Membrane steroid-binding protein 1 (MSBP1) negatively regulates brassinosteroid signaling by enhancing the endocytosis of BAK1

Cell Research

Volumn 19, Issue 7, 2009, Pages 864-876

  Song, Li ^a   Shi, Qiu Ming ^a   Yang, Xiao Hua ^a,b   Xu, Zhi Hong ^a   Xue, Hong Wei ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

BAK1; BR signaling; Endocytosiss; MSBP1

Indexed keywords

ARABIDOPSIS PROTEIN; BAK1 PROTEIN, ARABIDOPSIS; BRASSINOLIDE; BRI1 PROTEIN, ARABIDOPSIS; CARRIER PROTEIN; CHOLESTANOL; HETEROCYCLIC STEROID; MSBP1 PROTEIN, ARABIDOPSIS; PHYTOHORMONE; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE;

ARABIDOPSIS; ARTICLE; DIMERIZATION; ENDOCYTOSIS; METABOLISM; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CHOLESTANOLS; DIMERIZATION; ENDOCYTOSIS; PLANT GROWTH REGULATORS; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STEROIDS, HETEROCYCLIC;

EID: 68149162725     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2009.66     Document Type: Article

References (62)

1. Clouse SD, Sasse JM. BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 1998; 49:427-451.
2. Takahashi T, Gasch A, Nishizawa N, Chua N. The DIMINU-TO gene of Arabidopsis is involved in regulating cell elongation. Genes Dev 1995; 9:97-107.
3. Clouse SD, Langford M, Mcmorris TC. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 1996; 111:671-678.
4. Li J, Nagpal P, Vitart V, McMorris TC, Chory J. A role for brassinosteroids in light-dependent development of Arabidopsis. Science 1996; 272:398-401.
5. Szekeres M, Nemeth K, Koncz-kalman Z, et al. Brassinosteroids rescue the defciency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell1996; 85:171-182.
6. Li J, Nam KH, Vafeados D, Chory J. BIN2, a new brassinosteroids insensitive locus in Arabidopsis. Plant Physiol 2001; 127:14-22.
7. Li J, Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 1997; 90:929-938.
8. He ZH, Wang ZY, Li J, et al. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 2000; 288:2360-2363.
9. Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 2001; 410:380-383.
10. Kinoshita T, Cano-Delgado A, Seto H, et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 2005; 433:167-171.
11. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 2002; 110:213-222.
12. Li J, Nam KH. Regulation of brassinosteroids signaling by a GSK3/SHAGGY-like kinase. Science 2002; 295:1299-1301.
13. Wang X, Li X, Meisenhelder J, et al. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev Cell 2005; 8:855-865.
14. Wang X, Goshe MB, Soderblom EL, et al. Identifcation and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase. Plant Cell 2005; 17:1685-1703.
15. Russinova E, Borst JW, Kwaaitaal M, et al. Heterodimerization and endocytosis of Arabidopsis brassinosteroids receptors BRI1 and AtSERK3 (BAK1). Plant Cell 2004; 16:3216-3229.
16. Tang W, Kim TW, Oses-Prieto JA, et al. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 2008; 321:557-560.
17. Wang X, Chory J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 2006; 313:1118-1122.
18. Wang ZY, Nakano T, Gendron J, et al. Nuclear-localized BZR1 mediates brassinosteroids-induced growth and feedback suppression of brassinosteroids biosynthesis. Dev Cell 2002; 2:505-513.
19. Zhao J, Peng P, Schmitz RJ, Decker AD, Tax FE, Li J. Two putative BIN2 substrates are nuclear component of brassinosteroid signaling. Plant Physiol 2002; 13:1221-1229.
20. Yin Y, Wang ZY, Mora-Garcia S, et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 2002; 109:181-191.
21. Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 2005; 120:249-259.
22. Vert G, Chory J. Downstream nuclear event in brassinosteroids signaling. Nature 2006; 441:96-100.
23. He JX, Gendron JM, Yang Y, Li J, Wang ZY. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci USA 2002; 99:10185-10190.
24. He JX, Gendron JM, Sun Y, et al. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth response. Science 2005; 307:1634-1638.
25. Edwards PA, Ericsson J. Sterols and isoprenoids: signaling molecules derived from the cholesterol biosynthetic pathway. Annu Rev Biochem 1999; 68:157-185.
26. Michaux G, Gansmuller A, Hindelang C, Labouesse M. CHE-14, a protein with a sterol-sensing domain, is required for apical sorting in C. elegans ectodermal epithelial cells. Curr Biol 2000; 10:1098-1107.
27. Ingham PW. Hedgehog signaling: a tale of two lipids. Science 2001; 294:1879-1881.
28. Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle traffcking. Nature 2001; 413:425-428.
29. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 2002; 415:806-809.
30. Dhonukshe P, Aniento F, Hwang I, et al. Clathrin-mediated constitutive endocytosis of PIN auxin effux carriers in Arabidopsis. Curr Biol 2007; 17:520-527.
31. Gómez-Gómez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor fagellin in Arabidopsis. Mol Cell 2000; 5:1003-1011.
32. Robatzek S, Chinchilla D, Boller T. Ligand-induced endocy-tosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 2006; 20:537-542.
33. Chinchilla D, Zipfel C, Robatzek S, et al. A fagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007; 448:497-500.
34. Heese A, Hann DR, Gimenez-Ibanez S, et al. The receptorlike kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 2007; 104:12217-12222.
35. Geldner N, Hyman DL, Wang XL, Schumacher K, Chory J. Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 2007; 21:1598-1602.
36. Kwaaitaal MA, de Vries SC, Russinova E. Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein is present in sporophytic and gametophytic cells and undergoes endocytosis. Protoplasma 2005; 226:55-65.
37. Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 2006; 18:626-638.
38. Evans RM. The steroid and thyroid hormone receptor superfamily. Science 1988; 240:889-895.
39. Glass CK. Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocr Rev 1994; 15:391-407.
40. Beato M, Herrlich P, Schutz G. Steroid hormone receptors: many actors in search of a plot. Cell 1995; 83:851-857.
41. Mangelsdorf DJ, Thummel C, Beato M, et al. The nuclear receptor superfamily: the second decade. Cell 1995; 83:835-839.
42. Yang XH, Xu ZH, Xue HW. Arabidopsis membrane steroidbinding protein 1 is involved in inhibition of cell elongation. Plant Cell 2005; 17:116-131.
43. Sonnhammer ELL, von Heijne G, Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology. Menlo Park, CA: AAAI Press, 1998:175-182.
44. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 2001; 305:567-580.
45. Song WY, Wang GL, Chen LL, et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 1995; 270:1804-1806.
46. Nam KH, Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 2002; 110:203-212.
47. Whippo CW, Hangarter RP. A brassinosteroids-hypersensitive mutant of BAK1 indicates that a convergence of photomor-phogenic and hormonal signaling modulates phototropism. Plant Physiol 2005; 139:448-457.
48. Xu J, Scheres B. Dissection of Arabidopsis ADP-RIBOSY-LATION FACTOR 1 function in epidermal cell polarity. Plant Cell 2005; 17:525-536.
49. Yang X, Song L, Xue HW. Membrane steroid binding protein 1 (MSBP1) stimulates tropism by enhancing polar auxin transport. Mol Plant 2008; 1:1077-1087.
50. Wang X, Kota U, He K, et al. Se quential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 2008; 15:220-235.
51. Kobe B, Deisenhofer J. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature 1995; 374:183-186.
52. Jones DA, Jones JDG. The role of leucine-rich repeat proteins in plant defences. Adv Bot Res 1997; 24:89-167.
53. Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K. Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 2005; 17:1105-1119.
54. Ephritikhine G, Pagant S, Fujioka S, et al. The sax1 mutation defnes a new locus involved in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 1999; 18:315-320.
55. De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D. Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol 2005; 46: 827-836.
56. Bishop GJ. Brassinosteroid mutants of crops. J Plant Growth Regul 2003; 22:325-335.
57. Yang HQ, Tang RH, Cashmore AR. The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell 2001; 13:2573-2587.
58. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thali- ana. Plant J 1998; 16: 735-743.
59. Sheen J. Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol 2001; 127: 1466-1475.
60. Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO. pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J 2002; 31:375-383.
61. Shah K, Russinova E, Gadella TW Jr, Willemse J, De Vries SC. The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev 2002; 16:1707-1720.
62. Bradford MM. A rapid and sensitive for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-254.