An autophosphorylation site database for leucine-rich repeat receptor-like kinases in Arabidopsis thaliana

Plant Journal

Volumn 82, Issue 6, 2015, Pages 1042-1060

  Mitra, Srijeet K ^a,d   Chen, Ruiqiang ^a,e   Dhandaydham, Murali ^a   Wang, Xiaofeng ^a,f   Blackburn, Robert Kevin ^a   Kota, Uma ^a,g   Goshe, Michael B ^a   Schwartz, Daniel ^b   Huber, Steven C ^c   Clouse, Steven D ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d BASF CORPORATION   (United States)

^e VANDERBILT UNIVERSITY   (United States)

^f NORTHWEST A F UNIVERSITY   (China)

^g STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Arabidopsis thaliana; mass spectrometry; motif analysis; phosphorylation; receptor kinase

Indexed keywords

CELL PROLIFERATION; CLONE CELLS; CLONING; DATABASE SYSTEMS; MASS SPECTROMETRY; PHOSPHORYLATION; PLANTS (BOTANY);

ARABIDOPSIS THALIANA; EXTRACELLULAR DOMAINS; FUNCTIONAL CHARACTERIZATION; LEUCINE-RICH REPEAT RECEPTOR-LIKE KINASE; MOTIF ANALYSIS; PHOSPHORYLATION SITES; RECEPTOR KINASE; TRANSMEMBRANE SEQUENCES;

ENZYMES;

ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS);

ARABIDOPSIS PROTEIN; BAK1 PROTEIN, ARABIDOPSIS; BRI1 PROTEIN, ARABIDOPSIS; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SERK1 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; CYTOPLASM; ESCHERICHIA COLI; FACTUAL DATABASE; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOPLASM; DATABASES, FACTUAL; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES;

EID: 84930868267     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12863     Document Type: Article

References (61)

1. Adams, J.A., (2003) Activation loop phosphorylation and catalysis in protein kinases: is there functional evidence for the autoinhibitor model? Biochemistry, 42, 601-607.
2. Arsova, B., and, Schulze, W.X., (2012) Current status of the plant phosphorylation site database PhosPhAt and its use as a resource for molecular plant physiology. Front. Plant Sci. 3, 132.
3. Bajwa, V.S., Wang, X., Blackburn, R.K., et al. (2013) Identification and functional analysis of tomato BRI1 and BAK1 receptor kinase phosphorylation sites. Plant Physiol. 163, 30-42.
4. Becraft, P.W., (2002) Receptor kinase signaling in plant development. Annu. Rev. Cell Dev. Biol. 18, 163-192.
5. Bojar, D., Martinez, J., Santiago, J., Rybin, V., Bayliss, R., and, Hothorn, M., (2014) Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J. 78, 31-43.
6. Braun, D.M., and, Walker, J.C., (1996) Plant transmembrane receptors: new pieces in the signaling puzzle. Trends Biochem. Sci. 21, 70-73.
7. Butenko, M.A., and, Aalen, R.B., (2012) Receptor ligands in development. In Receptor-Like Kinases in Plants: From Development to Defense (, Tax, F., and, Kemmerling, B., ed.). Berlin: Springer-Verlag, pp. 195-226.
8. Cao, Y., Aceti, D.J., Sabat, G., Song, J., Makino, S., Fox, B.G., and, Bent, A.F., (2013) Mutations in FLS2 Ser-938 dissect signaling activation in FLS2-mediated Arabidopsis immunity. PLoS Pathog. 9, e1003313.
9. Cheng, H., Deng, W., Wang, Y., Ren, J., Liu, Z., and, Xue, Y., (2014) dbPPT: a comprehensive database of protein phosphorylation in plants. Database, 2014, bau121.
10. Clouse, S.D., (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell, 23, 1219-1230.
11. Clouse, S.D., Goshe, M.B., and, Huber, S.C., (2012) Phosphorylation and RLK signaling. In Receptor-Like Kinases in Plants (, Tax, F.E., and, Kemmerling, B., eds). Berlin: Springer-Verlag, pp. 227-251.
12. Clouse, S.D., Goshe, M.B., Huber, S.C., and, Li, J., (2008) Functional analysis and phosphorylation site mapping of leucine-rich repeat receptor-like kinases. In Plant Proteomics: Technologies, Strategies and Applications (, Agrawal, G.K., and, Rakwal, R., eds). Hoboken, NJ: John Wiley & Sons, pp. 469-484.
13. Clouse, S.D., Hall, A.F., Langford, M., McMorris, T.C., and, Baker, M.E., (1993) Physiological and molecular effects of brassinosteroids on Arabidopsis thaliana. J. Plant Growth Regul. 12, 61-66.
14. de Castro, E., Sigrist, C.J.A., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P.S., Gasteiger, E., Bairoch, A., and, Hulo, N., (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362-W365.
15. de Lorenzo, L., Merchan, F., Laporte, P., Thompson, R., Clarke, J., Sousa, C., and, Crespi, M., (2009) A novel plant leucine-rich repeat receptor kinase regulates the response of Medicago truncatula roots to salt stress. Plant Cell, 21, 668-680.
16. Durek, P., Schmidt, R., Heazlewood, J.L., Jones, A., MacLean, D., Nagel, A., Kersten, B., and, Schulze, W.X., (2010) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Res. 38, D828-D834.
17. Fan, J., Mohareb, F., Jones, A.M., and, Bessant, C., (2012) MRMaid: the SRM assay design tool for Arabidopsis and other species. Front. Plant Sci. 3, 164.
18. Gish, L.A., and, Clark, S.E., (2011) The RLK/Pelle family of kinases. Plant J. 66, 117-127.
19. Greeff, C., Roux, M., Mundy, J., and, Petersen, M., (2012) Receptor-like kinase complexes in plant innate immunity. Front. Plant Sci. 3, 209.
20. Karlova, R., Boeren, S., van Dongen, W., Kwaaitaal, M., Aker, J., Vervoort, J., and, de Vries, S., (2009) Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics, 9, 368-379.
21. Kim, T.W., and, Wang, Z.Y., (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681-704.
22. Knighton, D.R., Zheng, J.H., Ten Eyck, L.F., Ashford, V.A., Xuong, N.H., Taylor, S.S., and, Sowadski, J.M., (1991a) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science, 253, 407-414.
23. Knighton, D.R., Zheng, J.H., Ten Eyck, L.F., Xuong, N.H., Taylor, S.S., and, Sowadski, J.M., (1991b) Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science, 253, 414-420.
24. Lehti-Shiu, M.D., Zou, C., Hanada, K., and, Shiu, S.H., (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol. 150, 12-26.
25. 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.
26. Mitra, S.K., Goshe, M.B., and, Clouse, S.D., (2012) Experimental analysis of receptor kinase phosphorylation. Methods Mol. Biol. 876, 1-15.
27. Miyahara, A., Hirani, T.A., Oakes, M., Kereszt, A., Kobe, B., Djordjevic, M.A., and, Gresshoff, P.M., (2008) Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. J. Biol. Chem. 283, 25381-25391.
28. Mosher, S., and, Kemmerling, B., (2013) PSKR1 and PSY1R-mediated regulation of plant defense responses. Plant Signal. Behav. 8, e24119.
29. Nolen, B., Taylor, S., and, Ghosh, G., (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell, 15, 661-675.
30. O'Shea, J.P., Chou, M.F., Quader, S.A., Ryan, J.K., Church, G.M., and, Schwartz, D., (2013) pLogo: a probabilistic approach to visualizing sequence motifs. Nat. Methods, 10, 1211-1212.
31. Oh, M.H., Clouse, S.D., and, Huber, S.C., (2012a) Tyrosine phosphorylation of the BRI1 receptor kinase occurs via a post-translational modification and is activated by the juxtamembrane domain. Front. Plant Sci. 3, 175.
32. Oh, M.H., Kim, H.S., Wu, X., Clouse, S.D., Zielinski, R.E., and, Huber, S.C., (2012b) Calcium/calmodulin inhibition of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase provides a possible link between calcium and brassinosteroid signalling. Biochem. J. 443, 515-523.
33. Oh, M.-H., Wang, X., Clouse, S.D., and, Huber, S.C., (2012c) Deactivation of the Arabidopsis BRASSINOSTEROID INSENSITIVE 1 (BRI1) receptor kinase by autophosphorylation within the glycine-rich loop. Proc. Natl Acad. Sci. USA, 109, 327-332.
34. Oh, M.H., Ray, W.K., Huber, S.C., Asara, J.M., Gage, D.A., and, Clouse, S.D., (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.
35. Oh, M.H., Wang, X., Kota, U., Goshe, M.B., Clouse, S.D., and, Huber, S.C., (2009) Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 658-663.
36. Oh, M.H., Wang, X., Wu, X., Zhao, Y., Clouse, S.D., and, Huber, S.C., (2010) Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays a role in brassinosteroid signaling and basal defense gene expression. Proc. Natl Acad. Sci. USA, 107, 17827-17832.
37. Oliver, A.W., Knapp, S., and, Pearl, L.H., (2007) Activation segment exchange: a common mechanism of kinase autophosphorylation? Trends Biochem. Sci. 32, 351-356.
38. Pawson, T., (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell, 116, 191-203.
39. Peck, S.C., (2006) Phosphoproteomics in Arabidopsis: moving from empirical to predictive science. J. Exp. Bot. 57, 1523-1527.
40. Sakamoto, T., Deguchi, M., Brustolini, O.J., Santos, A.A., Silva, F.F., and, Fontes, E.P., (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol. 12, 229.
41. Santos, A.A., Carvalho, C.M., Florentino, L.H., Ramos, H.J., and, Fontes, E.P., (2009) Conserved threonine residues within the A-loop of the receptor NIK differentially regulate the kinase function required for antiviral signaling. PLoS ONE, 4, e5781.
42. Shah, K., Vervoort, J., and, de Vries, S.C., (2001) Role of threonines in the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phosphorylation. J. Biol. Chem. 276, 41263-41269.
43. Shiu, S.H., and, Bleecker, A.B., (2001a) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE, 2001, RE22.
44. Shiu, S.H., and, Bleecker, A.B., (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl Acad. Sci. USA, 98, 10763-10768.
45. Shiu, S.H., Karlowski, W.M., Pan, R., Tzeng, Y.H., Mayer, K.F., and, Li, W.H., (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell, 16, 1220-1234.
46. Sievers, F., Wilm, A., Dineen, D., et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539.
47. Stahl, Y., and, Simon, R., (2012) Receptor kinases in plant meristem development. In Receptor-Like Kinases in Plants: From Development to Defense (, Tax, F., and, Kemmerling, B., ed.). Berlin: Springer-Verlag, pp. 23-39.
48. Stegert, M.R., Hergovich, A., Tamaskovic, R., Bichsel, S.J., and, Hemmings, B.A., (2005) Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol. Cell. Biol. 25, 11019-11029.
49. Tor, M., Lotze, M.T., and, Holton, N., (2009) Receptor-mediated signalling in plants: molecular patterns and programmes. J. Exp. Bot. 60, 3645-3654.
50. Torii, K.U., (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int. Rev. Cytol. 234, 1-46.
51. Ubersax, J.A., and, Ferrell, J.E. Jr, (2007) Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 8, 530-541.
52. van Wijk, K.J., Friso, G., Walther, D., and, Schulze, W.X., (2014) Meta-analysis of Arabidopsis thaliana phospho-proteomics data reveals compartmentalization of phosphorylation motifs. Plant Cell, 26, 2367-2389.
53. Vert, G., Nemhauser, J.L., Geldner, N., Hong, F., and, Chory, J., (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu. Rev. Cell Dev. Biol. 21, 177-201.
54. 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.
55. 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.
56. Wu, X., Oh, M.H., Kim, H.S., Schwartz, D., Imai, B.S., Yau, P.M., Clouse, S.D., and, Huber, S.C., (2012) Transphosphorylation of E. coli proteins during production of recombinant protein kinases provides a robust system to characterize kinase specificity. Front. Plant Sci. 3, 262.
57. Xu, W.H., Wang, Y.S., Liu, G.Z., Chen, X., Tinjuangjun, P., Pi, L.Y., and, Song, W.Y., (2006) The autophosphorylated Ser686, Thr688, and Ser689 residues in the intracellular juxtamembrane domain of XA21 are implicated in stability control of rice receptor-like kinase. Plant J. 45, 740-751.
58. Yao, Q., Bollinger, C., Gao, J., Xu, D., and, Thelen, J.J., (2012) P(3)DB: an integrated database for plant protein phosphorylation. Front. Plant Sci. 3, 206.
59. Yoshida, S., and, Parniske, M., (2005) Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J. Biol. Chem. 280, 9203-9209.
60. Zhu, G., Fujii, K., Belkina, N., Liu, Y., James, M., Herrero, J., and, Shaw, S., (2005a) Exceptional disfavor for proline at the P + 1 position among AGC and CAMK kinases establishes reciprocal specificity between them and the proline-directed kinases. J. Biol. Chem. 280, 10743-10748.
61. Zhu, G., Fujii, K., Liu, Y., Codrea, V., Herrero, J., and, Shaw, S., (2005b) A single pair of acidic residues in the kinase major groove mediates strong substrate preference for P-2 or P-5 arginine in the AGC, CAMK, and STE kinase families. J. Biol. Chem. 280, 36372-36379.