. LuSXKnowlesSMWebbCJCelayaRBChaC 2010 The JmjC domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant Physiol

37. BaurleIDeanC 2006 The timing of developmental transitions in plants. Cell 125 655 664

38. WangJWCzechBWeigelD 2009 miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138 738 749

39. WuGParkMYConwaySRWangJWWeigelD 2009 The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138 750 759

40. HayamaRCouplandG 2003 Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6 13 19

41. AusinIAlonso-BlancoCJarilloJARuiz-GarciaLMartinez-ZapaterJM 2004 Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36 162 166

42. BaurleIDeanC 2008 Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE 3 e2733 doi:10.1371/journal.pone.0002733

43. HeYDoyleMRAmasinoRM 2004 PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18 2774 2784

44. MichaelsSDAmasinoRM 1999 FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11 949 956

45. SchmitzRJTamadaYDoyleMRZhangXAmasinoRM 2009 Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis. Plant Physiol 149 1196 1204

46. JohansonUWestJListerCMichaelsSAmasinoR 2000 Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290 344 347

47. LempeJBalasubramanianSSureshkumarSSinghASchmidM 2005 Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1 e6 doi:10.1371/journal.pgen.0010006

48. LimMHKimJKimYSChungKSSeoYH 2004 A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16 731 740

49. SimpsonGGDijkwelPPQuesadaVHendersonIDeanC 2003 FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113 777 787

50. HornyikCTerziLCSimpsonGG 2010 The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18 203 213

51. LiuFMarquardtSListerCSwiezewskiSDeanC 2010 Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327 94 97

52. SwiezewskiSLiuFMagusinADeanC 2009 Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462 799 802

53. SungSAmasinoRM 2004 Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427 159 164

54. SheldonCCConnABDennisESPeacockWJ 2002 Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14 2527 2537

55. SearleIHeYTurckFVincentCFornaraF 2006 The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20 898 912

56. JiangDGuXHeY 2009 Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21 1733 1746

57. PienSFleuryDMylneJSCrevillenPInzeD 2008 ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20 580 588

58. TamadaYYunJYWooSCAmasinoRM 2009 ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21 3257 3269

59. SungSHeYEshooTWTamadaYJohnsonL 2006 Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38 706 710

60. KardailskyIShuklaVKAhnJHDagenaisNChristensenSK 1999 Activation tagging of the floral inducer FT. Science 286 1962 1965

61. KobayashiYKayaHGotoKIwabuchiMArakiT 1999 A pair of related genes with antagonistic roles in mediating flowering signals. Science 286 1960 1962

62. TakadaSGotoK 2003 Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell 15 2856 2865

63. HeYAmasinoRM 2005 Role of chromatin modification in flowering-time control. Trends Plant Sci 10 30 35

64. AbeMKobayashiYYamamotoSDaimonYYamaguchiA 2005 FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309 1052 1056

65. WiggePAKimMCJaegerKEBuschWSchmidM 2005 Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309 1056 1059

66. CorbesierLVincentCJangSFornaraFFanQ 2007 FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316 1030 1033

67. JaegerKEWiggePA 2007 FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17 1050 1054

68. MathieuJWarthmannNKuttnerFSchmidM 2007 Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17 1055 1060

69. YangWJiangDJiangJHeY 2010 A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. Plant J 62 663 673

70. LuFCuiXZhangSJenuweinTCaoX 2011 Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43 715 719

71. ChristensenJAggerKCloosPAPasiniDRoseS 2007 RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 128 1063 1076

72. IwaseSLanFBaylissPde la Torre-UbietaLHuarteM 2007 The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128 1077 1088

73. LiFHuarteMZaratieguiMVaughnMWShiY 2008 Lid2 is required for coordinating H3K4 and H3K9 methylation of heterochromatin and euchromatin. Cell 135 272 283

74. AlonsoJMStepanovaANLeisseTJKimCJChenH 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657

75. BonkeMThitamadeeSMahonenAPHauserMTHelariuttaY 2003 APL regulates vascular tissue identity in Arabidopsis. Nature 426 181 186

76. ImlauATruernitESauerN 1999 Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11 309 322

77. ClarkeJHDeanC 1994 Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet 242 81 89

78. FletcherJCBrandURunningMPSimonRMeyerowitzEM 1999 Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283 1911 1914

79. HongEHJeongYMRyuJYAmasinoRMNohB 2009 Temporal and spatial expression patterns of nine Arabidopsis genes encoding Jumonji C-domain proteins. Mol Cells 27 481 490

80. AnHRoussotCSuarez-LopezPCorbesierLVincentC 2004 CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131 3615 3626

81. YantLMathieuJSchmidM 2009 Just say no: floral repressors help Arabidopsis bide the time. Curr Opin Plant Biol 12 580 586

82. TurckFFornaraFCouplandG 2008 Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59 573 594

83. KobayashiYWeigelD 2007 Move on up, it's time for change–mobile signals controlling photoperiod-dependent flowering. Genes Dev 21 2371 2384

84. LeeIAmasinoRM 1995 Effect of Vernalization, Photoperiod, and Light Quality on the Flowering Phenotype of Arabidopsis Plants Containing the FRIGIDA Gene. Plant Physiol 108 157 162

85. CloughSJBentAF 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743

86. HemerlyASFerreiraPde Almeida EnglerJVan MontaguMEnglerG 1993 cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5 1711 1723

87. JeffersonRAKavanaghTABevanMW 1987 GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6 3901 3907

88. BowlerCBenvenutoGLaflammePMolinoDProbstAV 2004 Chromatin techniques for plant cells. Plant J 39 776 789

89. SalehAAlvarez-VenegasRAvramovaZ 2008 An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3 1018 1025

90. WesleySVHelliwellCASmithNAWangMBRouseDT 2001 Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27 581 590

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#