Cytokinin signaling stabilizes the response activator ARR1

Plant Journal

Volumn 78, Issue 1, 2014, Pages 157-168

  Kurepa, Jasmina ^a   Li, Yan ^a,b   Smalle, Jan A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

26S proteasome; Arabidopsis thaliana; ARR1; cytokinin signaling; protein degradation

Indexed keywords

CHEMICAL ACTIVATION; GENE EXPRESSION; PLANTS (BOTANY);

26 S PROTEASOME; ARABIDOPSIS THALIANA; ARR1; ENVIRONMENTAL RESPONSE; PROTEIN DEGRADATION; REGULATORY MECHANISM; RESPONSE REGULATORS; TRANSCRIPTIONAL ACTIVATORS;

SIGNALING;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; TRACHEOPHYTA;

ARABIDOPSIS PROTEIN; ARR1 PROTEIN, ARABIDOPSIS; ATP DEPENDENT 26S PROTEASE; CYTOKININ; DNA BINDING PROTEIN; PROTEASOME; TRANSCRIPTION FACTOR;

ARABIDOPSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT ROOT; PROMOTER REGION; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOKININS; DNA-BINDING PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; MUTATION; PHENOTYPE; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; SEEDLING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84897420846     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12458     Document Type: Article

References (68)

1. Argyros, R.D., Mathews, D.E., Chiang, Y.H., Palmer, C.M., Thibault, D.M., Etheridge, N., Argyros, D.A., Mason, M.G., Kieber, J.J., and, Schaller, G.E., (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell, 20, 2102-2116.
2. Bhargava, A., Clabaugh, I., To, J.P., Maxwell, B.B., Chiang, Y.H., Schaller, G.E., Loraine, A., and, Kieber, J.J., (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 162, 272-294.
3. 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.
4. Brenner, W.G., Romanov, G.A., Köllmer, I., Burkle, L., and, Schmulling, T., (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J. 44, 314-333.
5. Brown, M.C., Joaquim, T.R., Chambers, R., et al. (2011) Impact of immunization technology and assay application on antibody performance-a systematic comparative evaluation. PLoS ONE, 6, e28718.
6. Brunelle, M., Fayad, T., and, Langlois, M.F., (2011) Degradation of thyroid hormone receptor beta 1: existence of stable and unstable forms. Thyroid, 21, 311-318.
7. Met30 is the rate-limiting regulatory step in degradation of polyubiquitinated Met4. Mol. Cell, 24, 689-699.
8. Choi, J., Huh, S.U., Kojima, M., Sakakibara, H., Paek, K.H., and, Hwang, I., (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev. Cell, 19, 284-295.
9. D'Agostino, I., Deruère, J., and, Kieber, J., (2000) Characterization of the response of the Arabidopsis ARR gene family to cytokinin. Plant Physiol. 124, 1706-1717.
10. Dietz, K.J., and, Herth, S., (2011) Plant nanotoxicology. Trends Plant Sci. 16, 582-589.
11. Dreher, K., and, Callis, J., (2007) Ubiquitin, hormones and biotic stress in plants. Ann. Bot. 99, 787-822.
12. Fowler, T., Sen, R., and, Roy, A.L., (2011) Regulation of primary response genes. Mol. Cell, 44, 348-360.
13. Glickman, M.H., and, Ciechanover, A., (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373-428.
14. van der Graaff, E.E., Hooykaas, P.J.J., and, Auer, C.A., (2001) Altered development of Arabidopsis thaliana carrying the Agrobacterium tumefaciens ipt gene is partially due to ethylene effects. Plant Growth Regul. 34, 305-315.
15. Gruhn, N., and, Heyl, A., (2013) Updates on the model and the evolution of cytokinin signaling. Curr. Opin. Plant Biol. 16, 569-574.
16. Gupta, S., and, Rashotte, A.M., (2012) Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep. 31, 801-812.
17. Hill, K., Mathews, D.E., Kim, H.J., et al. (2013) Functional characterization of type-B response regulators in the Arabidopsis cytokinin response. Plant Physiol. 162, 212-224.
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. Hoth, S., Ikeda, Y., Morgante, M., Wang, X., Zuo, J., Hanafey, M.K., Gaasterland, T., Tingey, S.V., and, Chua, N.H., (2003) Monitoring genome-wide changes in gene expression in response to endogenous cytokinin reveals targets in Arabidopsis thaliana. FEBS Lett. 554, 373-380.
20. 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.
21. Hwang, I., and, Sheen, J., (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature, 413, 383-389.
22. Imamura, A., Hanaki, N., Umeda, H., Nakamura, A., Suzuki, T., Ueguchi, C., and, Mizuno, T., (1998) Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc. Natl Acad. Sci. USA, 95, 2691-2696.
23. Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Taniguchi, M., Kiba, T., Ueguchi, C., Sugiyama, T., and, Mizuno, T., (1999) Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 40, 733-742.
24. 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.
25. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., and, Kakimoto, T., (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature, 409, 1060-1063.
26. 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.
27. Kelley, D.R., and, Estelle, M., (2012) Ubiquitin-mediated control of plant hormone signaling. Plant Physiol. 160, 47-55.
28. Kiba, T., Naitou, T., Koizumi, N., Yamashino, T., Sakakibara, H., and, Mizuno, T., (2005) Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His -> Asp phosphorelay circuitry. Plant Cell Physiol. 46, 339-355.
29. 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. USA, 103, 814-819.
30. Kim, K., Ryu, H., Cho, Y.H., Scacchi, E., Sabatini, S., and, Hwang, I., (2012) Cytokinin-facilitated proteolysis of Arabidopsis response regulator 2 attenuates signaling output in two-component circuitry. Plant J. 69, 934-945.
31. KMD controls cytokinin signaling by regulating the degradation of type-B response regulators. Proc. Natl Acad. Sci. USA 110, 10028-10033.
32. Kurepa, J., and, Smalle, J.A., (2011) Assaying transcription factor stability. Methods Mol. Biol. 754, 219-234.
33. Kurepa, J., A.,and, Smalle, J.A., (2008) 26S proteasome regulatory particle mutants have increased oxidative stress tolerance. Plant J. 53, 102-114.
34. Kurepa, J., Li, Y., and, Smalle, J.A., (2013a) Proteasome-dependent proteolysis has a critical role in fine-tuning the feedback inhibition of cytokinin signaling. Plant Signal. Behav. 8, e23474.
35. Kurepa, J., Li, Y., and, Smalle, J.A., (2013b) Reversion of the Arabidopsis rpn12a-1 exon-trap mutation by an intragenic suppressor that weakens the chimeric 5' splice site [v2; ref status: indexed}. F1000 Res. 2, 60.
36. Li, Y., Kurepa, J., and, Smalle, J., (2013) AXR1 promotes the Arabidopsis cytokinin response by facilitating ARR5 proteolysis. Plant J. 74, 13-24.
37. 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.
38. Lipford, J.R., and, Deshaies, R.J., (2003) Diverse roles for ubiquitin-dependent proteolysis in transcriptional activation. Nat. Cell Biol. 5, 845-850.
39. Lohrmann, J., Sweere, U., Zabaleta, E., Bäurle, I., Keitel, C., Kozma-Bognar, L., Brennicke, A., Schäfer, 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.
40. Mähönen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Törmäkangas, K., Ikeda, Y., Oka, A., Kakimoto, T., and, Helariutta, Y., (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science, 311, 94-98.
41. 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.
42. 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.
43. Muratani, M., and, Tansey, W.P., (2003) How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4, 192-201.
44. 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.
45. Ramakers, C., Ruijter, J.M., Deprez, R.H., and, Moorman, A.F., (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66.
46. 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.
47. Ren, B., Liang, Y., Deng, Y., Chen, Q., Zhang, J., Yang, X., and, Zuo, J., (2009) Genome-wide comparative analysis of type-A Arabidopsis response regulator genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res. 19, 1178-1190.
48. Ruijter, J.M., Ramakers, C., Hoogaars, W.M., Karlen, Y., Bakker, O., van den Hoff, M.J., and, Moorman, A.F., (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37, e45.
49. Ryu, M.Y., Cho, S.K., and, Kim, W.T., (2009) RNAi suppression of RPN12a decreases the expression of type-A ARRs, negative regulators of cytokinin signaling pathway, in Arabidopsis. Mol. Cells, 28, 375-382.
50. Sadanandom, A., Bailey, M., Ewan, R., Lee, J., and, Nelis, S., (2012) The ubiquitin-proteasome system: central modifier of plant signalling. New Phytol. 196, 13-28.
51. Sakai, H., Aoyama, T., and, Oka, A., (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703-711.
52. 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.
53. Schubert, U., Anton, L., Gibbs, J., Norbury, C., Yewdell, J., and, Bennink, J., (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature, 404, 770-774.
54. Shi, X., and, Rashotte, A.M., (2012) Advances in upstream players of cytokinin phosphorelay: receptors and histidine phosphotransfer proteins. Plant Cell Rep. 31, 789-799.
55. Smalle, J., and, Vierstra, R.D., (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590.
56. Smalle, J., Kurepa, J., Yang, P., Babiychuk, E., Kushnir, S., Durski, A., and, Vierstra, R.D., (2002) Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12. Plant Cell, 14, 17-32.
57. Smalle, J., Kurepa, J., Yang, P., Emborg, T.J., Babiychuk, E., Kushnir, S., and, Vierstra, R.D., (2003) The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell, 15, 965-980.
58. Stone, S.L., and, Callis, J., (2007) Ubiquitin ligases mediate growth and development by promoting protein death. Curr. Opin. Plant Biol. 10, 624-632.
59. Suzuki, T., Sakurai, K., Imamura, A., Nakamura, A., Ueguchi, C., and, Mizuno, T., (2000) Compilation and characterization of histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 64, 2486-2489.
60. 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.
61. Taniguchi, M., Sasaki, N., Tsuge, T., Aoyama, T., and, Oka, A., (2007) ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol. 48, 263-277.
62. To, J., Haberer, G., Ferreira, F., Deruere, J., Mason, M., Schaller, G., Alonso, J., Ecker, J., and, Kieber, J., (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell, 16, 658-671.
63. To, J.P.C., Deruere, J., Maxwell, B.B., Morris, V.F., Hutchison, C.E., Ferreira, F.J., Schaller, G.E., and, Kieber, J.J., (2007) Cytokinin regulates type-A Arabidopsis response regulator activity and protein stability via two-component phosphorelay. Plant Cell, 19, 3901-3914.
64. Tworkowski, K.A., Salghetti, S.E., and, Tansey, W.P., (2002) Stable and unstable pools of Myc protein exist in human cells. Oncogene, 21, 8515-8520.
65. 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.
66. Wang, S., Kurepa, J., and, Smalle, J.A., (2009) The Arabidopsis 26S proteasome subunit RPN1a is required for optimal plant growth and stress responses. Plant Cell Physiol. 50, 1721-1725.
67. 2 nanoparticles disrupt microtubular networks in Arabidopsis thaliana. Plant Cell Environ. 34, 811-820.
68. 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.