Histone H2B monoubiquitination facilitates the rapid modulation of gene expression during arabidopsis photomorphogenesis

PLoS Genetics

Volumn 8, Issue 7, 2012, Pages

  Bourbousse, Clara ^a,b,c   Ahmed, Ikhlak ^a,b,c   Roudier, François ^a,b,c   Zabulon, Gérald ^a,b,c   Blondet, Eddy ^d   Balzergue, Sandrine ^d   Colot, Vincent ^a,b,c   Bowler, Chris ^a,b,c   Barneche, Fredy ^a,b,c  

^a PSL RESEARCH UNIVERSITY   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2B; MESSENGER RNA; PROTEIN GIGANTEA; PROTEIN PRR7; PROTEIN TOC1; PROTEIN TZP; TRANSCRIPTOME; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL DIVISION; CHROMATIN; CONTROLLED STUDY; DARKNESS; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE LOCATION; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC REGULATION; GENETIC TRANSCRIPTION; GIGANTEA GENE; HISTONE UBIQUITINATION; ILLUMINATION; LIGHT EXPOSURE; MOLECULAR DYNAMICS; NONHUMAN; OSCILLATION; PHOTOMORPHOGENESIS; PLANT GENE; PLANT GENOME; PLANT RESPONSE; PROTEIN FUNCTION; PRR7 GENE; TOC1 GENE; TZP GENE; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; GENE EXPRESSION REGULATION, PLANT; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LIGHT; MORPHOGENESIS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTIONAL ACTIVATION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84864626950     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002825     Document Type: Article

References (75)

1. Baker M, (2011) Making sense of chromatin states. Nat Methods 8: 717-722.
2. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, et al. (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143: 212-224.
3. Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, et al. (2011) Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 21: 227-236.
4. Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, et al. (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. Embo J 30: 1928-1938.
5. Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, et al. (2011) Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479: 365-371.
6. Moazed D, (2011) Mechanisms for the inheritance of chromatin states. Cell 146: 510-518.
7. Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NC, et al. (2003) Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 17: 2648-2663.
8. Kao CF, Hillyer C, Tsukuda T, Henry K, Berger S, et al. (2004) Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev 18: 184-195.
9. Xiao T, Kao CF, Krogan NJ, Sun ZW, Greenblatt JF, et al. (2005) Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol Cell Biol 25: 637-651.
10. Lang G, Bonnet J, Umlauf D, Karmodiya K, Koffler J, et al. (2011) The Tightly Controlled Deubiquitination Activity of the Human SAGA Complex Differentially Modifies Distinct Gene Regulatory Elements. Mol Cell Biol 31: 3734-3744.
11. Shema E, Tirosh I, Aylon Y, Huang J, Ye C, et al. (2008) The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev 22: 2664-2676.
12. Weake VM, Workman JL, (2011) SAGA function in tissue-specific gene expression. Trends Cell Biol.
13. Fierz B, Chatterjee C, McGinty RK, Bar-Dagan M, Raleigh DP, et al. (2011) Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat Chem Biol 7: 113-119.
14. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, et al. (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
15. Pavri R, Zhu B, Li G, Trojer P, Mandal S, et al. (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125: 703-717.
16. Xin H, Takahata S, Blanksma M, McCullough L, Stillman DJ, et al. (2009) yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35: 365-376.
17. Fleming AB, Kao CF, Hillyer C, Pikaart M, Osley MA, (2008) H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell 31: 57-66.
18. Sun ZW, Allis CD, (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
19. Briggs SD, Xiao T, Sun ZW, Caldwell JA, Shabanowitz J, et al. (2002) Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418: 498.
20. Smith E, Shilatifard A, (2010) The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol Cell 40: 689-701.
21. Weake VM, Workman JL, (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29: 653-663.
22. Lee JS, Smith E, Shilatifard A, (2010) The language of histone crosstalk. Cell 142: 682-685.
23. Grasser KD, (2005) Emerging role for transcript elongation in plant development. Trends Plant Sci 10: 484-490.
24. Crevillen P, Dean C, (2010) Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14: 38-44.
25. Berr A, Shafiq S, Shen WH, (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809: 567-576.
26. Feng S, Jacobsen SE, Reik W, (2011) Epigenetic reprogramming in plant and animal development. Science 330: 622-627.
27. He G, Elling AA, Deng XW, (2011) The epigenome and plant development. Annu Rev Plant Biol 62: 411-435.
28. Fisher AJ, Franklin KA, (2011) Chromatin remodelling in plant light signalling. Physiol Plant 142: 305-313.
29. Chen M, Chory J, (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol.
30. Jiao Y, Lau OS, Deng XW, (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8: 217-230.
31. Kami C, Lorrain S, Hornitschek P, Fankhauser C, (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91: 29-66.
32. Charron JB, He H, Elling AA, Deng XW, (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21: 3732-3748.
33. Benhamed M, Bertrand C, Servet C, Zhou DX, (2006) Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18: 2893-2903.
34. Jang IC, Chung PJ, Hemmes H, Jung C, Chua NH, (2011) Rapid and reversible light-mediated chromatin modifications of Arabidopsis phytochrome A locus. Plant Cell 23: 459-470.
35. Chua YL, Brown AP, Gray JC, (2001) Targeted histone acetylation and altered nuclease accessibility over short regions of the pea plastocyanin gene. Plant Cell 13: 599-612.
36. Bergmuller E, Gehrig PM, Gruissem W, (2007) Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J Proteome Res 6: 3655-3668.
37. Liu Y, Koornneef M, Soppe WJ, (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19: 433-444.
38. Fleury D, Himanen K, Cnops G, Nelissen H, Boccardi TM, et al. (2007) The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19: 417-432.
39. Cao Y, Dai Y, Cui S, Ma L, (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20: 2586-2602.
40. Gu X, Jiang D, Wang Y, Bachmair A, He Y, (2009) Repression of the floral transition via histone H2B monoubiquitination. Plant J 57: 522-533.
41. Xu L, Menard R, Berr A, Fuchs J, Cognat V, et al. (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J 57: 279-288.
42. Peschke F, Kretsch T, (2011) Genome-wide analysis of light-dependent transcript accumulation patterns during early stages of Arabidopsis seedling deetiolation. Plant Physiol 155: 1353-1366.
43. Schroeder DF, Gahrtz M, Maxwell BB, Cook RK, Kan JM, et al. (2002) De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr Biol 12: 1462-1472.
44. Crowe ML, Serizet C, Thareau V, Aubourg S, Rouze P, et al. (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31: 156-158.
45. Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE, (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10: R62.
46. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, et al. (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008: 420747.
47. Wei N, Serino G, Deng XW, (2008) The COP9 signalosome: more than a protease. Trends Biochem Sci 33: 592-600.
48. Chen H, Shen Y, Tang X, Yu L, Wang J, et al. (2006) Arabidopsis CULLIN4 Forms an E3 Ubiquitin Ligase with RBX1 and the CDD Complex in Mediating Light Control of Development. Plant Cell 18: 1991-2004.
49. Dohmann EM, Levesque MP, De Veylder L, Reichardt I, Jurgens G, et al. (2008) The Arabidopsis COP9 signalosome is essential for G2 phase progression and genomic stability. Development 135: 2013-2022.
50. Tamayo P, Slonim D, Mesirov J, Zhu Q, Kitareewan S, et al. (1999) Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. Proc Natl Acad Sci U S A 96: 2907-2912.
51. Chory J, Peto C, Feinbaum R, Pratt L, Ausubel F, (1989) Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58: 991-999.
52. Leivar P, Quail PH, (2010) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16: 19-28.
53. Armstrong GA, Runge S, Frick G, Sperling U, Apel K, (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108: 1505-1517.
54. Shilatifard A, Conaway RC, Conaway JW, (2003) The RNA polymerase II elongation complex. Annu Rev Biochem 72: 693-715.
55. Schmitz RJ, Tamada Y, Doyle MR, Zhang X, Amasino RM, (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.
56. Minsky N, Shema E, Field Y, Schuster M, Segal E, et al. (2008) Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol 10: 483-488.
57. Oh S, Park S, van Nocker S, (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.
58. Ng HH, Robert F, Young RA, Struhl K, (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11: 709-719.
59. Shilatifard A, (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269.
60. Jiang D, Gu X, He Y, (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21: 1733-1746.
61. Jiang D, Kong NC, Gu X, Li Z, He Y, (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7: e1001330 doi:10.1371/journal.pgen.1001330.
62. Dhawan R, Luo H, Foerster AM, Abuqamar S, Du HN, et al. (2009) HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell 21: 1000-1019.
63. Batta K, Zhang Z, Yen K, Goffman DB, Pugh BF, (2011) Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev 25: 2254-2265.
64. Proudfoot NJ, Furger A, Dye MJ, (2002) Integrating mRNA processing with transcription. Cell 108: 501-512.
65. Penheiter KL, Washburn TM, Porter SE, Hoffman MG, Jaehning JA, (2005) A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol Cell 20: 213-223.
66. Perales M, Mas P, (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19: 2111-2123.
67. Li Y, Rosso MG, Viehoever P, Weisshaar B, (2007) GABI-Kat SimpleSearch: an Arabidopsis thaliana T-DNA mutant database with detailed information for confirmed insertions. Nucleic Acids Res 35: D874-878.
68. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
69. Berna G, Robles P, Micol JL, (1999) A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. Genetics 152: 729-742.
70. Fankhauser C, Casal JJ, (2004) Phenotypic characterization of a photomorphogenic mutant. Plant J 39: 747-760.
71. Castells E, Molinier J, Benvenuto G, Bourbousse C, Zabulon G, et al. (2011) The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. Embo J 30: 1162-1172.
72. Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton S, et al. (2004) Genome-wide analysis of Arabidopsis Pentratricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103.
73. Hilson P, Small I, Kuiper MT, (2003) European consortia building integrated resources for Arabidopsis functional genomics. Curr Opin Plant Biol 6: 426-429.
74. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, et al. (2007) NCBI GEO: mining tens of millions of expression profiles-database and tools update. Nucleic Acids Res 35: D760-765.
75. Gagnot S, Tamby JP, Martin-Magniette ML, Bitton F, Taconnat L, et al. (2008) CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res 36: D986-990.