Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition
Polycomb repressive complex 2 (PRC2) is a key regulator of epigenetic states catalyzing histone H3 lysine 27 trimethylation (H3K27me3), a repressive chromatin mark. PRC2 composition is conserved from humans to plants, but the function of PRC2 during the early stage of plant life is unclear beyond the fact that it is required for the development of endosperm, a nutritive tissue that supports embryo growth. Circumventing the requirement of PRC2 in endosperm allowed us to generate viable homozygous null mutants for FERTILIZATION INDEPENDENT ENDOSPERM (FIE), which is the single Arabidopsis homolog of Extra Sex Combs, an indispensable component of Drosophila and mammalian PRC2. Here we show that H3K27me3 deposition is abolished genome-wide in fie mutants demonstrating the essential function of PRC2 in placing this mark in plants as in animals. In contrast to animals, we find that PRC2 function is not required for initial body plan formation in Arabidopsis. Rather, our results show that fie mutant seeds exhibit enhanced dormancy and germination defects, indicating a deficiency in terminating the embryonic phase. After germination, fie mutant seedlings switch to generative development that is not sustained, giving rise to neoplastic, callus-like structures. Further genome-wide studies showed that only a fraction of PRC2 targets are transcriptionally activated in fie seedlings and that this activation is accompanied in only a few cases with deposition of H3K4me3, a mark associated with gene activity and considered to act antagonistically to H3K27me3. Up-regulated PRC2 target genes were found to act at different hierarchical levels from transcriptional master regulators to a wide range of downstream targets. Collectively, our findings demonstrate that PRC2-mediated regulation represents a robust system controlling developmental phase transitions, not only from vegetative phase to flowering but also especially from embryonic phase to the seedling stage.
Vyšlo v časopise:
Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1002014
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002014
Souhrn
Polycomb repressive complex 2 (PRC2) is a key regulator of epigenetic states catalyzing histone H3 lysine 27 trimethylation (H3K27me3), a repressive chromatin mark. PRC2 composition is conserved from humans to plants, but the function of PRC2 during the early stage of plant life is unclear beyond the fact that it is required for the development of endosperm, a nutritive tissue that supports embryo growth. Circumventing the requirement of PRC2 in endosperm allowed us to generate viable homozygous null mutants for FERTILIZATION INDEPENDENT ENDOSPERM (FIE), which is the single Arabidopsis homolog of Extra Sex Combs, an indispensable component of Drosophila and mammalian PRC2. Here we show that H3K27me3 deposition is abolished genome-wide in fie mutants demonstrating the essential function of PRC2 in placing this mark in plants as in animals. In contrast to animals, we find that PRC2 function is not required for initial body plan formation in Arabidopsis. Rather, our results show that fie mutant seeds exhibit enhanced dormancy and germination defects, indicating a deficiency in terminating the embryonic phase. After germination, fie mutant seedlings switch to generative development that is not sustained, giving rise to neoplastic, callus-like structures. Further genome-wide studies showed that only a fraction of PRC2 targets are transcriptionally activated in fie seedlings and that this activation is accompanied in only a few cases with deposition of H3K4me3, a mark associated with gene activity and considered to act antagonistically to H3K27me3. Up-regulated PRC2 target genes were found to act at different hierarchical levels from transcriptional master regulators to a wide range of downstream targets. Collectively, our findings demonstrate that PRC2-mediated regulation represents a robust system controlling developmental phase transitions, not only from vegetative phase to flowering but also especially from embryonic phase to the seedling stage.
Zdroje
1. FinkelsteinRReevesWAriizumiTSteberC 2008 Molecular aspects of seed dormancy. Annu Rev Plant Biol 59 387 415
2. HeY 2009 Control of the transition to flowering by chromatin modifications. Molecular Plant 2 554 564
3. FarronaSCouplandGTurckF 2008 The impact of chromatin regulation on the floral transition. Seminars in Cell & Developmental Biology 19 560 573
4. KimDHDoyleMRSungSAmasinoRM 2009 Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25 277 299
5. KinoshitaTHaradaJJGoldbergRB 2001 Polycomb repression of flowering during early plant development. Proceedings of the National Academy of Sciences
6. ChanvivattanaYBishoppASchubertDStockCMoonYH 2004 Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131 5263 5276
7. SchuettengruberBChourroutDVervoortMLeblancBCavalliG 2007 Genome regulation by polycomb and trithorax proteins. Cell 128 735 745
8. SchwartzYBPirrottaV 2008 Polycomb complexes and epigenetic states. Current Opinion in Cell Biology 20 266 273
9. PappBMüllerJ 2006 Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes & Development 20 2041 2054
10. BantigniesFCavalliG 2006 Cellular memory and dynamic regulation of polycomb group proteins. Current Opinion in Cell Biology 18 275 283
11. KohlerCVillarCB 2008 Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18 236 243
12. PienSGrossniklausU 2007 Polycomb group and trithorax group proteins in Arabidopsis. BBA-Gene Structure and Expression 1769 375 382
13. SimonJChiangABenderW 1992 Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 114 493 505
14. StruhlGAkamM 1985 Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J 4 3259 3264
15. FaustCSchumacherAHoldenerBMagnusonT 1995 The eed mutation disrupts anterior mesoderm production in mice. Development 121 273 285
16. HuhJHBauerMJHsiehTFischerR 2007 Endosperm gene imprinting and seed development. Current opinion in genetics & development 17 480 485
17. BergerFChaudhuryA 2009 Parental memories shape seeds. Trends in Plant Science 14 550 556
18. KinoshitaTIkedaYIshikawaR 2008 Genomic imprinting: A balance between antagonistic roles of parental chromosomes. Seminars in Cell and Developmental Biology 19 574 579
19. BarouxCPienSGrossniklausU 2007 Chromatin modification and remodeling during early seed development. Current opinion in genetics & development 17 473 479
20. KatzAOlivaMMosqunaAHakimOOhadN 2004 FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37 707 719
21. AwSJHamamuraYChenZSchnittgerABergerF 2010 Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis. Development
22. NowackMKGriniPEJakobyMJLafosMKonczC 2006 A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38 63 67
23. IwakawaHShinmyoASekineM 2006 Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45 819 831
24. NowackMKShirzadiRDissmeyerNDolfAEndlE 2007 Bypassing genomic imprinting allows seed development. Nature 447 312 315
25. KurzhalsRLTieFStrattonCAHartePJ 2008 Drosophila ESC-like can substitute for ESC and becomes required for Polycomb silencing if ESC is absent. Developmental Biology 313 293 306
26. BramsiepeJSchnittgerA submitted Endoreplication and development. Plant Signaling & Behavior
27. LindrothAMShultisDJasencakovaZFuchsJJohnsonL 2004 Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23 4286 4296
28. NaumannKFischerAHofmannIKraussVPhalkeS 2005 Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24 1418 1429
29. ZhangXClarenzOCokusSBernatavichuteYPellegriniM 2007 Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5 e129 doi:10.1371/journal.pbio.0050129
30. JacobYStroudHLeblancCFengSZhouL 2010 Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 2010 Jul 14
31. MaereSHeymansKKuiperM 2005 BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21 3448 3449
32. YoshidaNYanaiYChenLKatoYHiratsukaJ 2001 EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. The Plant Cell 13 2471 2481
33. TurckFRoudierFFarronaSMartin-MagnietteML 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
34. de FolterSImminkRGKiefferMParenicováLHenzSR 2005 Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. The Plant Cell 17 1424 1433
35. KimHUHsiehKRatnayakeCHuangAH 2002 A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277 22677 22684
36. HundertmarkMHinchaDK 2008 LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9 118
37. Bies-EthèveNGaubier-ComellaPDeburesALasserreEJobetE 2008 Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67 107 124
38. Alvarez-VenegasRPienSSadderMWitmerXGrossniklausU 2003 ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr Biol 13 627 637
39. TamadaYYunJYWooSCAmasinoRM 2009 ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. The Plant Cell 21 3257 3269
40. BerrAXuLGaoJCognatVSteinmetzA 2009 SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. PLANT PHYSIOLOGY 151 1476 1485
41. AichingerEVillarCBFarronaSReyesJCHennigL 2009 CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5 e1000605 doi:10.1371/journal.pgen.1000605
42. CarlesCCFletcherJ 2009 The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes & Development 23 2723 2728
43. ZhangXBernatavichuteYVCokusSPellegriniMJacobsenSE 2009 Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10 R62
44. SalehAAl-AbdallatANdamukongIAlvarez-VenegasRAvramovaZ 2007 The Arabidopsis homologs of trithorax (ATX1) and enhancer of zeste (CLF) establish 'bivalent chromatin marks' at the silent AGAMOUS locus. Nucleic Acids Research 35 6290 6296
45. PienSFleuryDMylneJSCrevillenPInzéD 2008 ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. The Plant Cell 20 580 588
46. AkkersRCvan HeeringenSJJacobiUGJanssen-MegensEMFrançoijsKJ 2009 A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Developmental Cell 17 425 434
47. 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
48. MikkelsenTSKuMJaffeDBIssacBLiebermanE 2007 Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 553 560
49. PanGTianSNieJYangCRuottiV 2007 Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1 299 312
50. ZhaoXDHanXChewJLLiuJChiuKP 2007 Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1 286 298
51. GanQSchonesDEHo EunSWeiGCuiK 2010 Monovalent and unpoised status of most genes in undifferentiated cell-enriched Drosophila testis. Genome Biol 11 R42
52. JeongJHSongHRKoJHJeongYMKwonYESeolJH 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
53. SchlerethAMöllerBLiuWKientzMFlipseJ 2010 MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464 913 916
54. LauSEhrismannJSSchlerethATakadaSMayerU 2010 Cell-cell communication in Arabidopsis early embryogenesis. Eur J Cell Biol 89 225 230
55. AmasinoR 2010 Seasonal and developmental timing of flowering. Plant J 61 1001 1013
56. DennisESPeacockWJ 2007 Epigenetic regulation of flowering. Current Opinion in Plant Biology 10 520 527
57. HendersonIRDeanC 2004 Control of Arabidopsis flowering: the chill before the bloom. Development 131 3829 3838
58. ZhangHOgasJ 2009 An Epigenetic Perspective on Developmental Regulation of Seed Genes. Molecular Plant 2 610 627
59. NorthHBaudSDebeaujonIDubosCDubreucqB 2010 Arabidopsis seed secrets unravelled after a decade of genetic and omics-driven research. Plant J 61 971 981
60. JunkerAHartmannASchreiberFBäumleinH 2010 An engineer's view on regulation of seed development. Trends in plant science
61. HoldsworthMJBentsinkLSoppeWJ 2008 Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179 33 54
62. BentsinkLJowettJHanhartCJKoornneefM 2006 Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci USA 103 17042 17047
63. LiuYKoornneefMSoppeWJ 2007 The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. The Plant Cell 19 433 444
64. Alonso-BlancoCBentsinkLHanhartCJBlankestijn-de VriesHKoornneefM 2003 Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164 711 729
65. Finch-SavageWELeubner-MetzgerG 2006 Seed dormancy and the control of germination. New Phytol 171 501 523
66. ChiangGCBaruaDKramerEMAmasinoRMDonohueK 2009 Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 106 11661 11666
67. MosqunaAKatzADeckerELRensingSAReskiR 2009 Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136 2433 2444
68. OkanoYAonoNHiwatashiYMurataTNishiyamaT 2009 A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc Natl Acad Sci USA 106 16321 16326
69. OhadNMargossianLHsuYCWilliamsCRepettiP 1996 A mutation that allows endosperm development without fertilization. Proc Natl Acad Sci U S A 93 5319 5324
70. IngouffMHaseloffJBergerF 2005 Polycomb group genes control developmental timing of endosperm. Plant J 42 663 674
71. LuoMBilodeauPDennisESPeacockWJChaudhuryA 2000 Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci U S A 97 10637 10642
72. DoyleMRAmasinoRM 2009 A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. PLANT PHYSIOLOGY 151 1688 1697
73. WangDTysonMDJacksonSSYadegariR 2006 Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis. Proc Natl Acad Sci USA 103 13244 13249
74. ArvidssonSKwasniewskiMRiaño-PachónDMMueller-RoeberB 2008 QuantPrime—a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 9 465
75. CroweMLSerizetCThareauVAubourgSRouzéP 2003 CATMA: a complete Arabidopsis GST database. Nucleic Acids Research 31 156 158
76. HilsonPAllemeerschJAltmannTAubourgSAvonA 2004 Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Research 14 2176 2189
77. LurinCAndrésCAubourgSBellaouiMBittonF 2004 Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. The Plant Cell 16 2089 2103
78. GagnotSTambyJPMartin-MagnietteMLBittonFTaconnatL 2008 CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Research 36 D986 90
79. GeXTsutsumiSAburataniHIwataS 2003 Reducing false positives in molecular pattern recognition. Genome informatics International Conference on Genome Informatics 14 34 43
80. Martin-MagnietteMLMary-HuardTBérardCRobinS 2008 ChIPmix: mixture model of regressions for two-color ChIP-chip analysis. Bioinformatics 24 i181 6
81. HulsenTde VliegJAlkemaW 2008 BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9 488
82. van der GraaffELauxTRensingSA 2009 The WUS homeobox-containing (WOX) protein family. Genome Biol 10 248
83. OhadNYadegariRMargossianLHannonMMichaeliD 1999 Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. The Plant Cell 11 407 416
84. IrishVF 2010 The flowering of Arabidopsis flower development. Plant J 61 1014 1028
85. LiuCThongZYuH 2009 Coming into bloom: the specification of floral meristems. Development 136 3379 3391
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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