The SWI2/SNF2 Chromatin Remodeler BRAHMA Regulates Polycomb Function during Vegetative Development and Directly Activates the Flowering Repressor Gene

English version České info

In flowering plants, the proper transition from vegetative growth to flowering is critical for their reproductive success and must be controlled precisely. Multiple genes have been shown to regulate the floral transition in response to environmental and endogenous cues. Among them is SHORT VEGETATIVE PHASE (SVP), a key flowering repressor gene in Arabidopsis. SVP is highly expressed during the vegetative phase to promote growth, but the mechanism by which the high expression level of SVP is maintained remains unknown. Here, we report a genome-wide study to examine the functional interplay between the BRM chromatin remodeler and the PcG proteins that catalyze trimethylation of lysine 27 on histone H3 (H3K27me3), a histone mark normally associated with transcriptionally repressed genes. We identify BRM as a direct upstream activator of SVP. BRM acts to keep the levels of H3K27me3 low at the SVP locus by inhibiting the binding and activities of the PcG proteins. Thus, our work identifies a previously unknown mechanism in regulation of flowering time and demonstrates the power of genome-wide approaches in dissecting regulatory networks controlling plant development.

Vyšlo v časopise: The SWI2/SNF2 Chromatin Remodeler BRAHMA Regulates Polycomb Function during Vegetative Development and Directly Activates the Flowering Repressor Gene. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004944
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004944

Souhrn

Zdroje

1. He Y (2012) Chromatin regulation of flowering. Trends Plant Sci 17: 556–562. doi: 10.1016/j.tplants.2012.05.001 22658650

2. Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16: S18–S31. doi: 10.1105/tpc.015958 15037730

3. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time interacting pathways as a basis for diversity. Plant Cell 14: S111–S130. doi: 10.1105/tpc.001362 12045273

4. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13: 627–639. doi: 10.1038/nrg3291 22898651

5. Li D, Liu C, Shen L, Wu Y, Chen H, et al. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15: 110–120. doi: 10.1016/j.devcel.2008.05.002 18606145

6. Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, et al. (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21: 397–402. doi: 10.1101/gad.1518407 17322399

7. Hartmann U, Höhmann S, Nettesheim K, Wisman E, Saedler H, et al. (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21: 351–360.

8. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343–349. doi: 10.1038/nature09784 21248841

9. Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9–22.

10. Simon JA, Kingston RE (2013) Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell 49: 808–824. doi: 10.1016/j.molcel.2013.02.013 23473600

11. Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10: 697–708. doi: 10.1038/nrm2763 19738629

12. Zheng B, Chen X (2011) Dynamics of histone H3 lysine 27 trimethylation in plant development. Curr Opin Plant Biol 14: 123–129. doi: 10.1016/j.pbi.2011.01.001 21330185

13. Bemer M, Grossniklaus U (2012) Dynamic regulation of Polycomb group activity during plant development. Curr Opin Plant Biol 15: 523–529. doi: 10.1016/j.pbi.2012.09.006 22999383

14. Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158: 35–43. doi: 10.1104/pp.111.186445 22086420

15. Köhler C, Hennig L (2010) Regulation of cell identity by plant Polycomb and trithorax group proteins. Curr Opin Genet Dev 20: 541–547. doi: 10.1016/j.gde.2010.04.015 20684877

16. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, et al. (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263–5276. 15456723

17. Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, et al. (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7: e1002014. doi: 10.1371/journal.pgen.1002014 21423668

18. Lafos M, Kroll P, Hohenstatt ML, Thorpe FL, Clarenz O, et al. (2011) Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet 7: e1002040. doi: 10.1371/journal.pgen.1002040 21490956

19. Lu F, Cui X, Zhang S, Jenuwein T, Cao X (2011) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43: 715–719. doi: 10.1038/ng.854 21642989

20. Lodha M, Marco CF, Timmermans MCP (2013) The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev 27: 596–601. doi: 10.1101/gad.211425.112 23468429

21. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273–304. doi: 10.1146/annurev.biochem.77.062706.153223 19355820

22. Saha A, Wittmeyer J, Cairns BR (2006) Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 7: 437–447. 16723979

23. Tamkun JW, Deuring R, Scott MP, Kissinger M, Pattatucci AM, et al. (1992) brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68: 561. 1346755

24. Hargreaves DC, Crabtree GR (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21: 396–420. doi: 10.1038/cr.2011.32 21358755

25. Ho L, Miller EL, Ronan JL, Ho WQ, Jothi R, et al. (2011) esBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating polycomb function. Nat Cell Biol 13: 903–913. doi: 10.1038/ncb2285 21785422

26. Han SK, Sang Y, Rodrigues A, F2010 B, Wu MF, et al. (2012) The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24: 4892–4906. doi: 10.1105/tpc.112.105114 23209114

27. Jerzmanowski A (2007) SWI/SNF chromatin remodeling and linker histones in plants. Biochim Biophys Acta 1769: 330–345. 17292979

28. Hurtado L, Farrona S, Reyes JC (2006) The putative SWI/SNF complex subunit BRAHMA activates flower homeotic genes in Arabidopsis thaliana. Plant Mol Biol 62: 291–304. 16845477

29. Bezhani S, Winter C, Hershman S, Wagner JD, Kennedy JF, et al. (2007) Unique, shared, and redundant roles for the Arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED. Plant Cell 19: 403–416. doi: 10.1105/tpc.106.048272 17293567

30. Archacki R, Buszewicz D, Sarnowski TJ, Sarnowska E, Rolicka AT, et al. (2013) BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in Arabidopsis. PLoS ONE 8: e58588. doi: 10.1371/journal.pone.0058588 23536800

31. Sarnowski TJ, Ríos G, Jásik J, Świeżewski S, Kaczanowski S, et al. (2005) SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles during Arabidopsis development. Plant Cell 17: 2454–2472. doi: 10.1105/tpc.105.031203 16055636

32. Vercruyssen L, Verkest A, Gonzalez N, Heyndrickx KS, Eeckhout D, et al. (2014) ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26: 210–229. doi: 10.1105/tpc.113.115907 24443518

33. Tang X, Hou A, Babu M, Nguyen V, Hurtado L, et al. (2008) The Arabidopsis BRAHMA chromatin-remodeling ATPase is involved in repression of seed maturation genes in leaves. Plant Physiol 147: 1143–1157. doi: 10.1104/pp.108.121996 18508955

34. Wu MF, Sang Y, Bezhani S, Yamaguchi N, Han SK, et al. (2012) SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors. Proc Natl Acad Sci USA 109: 3576–3581. doi: 10.1073/pnas.1113409109 22323601

35. Zhu Y, Rowley MJ, Böhmdorfer G, Wierzbicki AT (2012) A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol Cell 49: 1–12. doi: 10.1016/j.molcel.2012.11.011 23246435

36. Kwon CS, Hibara K, Pfluger J, Bezhani S, Metha H, et al. (2006) A role for chromatin remodeling in regulation of CUC gene expression in the Arabidopsis cotyledon boundary. Development 133: 3223–3230. 16854978

37. Jégu T, Latrasse D, Delarue M, Hirt H, Domenichini S, et al. (2014) The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26: 538–551. doi: 10.1105/tpc.113.114454 24510722

38. Sarnowska EA, Rolicka AT, Bucior E, Cwiek P, Tohge T, et al. (2013) DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiol 163: 305–317. doi: 10.1104/pp.113.223933 23893173

39. Farrona S, Hurtado L, Bowman JL, Reyes JC (2004) The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering. Development 131: 4965–4975. 15371304

40. Farrona S, Hurtado L, March-Díaz R, Schmitz RJ, Florencio FJ, et al. (2011) Brahma is required for proper expression of the floral repressor FLC in Arabidopsis. PLoS One 6: e17997. doi: 10.1371/journal.pone.0017997 21445315

41. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448–3449. 15972284

42. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, et al. (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44–51. 9052779

43. Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, et al. (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J 25: 4638–4649. doi: 10.1038/sj.emboj.7601311 16957776

44. Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, et al. (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 17542647

45. Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, et al. (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14: 869–871. 17676062

46. Larsson AS, Landberg K, Meeks-Wagner DR (1998) The TERMINAL FLOWER2 (TFL2) gene controls the reproductive transition and meristem identity in Arabidopsis thaliana. Genetics 149: 597–605. 9611176

47. Smaczniak C, Immink RGH, Muiño JM, Blanvillain R, Busscher M, et al. (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA 109: 1560–1565. doi: 10.1073/pnas.1112871109 22238427

48. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273–277. 1359429

49. Benlloch R, Berbel A, Serrano-Mislata A, Madueño F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot 100: 659–676. doi: 10.1093/aob/mcm146 17679690

50. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501–506. 15806101

51. Mizukami Y, Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71: 119–131. 1356630

52. Gregis V, Sessa A, Colombo L, Kater MM (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18: 1373–1382. doi: 10.1105/tpc.106.041798 16679456

53. Alvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, et al. (2003) ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr Biol 13: 627–637. 12699618

54. Carles CC, Fletcher JC (2009) The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev 23: 2723–2728. doi: 10.1101/gad.1812609 19952107

55. Aichinger E, Villar CBR, Farrona S, Reyes JC, Hennig L, et al. (2009) CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5: e1000605. doi: 10.1371/journal.pgen.1000605 19680533

56. Shao Z, Raible F, Mollaaghababa R, Guyon JR, Wu C, et al. (1999) Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98: 37–46. 10412979

57. Kia SK, Gorski MM, Giannakopoulos S, Verrijzer CP (2008) SWI/SNF mediates polycomb eviction and epigenetic reprogramming of the INK4b-ARF-INK4a locus. Mol Cell Biol 28: 3457–3464. doi: 10.1128/MCB.02019-07 18332116

58. Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME, et al. (2010) Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18: 316–328. doi: 10.1016/j.ccr.2010.09.006 20951942

59. Sun B, Looi L-S, Guo S, He Z, Gan E-S, et al. (2014) Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells. Science 343: 1248559. doi: 10.1126/science.1248559 24482483

60. Grunewald W, De Smet I, Lewis DR, Löfke C, Jansen L, et al. (2012) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci USA 109: 1554–1559. doi: 10.1073/pnas.1121134109 22307611

61. Helliwell CA, Wood CC, Robertson M, James Peacock W, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high—molecular—weight protein complex. Plant J 46: 183–192. 16623882

62. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, et al. (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13: 1768–1774. 14561401

63. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, et al. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709–713. 11395776

64. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, et al. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23: 3356–3364. doi: 10.1038/sj.emboj.7600340 15282547

65. Tang X, Bian S, Tang M, Lu Q, Li S, et al. (2012) MicroRNA-mediated repression of the seed maturation program during vegetative development in Arabidopsis. PLoS Genet 8: e1003091. doi: 10.1371/journal.pgen.1003091 23209442

66. Lu Q, Tang X, Tian G, Wang F, Liu K, et al. (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61: 259–270. doi: 10.1111/j.1365-313X.2009.04048.x 19843313

67. Schönrock N, Bouveret R, Leroy O, Borghi L, Köhler C, et al. (2006) Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev 20: 1667–1678. doi: 10.1101/gad.377206 16778081

68. Wang D, Tyson MD, Jackson SS, Yadegari R (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. doi: 10.1073/pnas.0605551103 16924116

69. Masiero S, Li MA, Will I, Hartmann U, Saedler H, et al. (2004) INCOMPOSITA: a MADS-box gene controlling prophyll development and floral meristem identity in Antirrhinum. Development 131: 5981–5990. 15539492

70. Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2: 213–218. 16163802

71. Li C, Wu K, Fu G, Li Y, Zhong Y, et al. (2009) Regulation of oleosin expression in developing peanut (Arachis hypogaea L.) embryos through nucleosome loss and histone modifications. J Exp Bot 60: 4371–4382. doi: 10.1093/jxb/erp275 19737778

72. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174

73. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, et al. (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40: D1202–D1210. doi: 10.1093/nar/gkr1090 22140109

74. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137. doi: 10.1186/gb-2008-9-9-r137 18798982

75. Nicol JW, Helt GA, Blanchard SG Jr, Raja A, Loraine AE (2009) The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25: 2730–2731. doi: 10.1093/bioinformatics/btp472 19654113

76. Zang C, Schones DE, Zeng C, Cui K, Zhao K, et al. (2009) A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25: 1952–1958. doi: 10.1093/bioinformatics/btp340 19505939

77. Xu H, Wei CL, Lin F, Sung WK (2008) An HMM approach to genome-wide identification of differential histone modification sites from ChIP-seq data. Bioinformatics 24: 2344–2349. doi: 10.1093/bioinformatics/btn402 18667444

78. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469. doi: 10.1104/pp.103.027979 14555774

79. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10069079

80. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121–1133. doi: 10.1105/tpc.105.039834 16531494