Histone H2B monoubiquitination is required to reach maximal transcript levels of circadian clock genes in Arabidopsis

Plant Journal

Volumn 72, Issue 2, 2012, Pages 249-260

  Himanen, Kristiina ^a,b,d   Woloszynska, Magdalena ^a,b   Boccardi, Tommaso M ^a,b   De Groeve, Steven ^a,b   Nelissen, Hilde ^a,b   Bruno, Leonardo ^c   Vuylsteke, Marnik ^a,b   Van Lijsebettens, Mieke ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF CALABRIA   (Italy)

^d Department of Agricultural Sciences ^*  (Finland)

Author keywords

Arabidopsis; chromatin; circadian clock; histone H2B monoubiquitination; histone H3K4 trimethylation; transcriptional elongation

Indexed keywords

ARABIDOPSIS; CHROMATIN; CIRCADIAN CLOCK; HISTONE H2B MONOUBIQUITINATION; TRIMETHYLATION;

ACETYLATION; CLOCKS; GENE EXPRESSION;

PROTEINS;

ARABIDOPSIS PROTEIN; ELO3 PROTEIN, ARABIDOPSIS; HISTONE; HISTONE ACETYLTRANSFERASE; HUB1 PROTEIN, ARABIDOPSIS; MESSENGER RNA; PLANT RNA; UBIQUITIN PROTEIN LIGASE;

ACETYLATION; ARABIDOPSIS; ARTICLE; CHROMATIN; CIRCADIAN RHYTHM; FLOWER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROARRAY ANALYSIS; MUTATION; OPEN READING FRAME; PHYSIOLOGY; PLANT LEAF; PRENATAL DEVELOPMENT; SEEDLING; TIME; TRANSCRIPTION INITIATION; TRANSGENIC PLANT; UBIQUITINATION;

ACETYLATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; CIRCADIAN CLOCKS; FLOWERS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HISTONE ACETYLTRANSFERASES; HISTONES; MICROARRAY ANALYSIS; MUTATION; OPEN READING FRAMES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; RNA, MESSENGER; RNA, PLANT; SEEDLING; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

ARABIDOPSIS;

EID: 84867571063     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05071.x     Document Type: Article

References (43)

1. Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A.V., Tariq, M., and, Paszkowski, J., (2004) Chromatin techniques for plant cells. Plant J. 39, 776-789 (Pubitemid 39218784)
2. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R., and, Görlach, J., (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell, 13, 1499-1510. (Pubitemid 32675716)
3. Bruno, L., Muto, A., Spadafora, N.D., Iaria, D., Chiappetta, A., Van Lijsebettens, M., and, Bitonti, M.B., (2011) Multi-probe in situ hybridization to whole mount Arabidopsis seedlings. Int. J. Dev. Biol. 55, 197-203.
4. Cao, Y., Dai, Y., Cui, S., and, Ma, L., (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell, 20, 2586-2602. (Pubitemid 352844578)
5. Cazzonelli, C.I., Millar, T., Finnegan, E.J., and, Pogson, B.J., (2009) Promoting gene expression in plants by permissive histone lysine methylation. Plant Signal. Behav. 4, 484-488.
6. Dhawan, R., Luo, H., Foerster, A.M., AbuQamar, S., Du, H.-N., Briggs, S.D., Mittelsten Scheid, O., and, Mengiste, T., (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.
7. Dodd, A.N., Salathia, N., Hall, A., Kévei, E., Tõth, R., Nagy, F., Hibberd, J.M., Millar, A.J., and, Webb, A.A.R., (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309, 630-633. (Pubitemid 41033650)
8. Doyle, M.R., Davis, S.J., Bastow, R.M., McWatters, H.G., Kozma-Bognár, L., Nagy, F., Millar, A.J., and, Amasino, R.M., (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature, 419, 74-77. (Pubitemid 34987872)
9. Fleury, D., Himanen, K., Cnops, G., 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. (Pubitemid 46941668)
10. Gu, X., Jiang, D., Wang, Y., Bachmair, A., and, He, Y., (2009) Repression of the floral transition via histone H2B monoubiquitination. Plant J. 57, 522-533.
11. Gutteridge, S., and, Gatenby, A.A., (1995) Rubisco synthesis, assembly, mechanism, and regulation. Plant Cell, 7, 809-819.
12. Haring, M., Offerman, S., Danker, T., Horst, I., Peterhansel, C., and, Stam, M., (2007) Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods, 3, 11.1-11.16.
13. Hejátko, J., Blilou, I., Brewer, P.B., Friml, J., Scheres, B., and, Benková, E., (2006) In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nat. Protoc. 4, 1939-1946. (Pubitemid 46773315)
14. Hwang, W.W., Venkatasubrahmanyam, S., Ianculescu, A.G., Tong, A., Boone, C., and, Madhani, H.D., (2003) A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol. Cell, 11, 261-266. (Pubitemid 36126606)
15. Khanna, R., Kikis, E.A., and, Quail, P.H., (2003) EARLY FLOWERING 4 functions in phytochrome B-regulated seedling de-etiolation. Plant Physiol. 133, 1530-1538. (Pubitemid 38047285)
16. Kreps, J.A., and, Kay, S.A., (1997) Coordination of plant metabolism and development by the circadian clock. Plant Cell, 9, 1235-1244. (Pubitemid 28181069)
17. Laribee, R.N., Fuchs, S.M., and, Strahl, B.D., (2007) H2B ubiquitylation in transcriptional control: a FACT-finding mission. Genes Dev. 21, 737-743. (Pubitemid 46572353)
18. Liu, Y., Koornneef, M., and, Soppe, W.J.J., (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. (Pubitemid 46941669)
19. Lolas, I.B., Himanen, K., Grønlund, J.T., Lynggaard, C., Houben, A., Melzer, M., Van Lijsebettens, M., and, Grasser, K.D., (2010) The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. Plant J. 61, 686-697.
20. Maere, S., Heymans, K., and, Kuiper, M., (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics, 21, 3448-3449. (Pubitemid 41222459)
21. McWatters, H.G., Kolmos, E., Hall, A., Doyle, M.R., Amasino, R.M., Guyla, P., Nagy, F., Millar, A.J., and, Davis, S.J., (2007) ELF4 is required for oscillatory properties of the circadian clock. Plant Physiol. 144, 391-401. (Pubitemid 46941642)
22. Minsky, N., Shema, E., Field, Y., Schuster, M., Segal, E., and, Oren, M., (2008) Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat. Cell Biol. 10, 483-488.
23. Nakanishi, S., Lee, J.S., Gardner, K.E., et al. (2009) Histone H2BK123 monoubiquitination is the critical determinant for H3K4 and H3K79 trimethylation by COMPASS and Dot1. J. Cell Biol. 186, 371-377.
24. Neff, M., Turk, E., and, Kalishman, M., (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 18, 613-615. (Pubitemid 35346679)
25. Nelissen, H., Fleury, D., Bruno, L., Robles, P., De Veylder, L., Traas, J., Micol, J.L., Van Montagu, M., Inzé, D., and, Van Lijsebettens, M., (2005) The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc. Natl Acad. Sci. USA, 102, 7754-7759. (Pubitemid 40744244)
26. Nelissen, H., Boccardi, T.M., Himanen, K., and, Van Lijsebettens, M., (2007) Impact of core histone modifications on transcriptional regulation and plant growth. Crit. Rev. Plant Sci. 26, 243-263. (Pubitemid 350034842)
27. Nelissen, H., De Groeve, S., Fleury, D., et al. (2010) Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. Proc. Natl Acad. Sci. USA, 107, 1678-1683.
28. Ni, Z., Kim, E.-D., Ha, M., Lackey, E., Liu, J., Zhang, Y., Sun, Q., and, Chen, Z.J., (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature, 457, 327-331.
29. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A., and, Reinberg, D., (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell, 125, 703-717. (Pubitemid 43732350)
30. Payne, R.W., (2010) GenStat Release 13 Reference Manual, Part 3 Procedure Library PL21. Hemel Hempstead, UK: VSN International.
31. Penfield, S., and, Hall, A., (2009) A role for multiple circadian clock genes in the response to signals that break seed dormancy in Arabidopsis. Plant Cell, 21, 1722-1732.
32. Perales, M., and, Más, P., (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell, 19, 2111-2123. (Pubitemid 47347456)
33. Roden, L.C., and, Ingle, R.A., (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell, 21, 2546-2552.
34. Schmitz, R.J., Tamada, Y., Doyle, M.R., Xiaoyu, Z., and, Amasino, R.M., (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.
35. Spencer, M., Casson, S., and, Lindsey, K., (2007) Transcriptional profiling of the Arabidopsis embryo. Plant Physiol. 143, 924-940. (Pubitemid 46940989)
36. Sridhar, V.V., Kapoor, A., Zhang, K., Zhu, J., Zhou, T., Hasegawa, P.M., Bressan, R.A., and, Zhu, J.-K., (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature, 447, 735-738. (Pubitemid 46889731)
37. Tanny, J.C., Erdjument-Bromage, H., Tempst, P., and, Allis, C.D., (2007) Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev. 21, 835-847. (Pubitemid 46572362)
38. Valvekens, D., Van Montagu, M., and, Van Lijsebettens, M., (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl Acad. Sci. USA, 85, 5536-5540.
39. Van Lijsebettens, M., and, Grasser, K., (2010) The role of the transcript elongation factors FACT and HUB1 in leaf growth and the induction of flowering. Plant Signal. Behav. 5, 715-717.
40. Vethantham, V., Yang, Y., Bowman, C., Asp, P., Lee, J.-H., Skalnik, D.G., and, Dynlacht, B.D., (2012) Dynamic loss of H2B ubiquitylation without corresponding changes in H3K4 tri-methylation during myogenic differentiation. Mol. Cell. Biol. 32, 1044-1055.
41. Vlieghe, K., Vuylsteke, M., Florquin, K., Rombauts, S., Maes, S., Ormenese, S., Van Hummelen, P., Van de Peer, Y., Inzé, D., and, De Veylder, L., (2003) Microarray analysis of E2Fa-DPa-overexpressing plants uncovers a cross-talking genetic network between DNA replication and nitrogen assimilation. J. Cell Sci. 116, 4249-4259. (Pubitemid 37337097)
42. Xiao, T., Kao, C.-F., Krogan, N.J., Sun, Z.-W., Greenblatt, J.F., Osley, M.A., and, Strahl, B.D., (2005) Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol. Cell. Biol. 25, 637-651. (Pubitemid 40096585)
43. Xu, L., Ménard, R., Berr, A., Fuchs, J., Cognat, V., Meyer, D., and, Shen, W.-H., (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.