The BRASSINOSTEROID INSENSITIVE1-LIKE3 signalosome complex regulates Arabidopsis root development

Plant Cell

Volumn 25, Issue 9, 2013, Pages 3377-3388

  Fàbregas, Norma ^a   Li, Na ^b   Boeren, Sjef ^b   Nash, Tara E ^c   Goshe, Michael B ^d   Clouse, Steven D ^c   de Vries, Sacco ^b   Caño Delgado, Ana I ^a  

^a CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d Department of Molecular and Structural Biochemistry ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; BAK1 PROTEIN, ARABIDOPSIS; BRASSINOSTEROID; BRL1 PROTEIN, ARABIDOPSIS; BRL3 PROTEIN, ARABIDOPSIS; CELL SURFACE RECEPTOR; HYBRID PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN SERINE THREONINE KINASE;

ARABIDOPSIS; CELL CYCLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIQUID CHROMATOGRAPHY; METABOLISM; MUTATION; PHENOTYPE; PHLOEM; PLANT ROOT; PROTEIN ANALYSIS; REPORTER GENE; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; CELL CYCLE; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; MULTIPROTEIN COMPLEXES; MUTATION; PHENOTYPE; PHLOEM; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN INTERACTION MAPPING; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84886487267     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.114462     Document Type: Article

References (49)

1. Albrecht, C., Russinova, E., Kemmerling, B., Kwaaitaal, M., and de Vries, S.C. (2008). Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and-independent signaling pathways. Plant Physiol. 148: 611-619.
2. Bell, E.M., Lin, W.C., Husbands, A.Y., Yu, L., Jaganatha, V., Jablonska, B., Mangeon, A., Neff, M.M., Girke, T., and Springer, P.S. (2012). Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc. Natl. Acad. Sci. USA 109: 21146-21151.
3. Caño-Delgado, A., Yin, Y., Yu, C., Vafeados, D., Mora-García, S., Cheng, J.C., Nam, K.H., Li, J., and Chory, J. (2004). BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341-5351.
4. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
5. Deng, Z., Zhang, X., Tang, W., Oses-Prieto, J.A., Suzuki, N., Gendron, J.M., Chen, H., Guan, S., Chalkley, R.J., Peterman, T.K., Burlingame, A.L., and Wang, Z.Y. (2007). A proteomics study of brassinosteroid response in Arabidopsis. Mol. Cell. Proteomics 6: 2058-2071.
6. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D., and Schumacher, K. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
7. Fàbregas, N., Ibañes, M., and Caño-Delgado, A.I. (2010). A systems biology approach to dissect the contribution of brassinosteroid and auxin hormones to vascular patterning in the shoot of Arabidopsis thaliana. Plant Signal. Behav. 5: 903-906.
8. Friedrichsen, D.M., Joazeiro, C.A., Li, J., Hunter, T., and Chory, J. (2000). Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol. 123: 1247-1256.
9. Gamborg, O.L., Miller, R.A., and Ojima, K. (1968). Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50: 151-158.
10. Geldner, N., Hyman, D.L., Wang, X., Schumacher, K., and Chory, J. (2007). Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21: 1598-1602.
11. Gendron, J.M., Liu, J.S., Fan, M., Bai, M.Y., Wenkel, S., Springer, P.S., Barton, M.K., and Wang, Z.Y. (2012). Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc. Natl. Acad. Sci. USA 109: 21152-21157.
12. González-García, M.P., Vilarrasa-Blasi, J., Zhiponova, M., Divol, F., Mora-García, S., Russinova, E., and Caño-Delgado, A.I. (2011). Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138: 849-859.
13. Gou, X., Yin, H., He, K., Du, J., Yi, J., Xu, S., Lin, H., Clouse, S.D., and Li, J. (2012). Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet. 8: e1002452.
14. Gudesblat, G.E., Schneider-Pizoń, J., Betti, C., Mayerhofer, J., Vanhoutte, I., van Dongen, W., Boeren, S., Zhiponova, M., de Vries, S., Jonak, C., and Russinova, E. (2012). SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat. Cell Biol. 14: 548-554.
15. Guo, H., Li, L., Ye, H., Yu, X., Algreen, A., and Yin, Y. (2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 106: 7648-7653.
16. Hacham, Y., Holland, N., Butterfield, C., Ubeda-Tomas, S., Bennett, M.J., Chory, J., and Savaldi-Goldstein, S. (2011). Brassinosteroid perception in the epidermis controls root meristem size. Development 138: 839-848.
17. He, K., Gou, X., Yuan, T., Lin, H., Asami, T., Yoshida, S., Russell, S.D., and Li, J. (2007). BAK1 and BKK1 regulate brassinosteroiddependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17: 1109-1115.
18. Hothorn, M., Belkhadir, Y., Dreux, M., Dabi, T., Noel, J.P., Wilson, I.A., and Chory, J. (2011). Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474: 467-471.
19. Ibañes, M., Fàbregas, N., Chory, J., and Caño-Delgado, A.I. (2009). Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc. Natl. Acad. Sci. USA 106: 13630-13635.
20. Karlova, R., Boeren, S., Russinova, E., Aker, J., Vervoort, J., and de Vries, S. (2006). The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROIDINSENSITIVE1. Plant Cell 18: 626-638.
21. Keller, A., Nesvizhskii, A.I., Kolker, E., and Aebersold, R. (2002). Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74: 5383-5392.
22. Kim, T.W., Guan, S., Burlingame, A.L., and Wang, Z.Y. (2011). The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43: 561-571.
23. Kim, T.W., Michniewicz, M., Bergmann, D.C., and Wang, Z.Y. (2012). Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482: 419-422.
24. Kinoshita, T., Caño-Delgado, A., Seto, H., Hiranuma, S., Fujioka, S., Yoshida, S., and Chory, J. (2005). Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433: 167-171.
25. Kuppusamy, K.T., Chen, A.Y., and Nemhauser, J.L. (2009). Steroids are required for epidermal cell fate establishment in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 106: 8073-8076.
26. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
27. Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., and Walker, J.C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222.
28. Mitra, S.K., Goshe, M.B., and Clouse, S.D. (2012). Experimental analysis of receptor kinase phosphorylation. Methods Mol. Biol. 876: 1-15.
29. Nesvizhskii, A.I., Keller, A., Kolker, E., and Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75: 4646-4658.
30. Rohila, J.S., Chen, M., Cerny, R., and Fromm, M.E. (2004). Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant J. 38: 172-181.
31. Russinova, E., Borst, J.W., Kwaaitaal, M., Caño-Delgado, A., Yin, Y., Chory, J., and de Vries, S.C. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16: 3216-3229.
32. She, J., Han, Z., Kim, T.W., Wang, J., Cheng, W., Chang, J., Shi, S., Wang, J., Yang, M., Wang, Z.Y., and Chai, J. (2011). Structural insight into brassinosteroid perception by BRI1. Nature 474: 472-476.
33. Smaczniak, C., Li, N., Boeren, S., America, T., van Dongen, W., Goerdayal, S.S., de Vries, S., Angenent, G.C., and Kaufmann, K. (2012). Proteomics-based identification of low-abundance signaling and regulatory protein complexes in native plant tissues. Nat. Protoc. 7: 2144-2158.
34. Sun, Y., et al. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19: 765-777.
35. Tang, W., Kim, T.W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., Wang, R., Burlingame, A.L., and Wang, Z.Y. (2008). BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321: 557-560.
36. Truernit, E., Bauby, H., Dubreucq, B., Grandjean, O., Runions, J., Barthélémy, J., and Palauqui, J.C. (2008). High-resolution wholemount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20: 1494-1503.
37. Wang, X., and Chory, J. (2006). Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313: 1118-1122.
38. Wang, X., Kota, U., He, K., Blackburn, K., Li, J., Goshe, M.B., Huber, S.C., and Clouse, S.D. (2008). Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 15: 220-235.
39. Wang, X., Goshe, M.B., Soderblom, E.J., Phinney, B.S., Kuchar, J.A., Li, J., Asami, T., Yoshida, S., Huber, S.C., and Clouse, S.D. (2005). Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell 17: 1685-1703.
40. Wang, Z.Y., Bai, M.Y., Oh, E., and Zhu, J.Y. (2012). Brassinosteroid signaling network and regulation of photomorphogenesis. Annu. Rev. Genet. 46: 701-724.
41. Wang, Z.Y., Seto, H., Fujioka, S., Yoshida, S., and Chory, J. (2001). BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410: 380-383.
42. Wang, Z.Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T., and Chory, J. (2002). Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2: 505-513.
43. Wilma van Esse, G., Westphal, A.H., Surendran, R.P., Albrecht, C., van Veen, B., Borst, J.W., and de Vries, S.C. (2011). Quantification of the brassinosteroid insensitive1 receptor in planta. Plant Physiol. 156: 1691-1700.
44. Witthöft, J., Caesar, K., Elgass, K., Huppenberger, P., Kilian, J., Schleifenbaum, F., Oecking, C., and Harter, K. (2011). The activation of the Arabidopsis P-ATPase 1 by the brassinosteroid receptor BRI1 is independent of threonine 948 phosphorylation. Plant Signal. Behav. 6: 1063-1066.
45. Wu, F.H., Shen, S.C., Lee, L.Y., Lee, S.H., Chan, M.T., and Lin, C.S. (2009). Tape-Arabidopsis Sandwich-A simpler Arabidopsis protoplast isolation method. Plant Methods 5: 16.
46. Wu, G., Wang, X., Li, X., Kamiya, Y., Otegui, M.S., and Chory, J. (2011). Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci. Signal. 4: ra29.
47. Ye, Q., Zhu, W., Li, L., Zhang, S., Yin, Y., Ma, H., and Wang, X. (2010). Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl. Acad. Sci. USA 107: 6100-6105.
48. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., and Chory, J. (2005). A new class of transcription factors mediates brassinosteroidregulated gene expression in Arabidopsis. Cell 120: 249-259.
49. Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., Guo, H., Anderson, S., Aluru, S., Liu, P., Rodermel, S., and Yin, Y. (2011). A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65: 634-646.