The Arabidopsis B-type response regulator 18 homomerizes and positively regulates cytokinin responses

Plant Journal

Volumn 72, Issue 5, 2012, Pages 721-731

  Veerabagu, Manikandan ^a   Elgass, Kirstin ^a   Kirchler, Tobias ^a   Huppenberger, Peter ^a   Harter, Klaus ^a   Chaban, Christina ^a   Mira Rodado, Virtudes ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Arabidopsis thaliana; ARR18; cytokinin; DNA binding; homomerization; transcriptional activation

Indexed keywords

ARABIDOPSIS THALIANA; ARR18; CYTOKININ; DNA BINDING; HOMOMERIZATION; TRANSCRIPTIONAL ACTIVATIONS;

AMINO ACIDS; PHOSPHORYLATION; PROTEINS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; ARR18 PROTEIN, ARABIDOPSIS; ASPARTIC ACID; CYTOKININ; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION; PLANT ROOT; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASPARTIC ACID; CYTOKININS; GENE EXPRESSION REGULATION, PLANT; PHOSPHORYLATION; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; TRACHEOPHYTA;

EID: 84870064092     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05101.x     Document Type: Article

References (72)

1. Bachhawat, P., Swapna, G.V., Montelione, G.T., and, Stock, A.M., (2005) Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states. Structure, 13, 1353-1363.
2. Baikalov, I., Schroder, I., Kaczor-Grzeskowiak, M., Grzeskowiak, K., Gunsalus, R.P., and, Dickerson, R.E., (1996) Structure of the Escherichia coli response regulator NarL. Biochemistry, 35, 11053-11061.
3. Benda, C., Scheufler, C., Tandeau de Marsac, N., and, Gartner, W., (2004) Crystal structures of two cyanobacterial response regulators in apo- and phosphorylated form reveal a novel dimerization motif of phytochrome-associated response regulators. Biophys. J. 87, 476-487.
4. Bisson, M.M., Bleckmann, A., Allekotte, S., and, Groth, G., (2009) EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1. Biochem. J. 424, 1-6.
5. Brandstatter, I., and, Kieber, J.J., (1998) Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell, 10, 1009-1019.
6. Caesar, K., Elgass, K., Chen, Z., Huppenberger, P., Witthoft, J., Schleifenbaum, F., Blatt, M.R., Oecking, C., and, Harter, K., (2011a) A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. Plant J. 66, 528-540.
7. Caesar, K., Thamm, A.M.K., Witthoft, J., Elgass, K., Huppenberger, P., Grefen, C., Horak, J., and, Harter, K., (2011b) Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J. Exp. Bot. 62, 5571-5580.
8. Chen, Y.H., Birck, C., Samama, J.P., and, Hulett, F.M., (2003) Residue r113 is essential for PhoP dimerization and function: a residue buried in the asymmetric PhoP dimer interface determined in the PhoPN three-dimensional crystal structure. J. Bacteriol. 185, 262-273.
9. Cho, Y.H., and, Yoo, S.D., (2007) ETHYLENE RESPONSE 1 histidine kinase activity of Arabidopsis promotes plant growth. Plant Physiol. 143, 612-616.
10. Desikan, R., Horak, J., Chaban, C., et al. (2008) The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLoS ONE, 3, e2491.
11. Dietrich, R.A., Richberg, M.H., Schmidt, R., Dean, C., and, Dangl, J.L., (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell, 88, 685-694.
12. Dortay, H., Mehnert, N., Burkle, L., Schmulling, T., and, Heyl, A., (2006) Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana. FEBS J. 273, 4631-4644.
13. Dortay, H., Gruhn, N., Pfeifer, A., Schwerdtner, M., Schmulling, T., and, Heyl, A., (2008) Toward an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J. Proteome Res. 7, 3649-3660.
14. Ehlert, A., Weltmeier, F., Wang, X., Mayer, C.S., Smeekens, S., Vicente-Carbajosa, J., and, Droge-Laser, W., (2006) Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J. 46, 890-900.
15. Elgass, K., Caesar, K., Schleifenbaum, F., Stierhof, Y.D., Meixner, A.J., and, Harter, K., (2009) Novel application of fluorescence lifetime and fluorescence microscopy enables quantitative access to subcellular dynamics in plant cells. PLoS ONE, 4, e5716.
16. Fiedler, U., and, Weiss, V., (1995) A common switch in activation of the response regulators NtrC and PhoB: phosphorylation induces dimerization of the receiver modules. EMBO J. 14, 3696-3705.
17. Galperin, M.Y., (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188, 4169-4182.
18. Gao, R., and, Stock, A.M., (2010) Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr. Opin. Microbiol. 13, 160-167.
19. Gao, Z., Wen, C.K., Binder, B.M., Chen, Y.F., Chang, J., Chiang, Y.H., Ill, R.J.K., Chang, C., and, Schaller, G.E., (2008) Heteromeric interactions among ethylene receptors mediate signaling in Arabidopsis. J. Biol. Chem. 283, 23801-23810.
20. Geisler-Lee, J., O'Toole, N., Ammar, R., Provart, N.J., Millar, A.H., and, Geisler, M., (2007) A predicted interactome for Arabidopsis. Plant Physiol. 145, 317-329.
21. Grefen, C., and, Harter, K., (2004) Plant two-component systems: principles, functions, complexity and cross talk. Planta, 219, 733-742.
22. Grefen, C., Stadele, K., Ruzicka, K., Obrdlik, P., Harter, K., and, Horak, J., (2008) Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol. Plant, 1, 308-320.
23. Grefen, C., Obrdlik, P., and, Harter, K., (2009) The determination of protein-protein interactions by the mating-based split-ubiquitin system (mbSUS). Methods Mol. Biol. 479, 217-233.
24. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and, Blatt, M.R., (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64, 355-365.
25. Hass, C., Lohrmann, J., Albrecht, V., et al. (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J. 23, 3290-3302.
26. Hua, J., Sakai, H., Nourizadeh, S., Chen, Q.G., Bleecker, A.B., Ecker, J.R., and, Meyerowitz, E.M., (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell, 10, 1321-1332.
27. Hutchison, C.E., Li, J., Argueso, C., et al. (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell, 18, 3073-3087.
28. Hwang, I., and, Sheen, J., (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature, 413, 383-389.
29. Imamura, A., Kiba, T., Tajima, Y., Yamashino, T., and, Mizuno, T., (2003) In vivo and in vitro characterization of the ARR11 response regulator implicated in the His-to-Asp phosphorelay signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 44, 122-131.
30. Ishida, K., Yamashino, T., Yokoyama, A., and, Mizuno, T., (2008) Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol. 49, 47-57.
31. Jeon, Y., Lee, Y.S., Han, J.S., Kim, J.B., and, Hwang, D.S., (2001) Multimerization of phosphorylated and non-phosphorylated ArcA is necessary for the response regulator function of the Arc two-component signal transduction system. J. Biol. Chem. 276, 40873-40879.
32. Kaminaka, H., Nake, C., Epple, P., et al. (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 25, 4400-4411.
33. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
34. Kiba, T., Aoki, K., Sakakibara, H., and, Mizuno, T., (2004) Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the wol cytokinin-receptor mutant. Plant Cell Physiol. 45, 1063-1077.
35. Kim, J., (2008) Phosphorylation of A-Type ARR to function as negative regulator of cytokinin signal transduction. Plant Signal. Behav. 3, 348-350.
36. Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C., Sheen, J., Nam, H.G., and, Hwang, I., (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc. Natl Acad. Sci. U S A, 103, 814-819.
37. Kirby, J., and, Kavanagh, T.A., (2002) NAN fusions: a synthetic sialidase reporter gene as a sensitive and versatile partner for GUS. Plant J. 32, 391-400.
38. Kirchler, T., Briesemeister, S., Singer, M., Schutze, K., Keinath, M., Kohlbacher, O., Vicente-Carbajosa, J., Teige, M., Harter, K., and, Chaban, C., (2010) The role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors. Eur. J. Cell Biol. 89, 175-183.
39. Liang, Y., Wang, X., Hong, S., Li, Y., and, Zuo, J., (2012) Deletion of the initial 45 residues of ARR18 induces cytokinin response in Arabidopsis. J. Genet. Genomics, 39, 37-46.
40. Lohrmann, J., and, Harter, K., (2002) Plant two-component signaling systems and the role of response regulators. Plant Physiol. 128, 363-369.
41. Lohrmann, J., Buchholz, G., Keitel, C., Sweere, U., Kircher, S., Baurle, I., Kudla, J., Schafer, E., and, Harter, K., (1999) Differential expression and nuclear localization of response regulator-like proteins from Arabidopsis thaliana. Plant Biol. 1, 495-505.
42. Lohrmann, J., Sweere, U., Zabaleta, E., Baurle, I., Keitel, C., Kozma-Bognar, L., Brennicke, A., Schafer, E., Kudla, J., and, Harter, K., (2001) The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Mol. Genet. Genomics, 265, 2-13.
43. Mack, T.R., Gao, R., and, Stock, A.M., (2009) Probing the roles of the two different dimers mediated by the receiver domain of the response regulator PhoB. J. Mol. Biol. 389, 349-364.
44. Mason, M.G., Li, J., Mathews, D.E., Kieber, J.J., and, Schaller, G.E., (2004) Type-B response regulators display overlapping expression patterns in Arabidopsis. Plant Physiol. 135, 927-937.
45. Mason, M.G., Mathews, D.E., Argyros, D.A., Maxwell, B.B., Kieber, J.J., Alonso, J.M., Ecker, J.R., and, Schaller, G.E., (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell, 17, 3007-3018.
46. Mira-Rodado, V., Sweere, U., Grefen, C., Kunkel, T., Fejes, E., Nagy, F., Schafer, E., and, Harter, K., (2007) Functional cross-talk between two-component and phytochrome B signal transduction in Arabidopsis. J. Exp. Bot. 58, 2595-2607.
47. Mockli, N., Deplazes, A., Hassa, P.O., Zhang, Z., Peter, M., Hottiger, M.O., Stagljar, I., and, Auerbach, D., (2007) Yeast split-ubiquitin-based cytosolic screening system to detect interactions between transcriptionally active proteins. Biotechniques, 42, 725-730.
48. 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.
49. Nixon, B.T., Yennawar, H.P., Doucleff, M., Pelton, J.G., Wemmer, D.E., Krueger, S., and, Kondrashkina, E., (2005) SAS solution structures of the apo and Mg2+/BeF3(-)-bound receiver domain of DctD from Sinorhizobium meliloti. Biochemistry, 44, 13962-13969.
50. Park, S., Meyer, M., Jones, A.D., Yennawar, H.P., Yennawar, N.H., and, Nixon, B.T., (2002a) Two-component signaling in the AAA + ATPase DctD: binding Mg2+ and BeF3- selects between alternate dimeric states of the receiver domain. FASEB J. 16, 1964-1966.
51. Park, S., Zhang, H., Jones, A.D., and, Nixon, B.T., (2002b) Biochemical evidence for multiple dimeric states of the Sinorhizobium meliloti DctD receiver domain. Biochemistry, 41, 10934-10941.
52. 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 Phytol. 194, 168-180.
53. 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.
54. Punwani, J.A., Hutchison, C.E., Schaller, G.E., and, Kieber, J.J., (2010) The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J. 62, 473-482.
55. Rashotte, A.M., Carson, S.D., To, J.P., and, Kieber, J.J., (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 132, 1998-2011.
56. Sakai, H., Aoyama, T., and, Oka, A., (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703-711.
57. Sakai, H., Honma, T., Aoyama, T., Sato, S., Kato, T., Tabata, S., and, Oka, A., (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science, 294, 1519-1521.
58. Schaller, G.E., Kieber, J.J., and, Shin-Han, S., (2008) Two-component signaling elements and histidyl-to-aspartyl phosphorelays. Arabidopsis Book, The American Society of Plant Biologists, http://www.bioone.org/doi/full/10.1199/ tab.0112.
59. Schutze, K., Harter, K., and, Chaban, C., (2009) Bimolecular fluorescence complementation (BiFC) to study protein-protein interactions in living plant cells. Methods Mol. Biol. 479, 189-202.
60. Stock, J., and, Da Re, S., (2000) Signal transduction: response regulators on and off. Curr. Biol. 10, R420-R424.
61. Stock, J.B., Ninfa, A.J., and, Stock, A.M., (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53, 450-490.
62. Stock, A.M., Robinson, V.L., and, Goudreau, P.N., (2000) Two-component signal transduction. Annu. Rev. Biochem. 69, 183-215.
63. Suzuki, T., Imamura, A., Ueguchi, C., and, Mizuno, T., (1998) Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol. 39, 1258-1268.
64. Suzuki, T., Miwa, K., Ishikawa, K., Yamada, H., Aiba, H., and, Mizuno, T., (2001) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42, 107-113.
65. Toro-Roman, A., Wu, T., and, Stock, A.M., (2005) A common dimerization interface in bacterial response regulators KdpE and TorR. Protein Sci. 14, 3077-3088.
66. Tran, L.S., 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. USA, 104, 20623-20628.
67. Ueguchi, C., Koizumi, H., Suzuki, T., and, Mizuno, T., (2001) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42, 231-235.
68. 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.
69. Walter, M., Chaban, C., Schutze, K., et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438.
70. West, A.H., and, Stock, A.M., (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26, 369-376.
71. Wulfetange, K., Lomin, S.N., Romanov, G.A., Stolz, A., Heyl, A., and, Schmulling, T., (2011) The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 156, 1808-1818.
72. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T., and, Mizuno, T., (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017-1023.