EMF1 and PRC2 Cooperate to Repress Key Regulators of Arabidopsis Development

English version České info

EMBRYONIC FLOWER1 (EMF1) is a plant-specific gene crucial to Arabidopsis vegetative development. Loss of function mutants in the EMF1 gene mimic the phenotype caused by mutations in Polycomb Group protein (PcG) genes, which encode epigenetic repressors that regulate many aspects of eukaryotic development. In Arabidopsis, Polycomb Repressor Complex 2 (PRC2), made of PcG proteins, catalyzes trimethylation of lysine 27 on histone H3 (H3K27me3) and PRC1-like proteins catalyze H2AK119 ubiquitination. Despite functional similarity to PcG proteins, EMF1 lacks sequence homology with known PcG proteins; thus, its role in the PcG mechanism is unclear. To study the EMF1 functions and its mechanism of action, we performed genome-wide mapping of EMF1 binding and H3K27me3 modification sites in Arabidopsis seedlings. The EMF1 binding pattern is similar to that of H3K27me3 modification on the chromosomal and genic level. ChIPOTLe peak finding and clustering analyses both show that the highly trimethylated genes also have high enrichment levels of EMF1 binding, termed EMF1_K27 genes. EMF1 interacts with regulatory genes, which are silenced to allow vegetative growth, and with genes specifying cell fates during growth and differentiation. H3K27me3 marks not only these genes but also some genes that are involved in endosperm development and maternal effects. Transcriptome analysis, coupled with the H3K27me3 pattern, of EMF1_K27 genes in emf1 and PRC2 mutants showed that EMF1 represses gene activities via diverse mechanisms and plays a novel role in the PcG mechanism.

Vyšlo v časopise: EMF1 and PRC2 Cooperate to Repress Key Regulators of Arabidopsis Development. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002512
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002512

Souhrn

Zdroje

1. LeeTIJennerRGBoyerLAGuentherMGLevineSS 2006 Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125 301 313

2. SchwartzYBKahnTGNixDALiXYBourgonR 2006 Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38 700 705

3. KlymenkoTPappBFischleWKocherTSchelderM 2006 A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev 20 1110 1122

4. CaoRWangLWangHXiaLErdjument-BromageH 2002 Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298 1039 1043

5. CaoRZhangY 2004 The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14 155 164

6. CzerminBMelfiRMcCabeDSeitzVImhofA 2002 Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111 185 196

7. KuzmichevANishiokaKErdjument-BromageHTempstPReinbergD 2002 Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16 2893 2905

8. MullerRGoodrichJ 2011 Sweet memories: epigenetic control in flowering. F1000 Biol Rep 3 13

9. DellinoGISchwartzYBFarkasGMcCabeDElginSC 2004 Polycomb silencing blocks transcription initiation. Mol Cell 13 887 893

10. KingIFEmmonsRBFrancisNJWildBMullerJ 2005 Analysis of a polycomb group protein defines regions that link repressive activity on nucleosomal templates to in vivo function. Mol Cell Biol 25 6578 6591

11. FrancisNJKingstonREWoodcockCL 2004 Chromatin compaction by a polycomb group protein complex. Science 306 1574 1577

12. KuMKocheRPRheinbayEMendenhallEMEndohM 2008 Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4 e1000242 doi:10.1371/journal.pgen.1000242

13. MajewskiIJRitchieMEPhipsonBCorbinJPakuschM 2011 Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells. Blood 116 731 739

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

15. ChanvivattanaYBishoppASchubertDStockCMoonYH 2004 Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131 5263 5276

16. SchubertDClarenzOGoodrichJ 2005 Epigenetic control of plant development by Polycomb-group proteins. Curr Opin Plant Biol 8 553 561

17. WoodCCRobertsonMTannerGPeacockWJDennisES 2006 The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci U S A 103 14631 14636

18. KinoshitaTHaradaJJGoldbergRBFischerRL 2001 Polycomb repression of flowering during early plant development. Proc Natl Acad Sci U S A 98 14156 14161

19. HennigLTarantoPWalserMSchonrockNGruissemW 2003 Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130 2555 2565

20. YoshidaNYanaiYChenLKatoYHiratsukaJ 2001 EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13 2471 2481

21. GendallARLevyYYWilsonADeanC 2001 The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107 525 535

22. GrossniklausUVielle-CalzadaJPHoeppnerMAGaglianoWB 1998 Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280 446 450

23. GoodrichJPuangsomleePMartinMLongDMeyerowitzEM 1997 A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386 44 51

24. SchatlowskiNCreaseyKGoodrichJSchubertD 2008 Keeping plants in shape: polycomb-group genes and histone methylation. Semin Cell Dev Biol 19 547 553

25. CalonjeMSungZR 2006 Complexity beneath the silence. Curr Opin Plant Biol 9 530 537

26. HennigLDerkachevaM 2009 Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25 414 423

27. YangCHChenLJSungZR 1995 Genetic regulation of shoot development in Arabidopsis: role of the EMF genes. Dev Biol 169 421 435

28. AubertDChenLMoonYHMartinDCastleLA 2001 EMF1, a novel protein involved in the control of shoot architecture and flowering in Arabidopsis. Plant Cell 13 1865 1875

29. SungZRBelachewAShunongBBertrand-GarciaR 1992 EMF, an Arabidopsis Gene Required for Vegetative Shoot Development. Science 258 1645 1647

30. BouyerDRoudierFHeeseMAndersenEDGeyD 2011 Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7 e1002014 doi:10.1371/journal.pgen.1002014

31. SanchezRKimMYCalonjeMMoonYHSungZR 2009 Temporal and spatial requirement of EMF1 activity for Arabidopsis vegetative and reproductive development. Mol Plant 2 643 653

32. ChenLChengJCCastleLSungZR 1997 EMF genes regulate Arabidopsis inflorescence development. Plant Cell 9 2011 2024

33. MoonYHChenLPanRLChangHSZhuT 2003 EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell 15 681 693

34. KimSYZhuTSungZR 2010 Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiol 152 516 528

35. AlexandreCMoller-SteinbachYSchonrockNGruissemWHennigL 2009 Arabidopsis MSI1 is required for negative regulation of the response to drought stress. Mol Plant 2 675 687

36. CalonjeMSanchezRChenLSungZR 2008 EMBRYONIC FLOWER1 participates in polycomb group-mediated AG gene silencing in Arabidopsis. Plant Cell 20 277 291

37. BratzelFLopez-TorrejonGKochMDel PozoJCCalonjeM 2010 Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20 1853 1859

38. CaoRTsukadaYZhangY 2005 Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20 845 854

39. Sanchez-PulidoLDevosDSungZRCalonjeM 2008 RAWUL: a new ubiquitin-like domain in PRC1 ring finger proteins that unveils putative plant and worm PRC1 orthologs. BMC Genomics 9 308

40. XuLShenWH 2008 Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol 18 1966 1971

41. 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

42. ZhangXClarenzOCokusSBernatavichuteYVPellegriniM 2007 Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5 e129 doi:10.1371/journal.pbio.0050129

43. ParkHYLeeSYSeokHYKimSHSungZR 2011 EMF1 Interacts with EIP1, EIP6 or EIP9 Involved in the Regulation of Flowering Time in Arabidopsis. Plant Cell Physiol 52 1376 1388

44. ToAValonCSavinoGGuilleminotJDevicM 2006 A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18 1642 1651

45. GriffithMEda Silva ConceicaoASmythDR 1999 PETAL LOSS gene regulates initiation and orientation of second whorl organs in the Arabidopsis flower. Development 126 5635 5644

46. BrewerPBHowlesPADorianKGriffithMEIshidaT 2004 PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower. Development 131 4035 4045

47. Alvarez-BuyllaERPelazSLiljegrenSJGoldSEBurgeffC 2000 An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci U S A 97 5328 5333

48. BemerMHeijmansKAiroldiCDaviesBAngenentGC 2010 An atlas of type I MADS box gene expression during female gametophyte and seed development in Arabidopsis. Plant Physiol 154 287 300

49. MasieroSColomboLGriniPESchnittgerAKaterMM 2011 The emerging importance of type I MADS box transcription factors for plant reproduction. Plant Cell 23 865 872

50. AidaMTasakaM 2006 Genetic control of shoot organ boundaries. Curr Opin Plant Biol 9 72 77

51. AidaMIshidaTFukakiHFujisawaHTasakaM 1997 Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9 841 857

52. HaCMJunJHFletcherJC 2010 Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics 186 197 206

53. KiefferMMasterVWaitesRDaviesB 2011 TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J

54. LafosMKrollPHohenstattMLThorpeFLClarenzO 2011 Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet 7 e1002040 doi:10.1371/journal.pgen.1002040

55. Rubio-SomozaIWeigelD 2011 MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16 258 264

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

57. MalloryAVaucheretH 2010 Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22 3879 3889

58. HaCMJunJHNamHGFletcherJC 2004 BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 45 1361 1370

59. KarimMRHirotaAKwiatkowskaDTasakaMAidaM 2009 A role for Arabidopsis PUCHI in floral meristem identity and bract suppression. Plant Cell 21 1360 1372

60. ChiniAFonsecaSFernandezGAdieBChicoJM 2007 The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448 666 671

61. JunJFiumeERoederAHMengLSharmaVK 2010 Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol 154 1721 1736

62. StrabalaTJO'DonnellPJSmitAMAmpomah-DwamenaCMartinEJ 2006 Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiol 140 1331 1344

63. BondDMDennisESFinneganEJ 2011 The low temperature response pathways for cold acclimation and vernalization are independent. Plant Cell Environ 34 1737 1748

64. CarlesCCFletcherJC 2010 Missing links between histones and RNA Pol II arising from SAND? Epigenetics 5 381 385

65. KotakeTTakadaSNakahigashiKOhtoMGotoK 2003 Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol 44 555 564

66. BratzelFYangCAngelovaALopez-TorrejonGKochM 2011 Regulation of the New Arabidopsis Imprinted Gene AtBMI1C Requires the Interplay of Different Epigenetic Mechanisms. Mol Plant

67. SimonJAKR 2009 Mechanism of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10 697 708

68. SchwartzYBKahnTGStenbergPOhnoKBourgonR 2010 Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet 6 e1000805 doi:10.1371/journal.pgen.1000805

69. SchoeftnerSSenguptaAKKubicekSMechtlerKSpahnL 2006 Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. Embo J 25 3110 3122

70. ChenDMolitorALiuCShenWH 2010 The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res 20 1332 1344

71. KallinEMCaoRJothiRXiaKCuiK 2009 Genome-wide uH2A localization analysis highlights Bmi1-dependent deposition of the mark at repressed genes. PLoS Genet 5 e1000506 doi:10.1371/journal.pgen.1000506

72. ChenLJDiaoZYSpechtCSungZR 2009 Molecular evolution of VEF-domain-containing PcG genes in plants. Mol Plant 2 738 754

73. LuoMPlattenDChaudhuryAPeacockWJDennisES 2009 Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2 711 723

74. WeinhoferIHehenbergerERoszakPHennigLKohlerC 2010 H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet 6 e1001152 doi:10.1371/journal.pgen.1001152

75. CarlesCCFletcherJC 2009 The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev 23 2723 2728

76. MurashigeTSkoogF 1962 A revised medium for rapid growth and bioassays with tocacco tissue cultures. Physiological Plant 15 473 497

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

78. ZilbermanDGehringMTranRKBallingerTHenikoffS 2007 Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39 61 69

79. ZilbermanDColeman-DerrDBallingerTHenikoffS 2008 Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456 125 129

80. BuckMJNobelABLiebJD 2005 ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6 R97

81. BerardiniTZMundodiSReiserLHualaEGarcia-HernandezM 2004 Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135 745 755