Mechanisms of signaling crosstalk between brassinosteroids and gibberellins

Plant Signaling and Behavior

Volumn 8, Issue 7, 2013, Pages

  Li, Qian Feng ^a   He, Jun Xian ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

BRASSINAZOLE RESISTANT 1; Brassinosteroids; BRI1 EMS SUPPRESSOR 1; DELLAs; Gibberellins; Growth and development; Signaling crosstalk

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINOSTEROID; BZR1 PROTEIN, ARABIDOPSIS; GAI PROTEIN, ARABIDOPSIS; GIBBERELLIN; NUCLEAR PROTEIN;

ARABIDOPSIS; BRASSINAZOLE- RESISTANT 1; BRI1-EMS-SUPPRESSOR 1; CELL ENLARGEMENT; DELLAS; FLOWER; GENE EXPRESSION REGULATION; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT GENE; REVIEW; SEEDLING; SIGNAL TRANSDUCTION; SIGNALING CROSSTALK;

BRASSINAZOLE- RESISTANT 1; BRASSINOSTEROIDS; BRI1-EMS-SUPPRESSOR 1; DELLAS; GIBBERELLINS; GROWTH AND DEVELOPMENT; SIGNALING CROSSTALK;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; CELL ENLARGEMENT; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GERMINATION; GIBBERELLINS; NUCLEAR PROTEINS; RECEPTOR CROSS-TALK; SEEDLING; SIGNAL TRANSDUCTION;

EID: 84879711013     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.24686     Document Type: Review

References (82)

1. Vert G, Chory J. Crosstalk in cellular signaling: back-ground noise or the real thing? Dev Cell 2011; 21:985-91; http://dx.doi.org/10.1016/j.devcel.2011.11.006.
2. Clouse SD. Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 2011; 23:1219-30; http://dx.doi.org/10.1105/tpc.111.084475
3. Wang ZY, Bai MY, Oh E, Zhu JY. Brassinosteroid signaling network and regulation of photomor-phogenesis. Annu Rev Genet 2012; 46:701-24; http://dx.doi.org/10.1146/annurev-genet-102209-163450
4. Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M. Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 2007; 58:183-98; http://dx.doi.org/10.1146/annurev.arplant.58.032806.103830
5. Sun TP. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 2011; 21:R338-45; http://dx.doi.org/10.1016/j.cub.2011.02.036
6. Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS. Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expan-sion. Plant Cell 2011; 23:1322-36; http://dx.doi.org/10.1105/tpc.111.084020
7. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 2012; 14:810-7; http://dx.doi.org/10.1038/ncb2546
8. Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, et al. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 2012; 109:13446-51; http://dx.doi.org/10.1073/pnas.1119992109
9. Li QF, Wang C, Jiang L, Li S, Sun SS, He JX. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 2012; 5:ra72; http://dx.doi.org/10.1126/scisig-nal.2002908
10. Li J, Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 1997; 90:929-38; http://dx.doi.org/10.1016/S0092-8674(00)80357-8
11. Li J, Nam KH. Regulation of brassinosteroid signal-ing by a GSK3/SHAGGY-like kinase. Science 2002; 295:1299-301;
12. Nam KH, Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 2002; 110:203-12; http://dx.doi.org/10.1016/S0092-8674(02)00814-0
13. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, et al. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 2008; 15:220-35; http://dx.doi.org/10.1016/j.dev-cel.2008.06.011
14. Wang X, Chory J. Brassinosteroids regulate dissocia-tion of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 2006; 313:1118-22; http://dx.doi.org/10.1126/sci-ence.1127593
15. Oh MH, Wang X, Kota U, Goshe MB, Clouse SD, Huber SC. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassino-steroid signaling in Arabidopsis. Proc Natl Acad Sci USA 2009; 106:658-63; http://dx.doi.org/10.1073/pnas.0810249106
16. Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, Zhu S, et al. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 2008; 321:557-60; http://dx.doi.org/10.1126/science.1156973
17. Kim TW, Guan S, Burlingame AL, Wang ZY. The CDG1 kinase mediates brassinosteroid signal transduc-tion from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol Cell 2011; 43:561-71; http://dx.doi.org/10.1016/j.molcel.2011.05.037
18. Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang JX, et al. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 2009; 11:1254-60; http://dx.doi.org/10.1038/ncb1970
19. He JX, Gendron JM, Yang Y, Li J, Wang ZY. The GSK3-like kinase BIN2 phosphorylates and destabi-lizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci USA 2002; 99:10185-90; http://dx.doi.org/10.1073/pnas.152342599
20. Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 2002; 109:181-91; http://dx.doi.org/10.1016/S0092-8674(02)00721-3
21. Peng P, Zhao J, Zhu Y, Asami T, Li J. A direct docking mechanism for a plant GSK3-like kinase to phos-phorylate its substrates. J Biol Chem 2010; 285:24646-53; http://dx.doi.org/10.1074/jbc.M110.142547
22. Kim TW, Wang ZY. Brassinosteroid signal trans-duction from receptor kinases to transcription factors. Annu Rev Plant Biol 2010; 61:681-704; http://dx.doi.org/10.1146/annurev.arplant.043008.092057
23. Vert G, Chory J. Downstream nuclear events in brassinosteroid signalling. Nature 2006; 441:96-100; http://dx.doi.org/10.1038/nature04681
24. Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, et al. Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 2007; 104:13839-44; http://dx.doi.org/10.1073/pnas.0706386104
25. Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, et al. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 2007; 13:177-89; http://dx.doi.org/10.1016/j.devcel.2007.06.009
26. Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, et al. PP2A activates brassinosteroid-respon-sive gene expression and plant growth by dephos-phorylating BZR1. Nat Cell Biol 2011; 13:124-31; http://dx.doi.org/10.1038/ncb2151
27. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, et al. BZR1 is a transcriptional repres-sor with dual roles in brassinosteroid homeostasis and growth responses. Science 2005; 307:1634-8; http://dx.doi.org/10.1126/sci-ence.1107580
28. Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. A new class of transcription factors mediates brassino-steroid-regulated gene expression in Arabidopsis. Cell 2005; 120:249-59; http://dx.doi.org/10.1016/j.cell.2004.11.044
29. Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, et al. Integration of brassinosteroid signal transduc-tion with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 2010; 19:765-77; http://dx.doi.org/10.1016/j.dev-cel.2010.10.010
30. Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 2011; 65:634-46; http://dx.doi.org/10.1111/j.1365-313X.2010.04449.x
31. Sun TP. Gibberellin-GID1-DELLA: a pivotal regula-tory module for plant growth and development. Plant Physiol 2010; 154:567-70; http://dx.doi.org/10.1104/pp.110.161554
32. Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, et al. Genetic characterization and functional analysis of the GID1 gibberellin recep-tors in Arabidopsis. Plant Cell 2006; 18:3399-414; http://dx.doi.org/10.1105/tpc.106.047415
33. Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A, et al. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 2007; 19:1209-20; http://dx.doi.org/10.1105/tpc.107.051441
34. Hirano K, Ueguchi-Tanaka M, Matsuoka M. GID1-mediated gibberellin signaling in plants. Trends Plant Sci 2008; 13:192-9; http://dx.doi.org/10.1016/j.tplants.2008.02.005
35. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, et al. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 2003; 15:1120-30; http://dx.doi.org/10.1105/tpc.010827
36. Dill A, Thomas SG, Hu J, Steber CM, Sun TP. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degrada-tion. Plant Cell 2004; 16:1392-405; http://dx.doi.org/10.1105/tpc.020958
37. Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M. The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 2002; 14:57-70; http://dx.doi.org/10.1105/tpc.010319
38. Depuydt S, Hardtke CS. Hormone signalling crosstalk in plant growth regulation. Curr Biol 2011; 21:R365-73; http://dx.doi.org/10.1016/j.cub.2011.03.013
39. Gregory LE, Mandava NB. The activity and interaction of brassinolide and gibberellic acid in mung bean epi-cotyls. Physiol Plant 1982; 54:239-43; http://dx.doi.org/10.1111/j.1399-3054.1982.tb00253.x
40. Katsumi M. Interaction of a brassinosteroid with IAA and GA3 in the elongation of cucumber hypocotyl sec-tions. Plant Cell Physiol 1985; 26:615-25
41. Müssig C, Shin GH, Altmann T. Brassinosteroids promote root growth in Arabidopsis. Plant Physiol 2003; 133:1261-71; http://dx.doi.org/10.1104/pp.103.028662
42. Tanaka K, Nakamura Y, Asami T, Yoshida S, Matsuo T, Okamoto S. Physiological roles of brassinosteroids in early growth of Arabidopsis: brassinosteroids have a synergistic relationship with gibberellin as well as auxin in light-grown hypocotyl elongation. J Plant Growth Regul 2003; 22:259-71; http://dx.doi.org/10.1007/s00344-003-0119-3
43. Leubner-Metzger G. Brassinosteroids and gibberellins promote tobacco seed germination by distinct path-ways. Planta 2001; 213:758-63; http://dx.doi.org/10.1007/s004250100542
44. Steber CM, McCourt P. A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 2001; 125:763-9; http://dx.doi.org/10.1104/pp.125.2.763
45. Ullah H, Chen JG, Wang S, Jones AM. Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 2002; 129:897-907; http://dx.doi.org/10.1104/pp.005017
46. Chen JG, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, et al. GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 2004; 135:907-15; http://dx.doi.org/10.1104/pp.104.038992
47. Colucci G, Apone F, Alyeshmerni N, Chalmers D, Chrispeels MJ. GCR1, the putative Arabidopsis G protein-coupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering. Proc Natl Acad Sci USA 2002; 99:4736-41; http://dx.doi.org/10.1073/pnas.072087699
48. Wilson RN, Heckman JW, Somerville CR. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 1992; 100:403-8; http://dx.doi.org/10.1104/pp.100.1.403
49. Huang S, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM. Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiol 1998; 118:773-81; http://dx.doi.org/10.1104/pp.118.3.773
50. Chory J, Nagpal P, Peto CA. Phenotypic and genetic analysis of det2, a new mutant that affects light-regu-lated seedling development in Arabidopsis. Plant Cell 1991; 3:445-59;
51. Azpiroz R, Wu Y, LoCascio JC, Feldmann KA. An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 1998; 10:219-30;
52. Sun T, Goodman HM, Ausubel FM. Cloning the Arabidopsis GA1 Locus by Genomic Subtraction. Plant Cell 1992; 4:119-28;
53. Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, et al. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 1996; 85:171-82; http://dx.doi.org/10.1016/S0092-8674(00)81094-6
54. Domagalska MA, Sarnowska E, Nagy F, Davis SJ. Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS ONE 2010; 5:e14012; http://dx.doi.org/10.1371/journal.pone.0014012
55. Nadhzimov UK, Jupe SC, Jones MG, Scott IM. Growth and gibberellin relations of the extreme dwarf dx tomato mutant. Physiol Plant 1988; 73:252-6; http://dx.doi.org/10.1111/j.1399-3054.1988.tb00594.x
56. Jager CE, Symons GM, Ross JJ, Smith JJ, Reid JB. The brassinosteroid growth response in pea is not mediated by changes in gibberellin content. Planta 2005; 221:141-8; http://dx.doi.org/10.1007/s00425-004-1454-8
57. Kurepin LV, Joo SH, Kim SK, Pharis RP, Back TG. Interaction of brassinosteroids with light quality and plant hormones in regulating shoot growth of young sunflower and Arabidopsis seedlings. J Plant Growth Regul 2012; 31:156-64; http://dx.doi.org/10.1007/s00344-011-9227-7
58. Shimada A, Ueguchi-Tanaka M, Sakamoto T, Fujioka S, Takatsuto S, Yoshida S, et al. The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1 and modulating brassinosteroid synthesis. Plant J 2006; 48:390-402; http://dx.doi.org/10.1111/j.1365-313X.2006.02875.x
59. Wang L, Wang Z, Xu Y, Joo SH, Kim SK, Xue Z, et al. OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J 2009; 57:498-510; http://dx.doi.org/10.1111/j.1365-313X.2008.03707.x
60. De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi IR, et al. Brassinosteroids antagonize gibberellin-and salicylate-mediated root immunity in rice. Plant Physiol 2012; 158:1833-46; http://dx.doi.org/10.1104/pp.112.193672
61. Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 2003; 33:887-98; http://dx.doi.org/10.1046/j.1365-313X.2003.01675.x
62. Bajguz A, Hayat S. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 2009; 47:1-8; http://dx.doi.org/10.1016/j.plaphy.2008.10.002
63. Hu MY, Luo M, Xiao YH, Li XB, Tan KL, Hou L, et al. Brassinosteroids and Auxin Down-Regulate DELLA Genes in Fiber Initiation and Elongation of Cotton. Agric Sci China 2011; 10:1168-76
64. Schünmann PH, Ougham HJ. Identification of three cDNA clones expressed in the leaf extension zone and with altered patterns of expression in the slender mutant of barley: a tonoplast intrinsic protein, a putative struc-tural protein and protochlorophyllide oxidoreductase. Plant Mol Biol 1996; 31:529-37; http://dx.doi.org/10.1007/BF00042226
65. Medford JI, Elmer JS, Klee HJ. Molecular cloning and characterization of genes expressed in shoot apical meristems. Plant Cell 1991; 3:359-70;
66. Bouquin T, Meier C, Foster R, Nielsen ME, Mundy J. Control of specific gene expression by gibberellin and brassinosteroid. Plant Physiol 2001; 127:450-8; http://dx.doi.org/10.1104/pp.010173
67. Yang G, Komatsu S. Molecular cloning and character-ization of a novel brassinolide enhanced gene OsBLE1 in Oryza sativa seedlings. Plant Physiol Biochem 2004; 42:1-6; http://dx.doi.org/10.1016/j.plaphy.2003.10.001
68. Nemhauser JL, Hong F, Chory J. Different plant hormones regulate similar processes through large-ly nonoverlapping transcriptional responses. Cell 2006; 126:467-75; http://dx.doi.org/10.1016/j.cell.2006.05.050
69. Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, et al. Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 2007; 19:3037-57; http://dx.doi.org/10.1105/tpc.107.054999
70. Vert G, Walcher CL, Chory J, Nemhauser JL. Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci USA 2008; 105:9829-34; http://dx.doi.org/10.1073/pnas.0803996105
71. Cheminant S, Wild M, Bouvier F, Pelletier S, Renou JP, Erhardt M, et al. DELLAs regulate chlorophyll and carotenoid biosynthesis to prevent photooxidative dam-age during seedling deetiolation in Arabidopsis. Plant Cell 2011; 23:1849-60; http://dx.doi.org/10.1105/tpc.111.085233
72. Yu X, Li L, Li L, Guo M, Chory J, Yin Y. Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 2008; 105:7618-23; http://dx.doi.org/10.1073/pnas.0802254105
73. Li L, Yu X, Thompson A, Guo M, Yoshida S, Asami T, et al. Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J 2009; 58:275-86; http://dx.doi.org/10.1111/j.1365-313X.2008.03778.x
74. Li L, Ye H, Guo H, Yin Y. Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci USA 2010; 107:3918-23; http://dx.doi.org/10.1073/pnas.0909198107
75. Oh E, Zhu JY, Wang ZY. Interaction between BZR1 and PIF4 integrates brassinosteroid and environ-mental responses. Nat Cell Biol 2012; 14:802-9; http://dx.doi.org/10.1038/ncb2545
76. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 2008; 451:475-9; http://dx.doi.org/10.1038/nature06448
77. de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, et al. A molecular framework for light and gibberellin control of cell elon-gation. Nature 2008; 451:480-4; http://dx.doi.org/10.1038/nature06520
78. Hou X, Lee LY, Xia K, Yan Y, Yu H. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 2010; 19:884-94; http://dx.doi.org/10.1016/j.devcel.2010.10.024
79. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, et al. Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev 2010; 24:2127-32; http://dx.doi.org/10.1101/gad.593410
80. Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu J, Heo JO, et al. Scarecrow-like 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci USA 2011; 108:2160-5; http://dx.doi.org/10.1073/pnas.1012232108
81. An F, Zhang X, Zhu Z, Ji Y, He W, Jiang Z, et al. Coordinated regulation of apical hook development by gibberellins and ethylene in etiolated Arabidopsis seed-lings. Cell Res 2012; 22:915-27; http://dx.doi.org/10.1038/cr.2012.29
82. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 2012; 24:2635-48; http://dx.doi.org/10.1105/tpc.112.098749