Dynamic Regulation of H3K27 Trimethylation during Differentiation
During growth of multicellular organisms, identities of stem cells and differentiated cells need to be maintained. Cell fate is epigenetically controlled by the conserved Polycomb-group (Pc-G) proteins that repress their target genes by catalyzing histone H3 lysine 27 trimethylation (H3K27me3). Although H3K27me3 is associated with mitotically stable gene repression, a large fraction of H3K27me3 target genes are tissue-specifically activated during differentiation processes. However, in plants it is currently unclear whether H3K27me3 is already present in undifferentiated cells and dynamically regulated to permit tissue-specific gene repression or activation. We used whole-genome tiling arrays to identify the H3K27me3 target genes in undifferentiated cells of the shoot apical meristem and in differentiated leaf cells. Hundreds of genes gain or lose H3K27me3 upon differentiation, demonstrating dynamic regulation of an epigenetic modification in plants. H3K27me3 is correlated with gene repression, and its release preferentially results in tissue-specific gene activation, both during differentiation and in Pc-G mutants. We further reveal meristem- and leaf-specific targeting of individual gene families including known but also likely novel regulators of differentiation and stem cell regulation. Interestingly, H3K27me3 directly represses only specific transcription factor families, but indirectly activates others through H3K27me3-mediated silencing of microRNA genes. Furthermore, H3K27me3 targeting of genes involved in biosynthesis, transport, perception, and signal transduction of the phytohormone auxin demonstrates control of an entire signaling pathway. Based on these and previous analyses, we propose that H3K27me3 is one of the major determinants of tissue-specific expression patterns in plants, which restricts expression of its direct targets and promotes gene expression indirectly by repressing miRNA genes.
Vyšlo v časopise:
Dynamic Regulation of H3K27 Trimethylation during Differentiation. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002040
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002040
Souhrn
During growth of multicellular organisms, identities of stem cells and differentiated cells need to be maintained. Cell fate is epigenetically controlled by the conserved Polycomb-group (Pc-G) proteins that repress their target genes by catalyzing histone H3 lysine 27 trimethylation (H3K27me3). Although H3K27me3 is associated with mitotically stable gene repression, a large fraction of H3K27me3 target genes are tissue-specifically activated during differentiation processes. However, in plants it is currently unclear whether H3K27me3 is already present in undifferentiated cells and dynamically regulated to permit tissue-specific gene repression or activation. We used whole-genome tiling arrays to identify the H3K27me3 target genes in undifferentiated cells of the shoot apical meristem and in differentiated leaf cells. Hundreds of genes gain or lose H3K27me3 upon differentiation, demonstrating dynamic regulation of an epigenetic modification in plants. H3K27me3 is correlated with gene repression, and its release preferentially results in tissue-specific gene activation, both during differentiation and in Pc-G mutants. We further reveal meristem- and leaf-specific targeting of individual gene families including known but also likely novel regulators of differentiation and stem cell regulation. Interestingly, H3K27me3 directly represses only specific transcription factor families, but indirectly activates others through H3K27me3-mediated silencing of microRNA genes. Furthermore, H3K27me3 targeting of genes involved in biosynthesis, transport, perception, and signal transduction of the phytohormone auxin demonstrates control of an entire signaling pathway. Based on these and previous analyses, we propose that H3K27me3 is one of the major determinants of tissue-specific expression patterns in plants, which restricts expression of its direct targets and promotes gene expression indirectly by repressing miRNA genes.
Zdroje
1. BartonMK 2010 Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341 95 113
2. SchuettengruberBChourroutDVervoortMLeblancBCavalliG 2007 Genome regulation by polycomb and trithorax proteins. Cell 128 735 745
3. MullerJVerrijzerP 2009 Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev 19 150 158
4. JohnsonLMollahSGarciaBAMuratoreTLShabanowitzJ 2004 Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32 6511 6518
5. ZhangXClarenzOCokusSBernatavichuteYVPellegriniM 2007 Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5 e129 doi:10.1371/journal.pbio.0050129
6. SchwartzYBKahnTGNixDALiXYBourgonR 2006 Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38 700 705
7. BernsteinBEMikkelsenTSXieXKamalMHuebertDJ 2006 A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125 315 326
8. SchubertDPrimavesiLBishoppARobertsGDoonanJ 2006 Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J 25 4638 4649
9. HansenKHBrackenAPPasiniDDietrichNGehaniSS 2008 A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10 1291 1300
10. MullerJHartCMFrancisNJVargasMLSenguptaA 2002 Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111 197 208
11. CaoRWangLWangHXiaLErdjument-BromageH 2002 Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298 1039 1043
12. CzerminBMelfiRMcCabeDSeitzVImhofA 2002 Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111 185 196
13. KuzmichevANishiokaKErdjument-BromageHTempstPReinbergD 2002 Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16 2893 2905
14. JiangDWangYWangYHeY 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
15. LindrothAMShultisDJasencakovaZFuchsJJohnsonL 2004 Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23 4286 4296
16. SchatlowskiNCreaseyKGoodrichJSchubertD 2008 Keeping plants in shape: Polycomb-group genes and histone methylation. Semin Cell Dev Biol 19 2291 2305
17. KohlerCVillarCB 2008 Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18 236 243
18. ChanvivattanaYBishoppASchubertDStockCMoonYH 2004 Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131 5263 5276
19. SchubertDClarenzOGoodrichJ 2005 Epigenetic control of plant development by Polycomb-group proteins. Curr Opin Plant Biol 8 553 561
20. OhSParkSvanNS 2008 Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet 4 e1000077 doi:10.1371/journal.pgen.1000077
21. 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
22. CharronJBHeHEllingAADengXW 2009 Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21 3732 3748
23. SchuettengruberBGanapathiMLeblancBPortosoMJaschekR 2009 Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol 7 e13 doi:10.1371/journal.pbio.1000013
24. BrackenAPDietrichNPasiniDHansenKHHelinK 2006 Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20 1123 1136
25. BoyerLAPlathKZeitlingerJBrambrinkTMedeirosLA 2006 Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441 349 353
26. LeeTIJennerRGBoyerLAGuentherMGLevineSS 2006 Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125 301 313
27. SquazzoSLO'GeenHKomashkoVMKrigSRJinVX 2006 Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res 16 890 900
28. OktabaKGutierrezLGagneurJGirardotCSenguptaAK 2008 Dynamic regulation by polycomb group protein complexes controls pattern formation and the cell cycle in Drosophila. Dev Cell 15 877 889
29. TolhuisBde WitEMuijrersITeunissenHTalhoutW 2006 Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38 694 699
30. PappBMullerJ 2006 Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20 2041 2054
31. DealRBHenikoffS 2010 A Simple Method for Gene Expression and Chromatin Profiling of Individual Cell Types within a Tissue. Developmental Cell 18 1030 1040
32. MikkelsenTSKuMJaffeDBIssacBLiebermanE 2007 Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 553 560
33. AzuaraVPerryPSauerSSpivakovMJorgensenHF 2006 Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8 532 538
34. LafosMSchubertD 2009 Balance of power—dynamic regulation of chromatin in plant development. Biol Chem 390 1113 1123
35. FletcherJCBrandURunningMPSimonRMeyerowitzEM 1999 Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283 1911 1914
36. ZilbermanDGehringMTranRKBallingerTHenikoffS 2007 Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39 61 69
37. Thibaud-NissenFWuHRichmondTRedmanJCJohnsonC 2006 Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. Plant J 47 152 162
38. SemiartiEUenoYTsukayaHIwakawaHMachidaC 2001 The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128 1771 1783
39. FitzgeraldJNHuiPSBergerF 2009 Polycomb group-dependent imprinting of the actin regulator AtFH5 regulates morphogenesis in Arabidopsis thaliana. Development 136 3399 3404
40. GustafsonAMAllenEGivanSSmithDCarringtonJC 2005 ASRP: the Arabidopsis Small RNA Project Database. Nucleic Acids Res 33 D637 D640
41. ChandlerJW 2009 Local auxin production: a small contribution to a big field. Bioessays 31 60 70
42. ZhaoY 2010 Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61 49 64
43. VannesteSFrimlJ 2009 Auxin: a trigger for change in plant development. Cell 136 1005 1016
44. LiscumEReedJW 2002 Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49 387 400
45. SungSSchmitzRJAmasinoRM 2006 A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 20 3244 3248
46. CalonjeMSanchezRChenLSungZR 2008 EMBRYONIC FLOWER1 participates in polycomb group-mediated AG gene silencing in Arabidopsis. Plant Cell 20 277 291
47. GendallARLevyYYWilsonADeanC 2001 The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107 525 535
48. KatzAOlivaMMosqunaAHakimOOhadN 2004 FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37 707 719
49. XuLShenWH 2008 Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol 18 1966 1971
50. PalatnikJFAllenEWuXSchommerCSchwabR 2003 Control of leaf morphogenesis by microRNAs. Nature 425 257 263
51. 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
52. BaubecTPecinkaARozhonWMittelstenSO 2009 Effective, homogeneous and transient interference with cytosine methylation in plant genomic DNA by zebularine. Plant J 57 542 554
53. WuMFTianQReedJW 2006 Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133 4211 4218
54. NegreNHennetinJSunLVLavrovSBellisM 2006 Chromosomal distribution of PcG proteins during Drosophila development. PLoS Biol 4 e170 doi:10.1371/journal.pbio.0040170
55. JacksonJPJohnsonLJasencakovaZZhangXPerezBurgosL 2004 Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112 308 315
56. JacobYFengSLeBlancCABernatavichuteYVStroudH 2009 ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol 16 763 768
57. GriggSPCanalesCHayATsiantisM 2005 SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437 1022 1026
58. ChellappanPXiaJZhouXGaoSZhangX 2010 siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Res doi 10.1093/nar/gkq590
59. BaoNLyeKWBartonMK 2004 MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7 653 662
60. Jones-RhoadesMWBartelDP 2004 Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14 787 799
61. RhoadesMWReinhartBJLimLPBurgeCBBartelB 2002 Prediction of plant microRNA targets. Cell 110 513 520
62. KuchenSReschWYamaneAKuoNLiZ 2010 Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 32 828 839
63. EnderleDBeiselCStadlerMBGerstungMAthriP 2011 Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res doi:10.1101/gr.114348.110
64. ZhaoY 2008 The role of local biosynthesis of auxin and cytokinin in plant development. Curr Opin Plant Biol 11 16 22
65. ZazimalovaEMurphyASYangHHoyerovaKHosekP 2010 Auxin transporters—why so many? Cold Spring Harb Perspect Biol 2 a001552
66. ParryGCalderon-VillalobosLIPriggeMPeretBDharmasiriS 2009 Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci U S A 106 22540 22545
67. NavarroLDunoyerPJayFArnoldBDharmasiriN 2006 A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312 436 439
68. GodaHSasakiEAkiyamaKMaruyama-NakashitaANakabayashiK 2008 The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55 526 542
69. RizzardiKLandbergKNilssonLLjungKSundås-LarssonA 2010 TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes. Plant J DOI:10.1111/j.1365-313X.2010.04470.x
70. KimSYZhuTSungZR 2010 Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiol 152 516 528
71. SungSAmasinoRM 2004 Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427 159 164
72. BastowRMylneJSListerCLippmanZMartienssenRA 2004 Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427 164 167
73. GentlemanRCCareyVJBatesDMBolstadBDettlingM 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 R80
74. ToedlingJSkylarOKruegerTFischerJJSperlingS 2007 Ringo—an R/Bioconductor package for analyzing ChIP-chip readouts. BMC Bioinformatics 8 221
75. Perez-RodriguezPRiano-PachonDMCorreaLGRensingSAKerstenB 2010 PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38 D822 D827
76. CzechowskiTStittMAltmannTUdvardiMKScheibleWR 2005 Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139 5 17
77. YanDZhangYNiuLYuanYCaoX 2007 Identification and characterization of two closely related histone H4 arginine 3 methyltransferases in Arabidopsis thaliana. Biochem J 408 113 121
78. Colon-CarmonaAYouRHaimovitch-GalTDoernerP 1999 Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20 503 508
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 4
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Survival Motor Neuron Protein Regulates Stem Cell Division, Proliferation, and Differentiation in
- PTG Depletion Removes Lafora Bodies and Rescues the Fatal Epilepsy of Lafora Disease
- Variable Pathogenicity Determines Individual Lifespan in
- An Evolutionary Genomic Approach to Identify Genes Involved in Human Birth Timing