Browse > Article
http://dx.doi.org/10.5352/JLS.2012.22.3.428

Update on Phosphorylation-Mediated Brassinosteroid Signaling Pathways  

Lee, Yew (Division of Biological Science and Technology, Yonsei University)
Kim, Soo-Hwan (Division of Biological Science and Technology, Yonsei University)
Publication Information
Journal of Life Science / v.22, no.3, 2012 , pp. 428-436 More about this Journal
Abstract
Protein phosphorylation is a universal mechanism that regulates cellular activities. The brassinosteroid (BR) signal transduction pathway is a relay of phosphorylation and dephosphorylation cascades. It starts with the BR-induced activation of the membrane receptor kinase brassinosteroid insensitive 1 (BRI1), resulting in the dephosphorylation of transcription factors such as BZR1/BES2 and BZR2/BES1 followed by BR-induced gene expression. Brassinosteroid signal transduction research has progressed rapidly by identifying the phosphorylation/dephosphorylation site(s) of the BR-regulated kinase and phosphatase substrates with a simultaneous pursuit of mutant phenotypes. Autophosphorylation, transphosphorylation, and serine/threonine and tyrosine phosphorylation of the receptor protein kinases BRI1 and BRI1-associated kinase (BAK1) have increased the understanding of the regulatory role of those kinases during physiological and developmental processes in plants. The phosphorylation event initiated by BR is also found in the regulation of receptor-mediated endocytosis and the subsequent degradation of the receptor. However, the basic molecular links of the BR signal transduction pathway are not well understood regarding this phosphorylation/dephosphorylation event. This review summarizes the current state of BR signal transduction research to uncover the phosphorylation/dephosphorylation networks and suggests directions for future research on steroid signal transduction to gain a more comprehensive understanding of the process.
Keywords
Brassinosteroid; protein phosphorylation; leucine-rich repeat receptor-like-protein kinase (LRR-RLK); phosphatase; receptor-like cytoplasmic kinase (RLCK);
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Wu, G., X. Wang, X. Li, Y. Kamiya, M. S. Otegui, and J. Chory. 2011. Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci. Signal. 4, ra29.   DOI
2 Yang, C. J., C. Zhang, Y. N. Lu, J. Q. Jin, and X. L. Wang. 2011. The mechanism of Brassinosteroids' Action, From signal transduction to plant development. Mol. Plant doi, 10.1093/mp/ssr020.   DOI
3 Ye, H., L. Li, and Y. Yin. 2011. Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathway. J. Integr. Plant Biol. 53, 455-468.   DOI   ScienceOn
4 Yin, Y., D. Vafeados, Y. Tao, T. Yokoda, T. Asami, and J. Chory. 2005. A new class of transcription factors mediate brassinosteroid-regulated gene expression in Arabidopsis. Cell 120, 249-259.   DOI   ScienceOn
5 Yin, Y., Z. Y. Wang, S. Mora-Garcia, J. Li, S. Yoshida, T. Asami, and J. Chory. 2002. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181-191.   DOI   ScienceOn
6 Yun, H. S., Y. H. Bae, Y. J. Lee, S. C. Chang, and S. K. Kim. 2009. Analysis of phosphorylation of the BRI1/BAK1 complex in Arabidopsis reveals amino acid residues critical for receptor formation and activation of BR signaling. Mol. Cell 27, 183-190.   DOI   ScienceOn
7 Zhou, A., H. Wang, J. C. Walker, and J. Li. 2004. BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant J. 40, 399-409.   DOI   ScienceOn
8 Tang, W., M. Yuan, R. Wang, Y. Yang, C. Wang, J. A. Oses-Prieto, T. W. Kim, H. W. Zhou, Z. Deng, S. S. Gampala, J. M. Gendron, E. M. Jonassen, C. Lillo, A. DeLong, A. L. Burlingame, Y. Sun, and Z. Y. Wang. 2011. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124-131.   DOI   ScienceOn
9 Vert, G. and J. Chory. 2006. Downstream nuclear events in brassinosteroid signalling. Nature 441, 96-100.   DOI   ScienceOn
10 Vert, G., J. L. Nemhauser, N. Geldner, F. Hong, and J. Chory. 2005. Molecular mechanisms of steroid hormone signaling in plants. Ann. Rev. Cell Dev. Biol. 21, 177-201.   DOI   ScienceOn
11 Wang, X. and J. Chory. 2006. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, form the plasma membrane. Science 313, 1118-1122.   DOI   ScienceOn
12 Wang, Z. Y., T. Nakano, J. Gendron, J. He, M. Chen, D. Vafeados, Y. Yang, S. Fujioka, S. T. Asami, and J. Chory. 2002. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505-513.   DOI   ScienceOn
13 Wang, X., M. B. Goshe, E. J. Soderblom, B. S. Phinney, J. A. Kuchar, J. Li, T. Asami, S. Yoshida, S. C. Huber, and S. D. Clouse. 2005a. Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSTIVE1 receptor kinase. Plant Cell 17, 1685-1703.   DOI   ScienceOn
14 Wang, X., U. Kota, K. He, K. Blackburn, J. Li, M.B. Goshe, S. C. Huber, and S. D. Clouse. 2008. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 15, 220-235.   DOI   ScienceOn
15 Wang, X., X. Li, J. Meisenhelder, T. Hunter, S. Yoshida, T. Asami, and J. Chory. 2005b. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8, 855-865.   DOI   ScienceOn
16 White, R. and M. G. Parker. 1998. Molecular mechanisms of steroid hormone action. Endocrine-Related Cancer 5, 1-14.   DOI   ScienceOn
17 Wu, D. and W. Pan. 2010, GSK3: multifaceted kinase in Wnt signaling. Trends Biochem. Sci. 35, 161-168.   DOI
18 Russinova, E., J. W. Borst, M. Kwaaitaal, A. Cãno-Delgado, Y. Yin, Chory, J., and S. C. de Vries. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216-3229.   DOI   ScienceOn
19 Ryu, H., K. Kim, H. Cho, J. Park, S. Choe, and I. Hwang. 2007. Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19, 2749-2762.   DOI   ScienceOn
20 Shah, K., E. Russinova, T. W. Jr. Gadella, J. Willemse, and S. C. de Vries. 2002. The Arabidopsis kinase associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev. 16, 1707-1720.   DOI   ScienceOn
21 Shan, L., P. He, J. Li, A. Heese, S. C. Peck, T. Nurnberger, G. B. Martin, and J. Sheen. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17-27.   DOI   ScienceOn
22 Shiu, S. H., W. M. Karlowski, R. Pan, Y. H. Tzeng, K. F. Mayer, and W. H. Li. 2004. Comparative analysis of the receptor- like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234.   DOI   ScienceOn
23 Schlessinger, J. 2002. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110, 669-672.   DOI   ScienceOn
24 Schulze, B., T. Mentzel, A. K. Jehle, K. Mueller, S. Beeler, T. Boller, G. Felix, and D. Chinchilla. 2010. Rapid heterodimerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444-9451.   DOI
25 Stanevich, V., L. Jiang, K. A. Satyshur, Y. Li, P. D. Jeffrey, Z. Li, P. Menden, M. F. Semmelhack, and Y. Xing. 2011. The structural basis for tight control of PP2A methylation and function by LCMT-1. Mol. Cell 41, 331-342.   DOI   ScienceOn
26 Tang, W., T. W. Kim, J. A. Oses-Prieto, Y. Sun, Z. Deng, S. Zhu, R. Wang, A. L. Burlingame, and Z. Y. Wang. 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557-560.   DOI
27 Muto, H., N. Yabe, T. Asami, K. Hasunuma, and K. T. Yamamoto. 2004. Overexpression of constitutive differential growth 1 gene, which encodes a RLCKVII-subfamily protein kinase, causes abnormal differential and elongation growth after organ differentiation in Arabidopsis. Plant Physiol. 136, 3124-3133.   DOI   ScienceOn
28 Oh, M. H., S. D. Clouse, and S. C. Huber. 2009a. Tyrosine phosphorylation in brassinosteroid signaling. Plant Signal. Behav. 4, 1182-1185.   DOI   ScienceOn
29 Nam, K. H. and J. Li. 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212.   DOI   ScienceOn
30 Nam, K. H. and J. Li. 2004. The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROIDINSENSITIVE 1. Plant Cell 16, 2406-2417.   DOI   ScienceOn
31 Oh, M. H., W. K. Ray, S. C. Huber, J. M. Asara, D. A. Gage, and S. D. Clouse. 2000. Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol. 124, 751-766.   DOI   ScienceOn
32 Oh, M. H., X. Wang, U. Kota, M. B. Goshe, S. D. Clouse, and S. C. Huber. 2009b. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 106, 658-663.   DOI   ScienceOn
33 Perez-Perez, J. M., M. R. Ponce, and J. L. Micol. 2002. The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161-173.   DOI   ScienceOn
34 Postel, S., I. Küfner, C. Beuter, S. Mazzotta, A. Schwedt, A. Borlotti, T. Halter, B. Kemmerling, and T. Nürnberger. 2010. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur. J. Cell Biol. 89, 169-174.   DOI   ScienceOn
35 Rahimi, R. A. and E. B. Leof, 2007. TGF-beta signaling: a tale of two responses. J. Biol. Chem. 102, 593-608.
36 Kemmerling, B., A. Schwedt, P. Rodriguez, S. Mazzotta, M. Frank, S. A. Qamar, T. Mengiste, S., Parker, J. E. Betsuyaku, C. Mussig, B. P. Thomma, C. Albrecht, S. C. de Vries, H. Hirt, and T. Nurnberger. 2007. The BRI1-associated kinase 1, BAK1, has a brassinolide independent role in plant cell-death control. Curr. Biol. 17, 1116-1122.   DOI   ScienceOn
37 Kinoshita, T., A. Cãno-Delgado, H. Seto, S. Hiranuma, S. Fujioka, S. Yoshida, and J. Chory. 2005. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167-171.   DOI   ScienceOn
38 Kim, T. W., S. Guan, A. L. Burlingame, and Z. Y. Wang. 2011. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK-3-like kinase BIN2. Mol. Cell 43, 561-571.   DOI   ScienceOn
39 Kim, T. W., S. Guan, Y. Sun, Z. Deng, W. Tang, J. X. Shang, Y. Sun, A. L., Burlingame, and Z. Y. Wang. 2009. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nature Cell Biol. 11, 1254-1262.   DOI   ScienceOn
40 Kim, T. W. and Z. Y. Wang. 2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Ann. Rev. Plant Biol. 61, 681-704.   DOI   ScienceOn
41 Li, J. and J. Chory. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.   DOI   ScienceOn
42 Li, J. and K. H. Nam. 2002. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295: 1299-1301.
43 Li, J., J. Wen, K. A. Lease, J. T. Doke, F. E. Tax, and J. C. Walker. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222.   DOI   ScienceOn
44 Liu, T. and Z. H. Feng. 2010, Regulation of TGF-beta signaling by protein phosphatases. Biochem. J. 430, 191-198.   DOI   ScienceOn
45 Mora-Garcia, S., G. Vert, Y. Yin, A. Cãno-Delgado, H. Cheong, and J. Chory. 2004. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448-460.   DOI   ScienceOn
46 Heese, A., D. R. Hann, S. Gimenez-Ibanez, A. M. Jones, K. He, J. Li, J. I. Schroeder, S. C. Peck, and J. P. Rathjen. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104, 12217-12222.   DOI   ScienceOn
47 He, K., X. Gou, R. A. Powell, H. Yang, T. Yuan, Z. Guo, and J. Li. 2008. Receptor-like protein kinases, BAK1 and BKK1, regulate a light-dependent cell-death control pathway. Plant Signal. Behav. 3, 813-815.   DOI   ScienceOn
48 He, K., X. Gou, T., Yuan, H. Lin, T. Asami, S. Yoshida, S. D. Russell, and J. Li. 2007. BAK1 and BKK1 regulate brassinosteroid- dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 1109-1115.   DOI   ScienceOn
49 Hecht, V., J. P. Vielle-Calzada, M. V. Hartog, E. D. Schmidt, K. Boutilier, U. Grossniklaus, and S. C. de Vries. 2001. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 127, 803-816.   DOI   ScienceOn
50 Jaillais, Y., M. Hothorn, Y. Belkhadir, T. Dabi, Z. L. Nimchuk, E. M. Meyerowitz, and J. Chory. 2011. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 25, 232-237.   DOI   ScienceOn
51 Janssens, V., S. Longin, and J. Goris. 2008. PP2A holoenzyme assembly, In cauda venenum (the sting is in the tail). Trends Biochem. Sci. 33, 113-121.   DOI
52 Karlova, R., S. Boeren, E. Russinova, J. Aker, J. Vervoort, and S. C. de Vries. 2006. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID- INSENSITIVE1. Plant Cell 18, 626-638.   DOI   ScienceOn
53 Karlova, R., S. Boeren, W. van Dongen, M. Kwaaitaal, and J. Aker. 2009. Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics 9, 368-379.   DOI   ScienceOn
54 Eden, E. R., I. J. White, and C. E. Futter. 2009, Down-regulation of epidermal growth factor receptor signaling within multivesicular bodies. Biochem. Soc. Trans. 37, 173-177.   DOI   ScienceOn
55 Colcombet, J., A. Boisson-Dernier, R. Ros-Palau, C. E. Vera, and J. I. Schroeder. 2005. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350-3361.   DOI   ScienceOn
56 Deng, Z., X. Zhang, W. Tang, J. A. Oses-Prieto, and N. Suzuki. 2007. A proteomics study of brassinosteroid response in Arabidopsis. Mol. Cell Proteomics 6, 2058-2071.   DOI   ScienceOn
57 Di Rubbo, S., N. G. Irani, and E. Russinova. 2011. PP2A Phosphatases, The "On-Off" Regulatory Switches of Brassinosteroid Signaling. Sci. Signal. 4, pe25.   DOI
58 Ehsan, H., W. K. Ray, B. Phinney, X. Wang, S. C. Huber, and S. D. Clouse. 2005. Interaction of Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase with a homolog of mammalian TGF-beta receptor interacting protein. Plant J. 43, 251-261.   DOI   ScienceOn
59 Friedrichsen, D. M., C. A. Joazeiro, J. Li, T. Hunter, and J. Chory. 2000. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine rich repeat receptor serine/threonine kinase. Plant Physiol. 123, 1247-1256.   DOI   ScienceOn
60 Fujioka, S. and T. Yokota. 2003. Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137-164.   DOI   ScienceOn
61 Gampala, S. S., T. W. Kim, J. X. He, W. Tang, Z. Deng, M. Y. Bai, S. Guan, S. Lalonde, Y. Sun, J. M. Gendron, H. Chen, N. Shibagaki, R. J. Ferl, D. Ehrhardt, K. Chong, A. L. Burlingame, and Z. Y. Wang. 2007. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13, 177-189.   DOI   ScienceOn
62 Bar, M., M. Sharfman, M. Ron, and A. Avni. 2010. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 63, 791-800.   DOI   ScienceOn
63 He, J. X., J. M. Gendron, Y. Yang, J. Li, and Z. Y. Wang. 2002. The GSK3- like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 10185-10190.   DOI   ScienceOn
64 Albrecht, C., E. Russinova, B. Kemmerling, M., Kwaaitaal, and S. C. de Vries. 2008. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways. Plant Physiol. 148, 611-619.   DOI   ScienceOn
65 Avraham, R. and Y. Yarden. 2011. Feedback regulation of EGFR signaling, decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12, 104-117.   DOI   ScienceOn
66 Cano-Delgado, A., Y. Yin, C. Yu, D., Vafeados, S. Mora-García, J. C. Cheng, K. H. Nam, J. Li, and J. Chory. 2004. BRL1 and BRL3 are novel Brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341-5351.   DOI   ScienceOn
67 Chinchilla, D., L. Shan, P. He, S. C. de Vries, and B. Kemmerling. 2009. One for all, The receptor-associated kinase BAK1. Trends Plant Sci. 14, 535-541.   DOI   ScienceOn
68 Choe, S., R. J. Schmitz, S., Fujioka, S. Takatsuto, M. O. Lee, S. Yoshida, K. A. Feldmann, and F. E. Tax. 2002. Arabidopsis brassinosteroid insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3beta-like kinase. Plant Physiol. 130, 1506-1515.   DOI   ScienceOn
69 Clouse, S. D. 2002. Brassinosteroid signaling, novel downstream components emerge. Curr. Biol. 12, R485-487.   DOI   ScienceOn
70 Clouse, S. D. 2011. Brassinosteroid signal transduction, From receptor kinase activation to transcriptional networks regulating plant development. Plant Cell doi, 10.1105/tpc.111.084475.   DOI
71 Clouse, S. D., M. Langford, and T. C. McMorris. 1996. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111, 671-678.   DOI   ScienceOn
72 Clouse, S. D. and J. M. Sasse. 1998. BRASSINOSTEROIDS, Essential Regulators of Plant Growth and Development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427-451.   DOI   ScienceOn
73 Aker, J. and S. C. de Vries. 2008. Plasma membrane receptor complexes. Plant Physiol. 147, 1560-1564.   DOI   ScienceOn