Structure-function analysis of arabidopsis thaliana histidine kinase AHK5 bound to its cognate phosphotransfer protein AHP1

Molecular Plant

Volumn 6, Issue 3, 2013, Pages 959-970

  Bauer, Johannes ^a   Reiss, Kerstin ^a   Veerabagu, Manikandan ^a   Heunemann, Michael ^a   Harter, Klaus ^a   Stehle, Thilo ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

multi step phosphorelay; phosphotransfer protein; plant signaling; sensor histidine kinase; two component system

Indexed keywords

ARABIDOPSIS THALIANA; EUKARYOTA; PROKARYOTA;

EID: 84878270550     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss126     Document Type: Article

References (51)

1. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.-W., Kapral, G.J., Grosse- Kunstleve, R.W., et al. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D-Biological Crystallography. 66, 213-221.
2. Altschul, S.F., Madden, T.L., Schaeffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Andersson, K., Hamalainen, M., and Malmqvist, M. (1999). Identification and optimization of regeneration conditions for affinity-based biosensor assays: a multivariate cocktail approach. Anal. Chem. 71, 2475-2481.
4. Bahadur, R.P., and Zacharias, M. (2008). The interface of protein- protein complexes: analysis of contacts and prediction of interactions. Cellular Mol. Life Sci. 65, 1059-1072.
5. Bell, C.H., Porter, S.L., Strawson, A., Stuart, D.I., and Armitage, J.P. (2010). Using structural information to change the phosphotransfer specificity of a two-component chemotaxis signalling complex. Plos Biol. 8, e1000306.
6. Bond, C.S. (2003). TopDraw: a sketchpad for protein structure topology cartoons. Bioinformatics. 19, 311-312.
7. Capra, E.J., Perchuk, B.S., Lubin, E.A., Ashenberg, O., Skerker, J.M., and Laub, M.T. (2010). Systematic dissection and trajectory- scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. Plos Genetics. Plos Genetics, 6, doi: e1001220.
8. Deng, Y., Dong, H., Mu, J., Ren, B., Zheng, B., Ji, Z., Yang, W.-C., Liang, Y., and Zuo, J. (2010). Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell. 22, 1232-1248.
9. Desikan, R., Horak, J., Chaban, C., Mira-Rodado, V., Witthoeft, J., Elgass, K., Grefen, C., Cheung, M.-K., Meixner, A.J., Hooley, R., et al. (2008). The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. Plos One, 3, e2491.
10. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010). Features and development of Coot. Acta Crystallographica Section D-Biological Crystallography. 66, 486-501.
11. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., and Lopez, R. (2010). A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38, W695-W699.
12. Grefen, C., and Harter, K. (2004). Plant two-component systems: principles, functions, complexity and cross talk. Planta. 219, 733-742.
13. Guhaniyogi, J., Robinson, V.L., and Stock, A.M. (2006). Crystal structures of beryllium fluoride-free and beryllium fluoridebound CheY in complex with the conserved C-terminal peptide of CheZ reveal dual binding modes specific to CheY conformation. J. Mol. Biol. 359, 624-645.
14. Hass, C., Lohrmann, J., Albrecht, V., Sweere, U., Hummel, F., Yoo, S.D., Hwang, I., Zhu, T., Schafer, E., Kudla, J., et al. (2004). The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J. 23, 3290-3302.
15. Holm, L., and Rosenstrom, P. (2010). Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549.
16. Horak, J., Grefen, C., Berendzen, K.W., Hahn, A., Stierhof, Y.D., Stadelhofer, B., Stahl, M., Koncz, C., and Harter, K. (2008). The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol. 8, 77.
17. Horak, J., Janda, L., Pekarova, B., and Hejatko, J. (2011). Molecular mechanisms of signalling specificity via phosphorelay pathways in Arabidopsis. Current Protein & Peptide Science. 12, 126-136.
18. Hosoda, K., Imamura, A., Katoh, E., Hatta, T., Tachiki, M., Yamada, H., Mizuno, T., and Yamazaki, T. (2002). Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell. 14, 2015-2029.
19. Hothorn, M., Dabi, T., and Chory, J. (2011). Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nature Chemical Biology. 7, 766-768.
20. Hutchison, C.E., Li, J., Argueso, C., Gonzalez, M., Lee, E., Lewis, M.W., Maxwell, B.B., Perdue, T.D., Schaller, G.E., Alonso, J.M., et al. (2006). The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell. 18, 3073-3087.
21. Kabsch, W. (2010). XDS. Acta Crystallographica Section D-Biological Crystallography. 66, 125-132.
22. Knowles, J.R. (1980). Enzyme-catalyzed phosphoryl transfer reactions. Ann. Rev. Biochem. 49, 877-919.
23. Krissinel, E., and Henrick, K. (2007). Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
24. Langer, G., Cohen, S.X., Lamzin, V.S., and Perrakis, A. (2008). Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nature Protocols. 3, 1171-1179.
25. Laub, M.T., and Goulian, M. (2007). Specificity in two-component signal transduction pathways. In Annual Review of Genetics (Palo Alto: Annual Reviews), pp. 121-145.
26. Mahonen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Tormakangas, K., Ikeda, Y., Oka, A., Kakimoto, T., Helariutta, Y., et al. (2006). Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science. 311, 94-98.
27. Muller-Dieckmann, H.J., Grantz, A.A., and Kim, S.H. (1999). The structure of the signal receiver domain of the Arabidopsis thaliana ethylene receptor ETR1. Structure with Folding & Design. 7, 1547-1556.
28. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997). Refinement of macromolecular structures by the maximumlikelihood method. Acta Crystallographica Section D-Biological Crystallography. 53, 240-255.
29. Nishimura, C., Ohashi, Y., Sato, S., Kato, T., Tabata, S., and Ueguchi, C. (2004). Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell. 16, 1365-1377.
30. Painter, J., and Merritt, E.A. (2006). TLSMD web server for the generation of multi-group TLS models. J. Applied Crystallography. 39, 109-111.
31. Pekarova, B., Klumpler, T., Triskova, O., Horak, J., Jansen, S., Dopitova, R., Borkovcova, P., Papouskova, V., Nejedla, E., Sklenar, V., et al. (2011). Structure and binding specificity of the receiver domain of sensor histidine kinase CKI1 from Arabidopsis thaliana. Plant J. 67, 827-839.
32. Pham, J., Liu, J., Bennett, M.H., Mansfield, J.W., and Desikan, R. (2012). Arabidopsis histidine kinase 5 regulates salt sensitivity and resistance against bacterial and fungal infection. New Phytologist. 194, 168-180.
33. Pischke, M.S., Jones, L.G., Otsuga, D., Fernandez, D.E., Drews, G.N., and Sussman, M.R. (2002). An Arabidopsis histidine kinase is essential for megagametogenesis. Proc. Natl Acad. Sci. U S A. 99, 15800-15805.
34. Posas, F., WurglerMurphy, S.M., Maeda, T., Witten, E.A., Thai, T.C., and Saito, H. (1996). Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1- YPD1-SSK1 'two-component' osmosensor. Cell. 86, 865-875.
35. Schaller, G.E., Kieber, J.J., and Shiu, S.-H. (2008). Two-component signaling elements and histidyl-aspartyl phosphorelays. The Arabidopsis Book/American Society of Plant Biologists. 6, e0112.
36. Schuetze, K., Harter, K., and Chaban, C. (2009). Bimolecular fluorescence complementation (BiFC) to study protein-protein interactions in living plant cells. In Methods in Molecular Biology, Pfannschmidt, T., ed. (Totowa: Human Press Inc), pp. 189-202.
37. Skerker, J.M., Perchuk, B.S., Siryaporn, A., Lubin, E.A., Ashenberg, O., Goulian, M., and Laub, M.T. (2008). Rewiring the specificity of two-component signal transduction systems. Cell. 133, 1043-1054.
38. Sugawara, H., Kawano, Y., Hatakeyama, T., Yamaya, T., Kamiya, N., and Sakakibara, H. (2005). Crystal structure of the histidine- containing phosphotransfer protein ZmHP2 from maize. Protein Sci. 14, 202-208.
39. Tran, L.-S.P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl Acad. Sci. U S A. 104, 20623-20628.
40. Urao, T., Yakubov, B., Satoh, R., Yamaguchi-Shinozaki, K., Seki, M., Hirayama, T., and Shinozaki, K. (1999). A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell. 11, 1743-1754.
41. Varughese, K.I., Tsigelny, I., and Zhao, H.Y. (2006). The crystal structure of beryllofluoride Spo0F in complex with the phosphotransferase Spo0B represents a phosphotransfer pretransition state. J. Bacteriol. 188, 4970-4977.
42. Voinnet, O., Lederer, C., and Baulcombe, D.C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell. 103, 157-167.
43. Volz, K. (1993). Structural conservation in the CheY superfamily. Biochemistry. 32, 11741-11753.
44. Volz, K., and Matsumura, P. (1991). Crystal structure of Escherichia coli CheY refined at 1.7-A resolution. J. Biol. Chem. 266, 15511-15519.
45. Vonrhein, C., Blanc, E., Roversi, P., and Bricogne, G. (2007). Automated structure solution with autoSHARP. Methods Mol. Biol. (Clifton, NJ). 364, 215-230.
46. Walter, M., Chaban, C., Schutze, K., Batistic, O., Weckermann, K., Nake, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., et al. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438.
47. Wilson, D., Pethica, R., Zhou, Y., Talbot, C., Vogel, C., Madera, M., Chothia, C., and Gough, J. (2009). SUPERFAMILY-sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res. 37, D380-D386.
48. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G.W., McCoy, A., et al. (2011). Overview of the CCP4 suite and current developments. Acta Crystallographica Section D-Biological Crystallography. 67, 235-242.
49. Xu, Q., Porter, S.W., and West, A.H. (2003). The yeast YPD1/ SLN1 complex: insights into molecular recognition in twocomponent signaling systems. Structure (Cambridge). 11, 1569-1581.
50. Xu, Y.W., Morera, S., Janin, J., and Cherfils, J. (1997). AlF3 mimics the transition state of protein phosphorylation in the crystal structure of nucleoside diphosphate kinase and MgADP. Proc. Natl Acad. Sci. U S A. 94, 3579-3583.
51. Zhao, X., Copeland, D.M., Soares, A.S., and West, A.H. (2008). Crystal structure of a complex between the phosphorelay protein YPD1 and the response regulator domain of SLN1 bound to a phosphoryl analog. J. Mol. Biol. 375, 1141-1151.