Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis

Plant Journal

Volumn 33, Issue 2, 2003, Pages 221-233

  Huang, Yafan ^a,c   Li, Hui ^a   Hutchison, Claire E ^b   Laskey, James ^b   Kieber, Joseph J ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

CTR1; Ethylene; Hormones; Protein kinase; Signal transduction

Indexed keywords

AMINO ACIDS; CATALYSIS; CATALYST ACTIVITY; ETHYLENE;

PROTEIN KINASES;

ENZYMES;

NASA DISCIPLINE PLANT BIOLOGY; NASA PROGRAM FUNDAMENTAL SPACE BIOLOGY; NON-NASA CENTER;

ALLELES; AMINO ACID SEQUENCE; ARABIDOPSIS; CATALYSIS; ETHYLENES; MOLECULAR SEQUENCE DATA; MUTATION; PLANT PROTEINS; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 0037266972     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01620.x     Document Type: Article

References (52)

1. Abeles, F.B., Morgan, P.W. and Saltveit, M.E., Jr (1992) Ethylene in Plant Biology, 2nd edn. San Diego, CA: Academic Press.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (eds) (1994) Current Protocols in Molecular Biology, New York: John Wiley and Sons.
3. Bleecker, A.B., Estelle, M.A., Somerville, C. and Kende, H. (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science, 241, 1086-1089.
4. Bleecker, A.B. and Kende, H. (2000) Ethylene: a gaseous signaling molecule in plants. Annu. Rev. Cell Dev. Biol. 16, 1-18.
5. Chang, C., Kwok, S.F., Bleecker, A.B. and Meyerowitz, E.M. (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science, 262, 539-544.
6. Chen, Y.-F., Randlett, M.D., Findell, J.L. and Schaller, G.E. (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J. Biol. Chem. 277, 19861-19866.
7. Chien, C.-T., Bartel, P.L., Sternglanz, R. and Fields, S. (1991) The two hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA, 88, 9578-9582.
8. Chow, Y.-H., Pumiglia, K., Jun, T.H., Dent, P., Sturgill, T.W. and Jove, R. (1995) Functional mapping of the N-terminal regulatory domain in the human Raf-1 proetin kinase. J. Biol. Chem. 270, 14100-14106.
9. Clark, K.L., Larsen, P.B., Wang, X. and Chang, C. (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl. Acad. Sci. USA, 95, 5401-5406.
10. Daum, G., Eisenmann-Tappe, I., Fries, H.-W., Troppmair, J. and Rapp, U.R. (1994) The ins and outs of Raf kinases. Trends Biochem. Sci. 19, 474-479.
11. Edwards, K., Johnstone, C. and Thompson, C. (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucl. Acids Res. 6, 1349.
12. Ferrier, A.F., Lee, M., Anderson, W.B., Benvenuto, G., Morrison, D.K., Lowy, D.R. and DeClue, J.E. (1997) Sequential modification of serines 621 and 624 in the Raf-1 carboxyl terminus produces alternations in its electrophoretic mobility. J. Biol. Chem. 272, 2136-2142.
13. Force, T., Bonventre, J.V., Heidecker, G., Rapp, U., Avruch, J. and Kyriakis, J.M. (1994) Enzymatic characteristics of the Raf-1 protein kinase. Proc. Natl. Acad. Sci. USA, 91, 1270-1274.
14. Frye, C.A., Tang, D. and Innes, R.W. (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA, 98, 373-378.
15. Galaktionov, K., Jessus, C. and Beach, D. (1995) Raf-1 interaction with Cdc25 phosphatase ties mitogenic signal transduction to cell cycle activation. Genes Dev. 9, 1046-1058.
16. Gamble, R.L., Coonfield, M.L. and Schaller, G.E. (1998) Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc. Natl. Acad. Sci. USA, 95, 7825-7829.
17. Hanks, S.K. and Quinn, A.M. (1991) Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Meth. Enzymol. 200, 38-62.
18. Harlow, E. and Lane, D. (1988) Antibodies: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Laboratory.
19. Heidecker, G., Huleihel, M., Cleveland, J.L., Kolch, W., Beck, T.W., Lloyd, P., Pawson, T. and Rapp, U.R. (1990) Mutational activation of c-Raf-1 and definition of the minimal transforming sequence. Mol. Cell Biol. 10, 2503-2512.
20. Hirayama, T., Kieber, J.J., Hirayama, N., Kogan, M., Guzman, P., Nourizadeh, S., Alonso, J.M., Dailey, W.P., Dancis, A. and Ecker, J.R. (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell, 97, 383-393.
21. Hua, J., Chang, C., Sun, Q. and Meyerowitz, E.M. (1995) Ethylene-insensitivity conferred by Arabidopsis ERS gene. Science, 269, 1712-1714.
22. Hua, J. and Meyerowitz, E.M. (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell, 94, 261-271.
23. 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.
24. Huang, Y., Li, H., Gupta, R., Morris, P.C., Luan, S. and Kieber, J.J. (2000) ATMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation. Plant Physiol. 122, 1301-1310.
25. Hüser, M., Luckett, J., Chiloeches, A., Mercer, K., Iwobi, M., Giblett, S., Sun, X.M., Brown, J., Marais, R. and Pritchrd, C. (2001) MEK kinase activity is not necessary for Raf-1 function. EMBO J. 20, 1940-1951.
26. Ichimura, K. et al. (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301-308.
27. Jouannic, S., Hamal, A., Leprince, A.S., Tregear, J.W., Kreis, M. and Henry, Y. (1999) Characterization of novel plant genes encoding MEKK/STE11 and RAF-related protein kinases. Gene, 229, 171-181.
28. Kieber, J.J., Rothenburg, M., Roman, G., Feldmann, K.A. and Ecker, J.R. (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis encodes a member of the Raf family of protein kinases. Cell, 72, 427-441.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
30. Leevers, S.J., Paterson, H.F. and Marshall, C.J. (1994) Recruitment for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature, 9, 411-414.
31. Lewis, T.S., Shapiro, P.S. and Ahn, N.G. (1998) Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74, 49-139.
32. Lin, J.H., Makris, A., McMahon, C., Bear, S.E., Patriotis, C., Prasad, V.R., Brent, R., Golemis, E.A. and Tsichlis, P.N. (1999) The ankyrin repeat containing adaptor protein Tvl-1 is a novel substrate and regulator of Raf-1. J. Biol. Chem. 274, 14706-14715.
33. Morris, P.C., Guerrier, D., Leung, J. and Giraudat, J. (1997) Cloning and characterization of MEK1, an Arabidopsis gene encoding a homologue of MAP kinase kinase. Plant Mol. Biol. 35, 1057-1064.
34. Morrison, D.K. and Cutler, R.E., Jr. (1997) The complexity of Raf-1 regulation. Curr. Opin. Cell Biol. 9, 174-179.
35. Pallin, J.B., Woeste, K.E. and Kieber, J.J. (1996) Role of the CTR1 kinase in ethylene signal transduction in Arabidopsis. In Protein Phosphorylation in Plants (Shewry, P.R., Halford, N.G. and Hooley, R., eds). Oxford: Clarendon Press, pp. 255-265.
36. Pan, Z. and Chang, C. (1999) Functional complementation of the Schizosaccharomyces pombe wis1 mutant by Arabidopsis MEK1 and non-catalytic enhancement by CTR1. FEBS Lett. 459, 405-410.
37. Peyssonnaux, C. and Eychene, A. (2001) The Raf/MEK/ERK pathway: new concepts of activation. Biol. Cell, 93, 53-62.
38. Rapp, U.R., Goldsborough, M.D., Mark, M.D., Bonner, T.I., Groffen, J., Reynolds, F.H.J. and Stephenson, J.R. (1983) Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc. Natl. Acad. Sci. USA, 80, 4218-4222.
39. Rodriguez, F.I., Esch, J.J., Hall, A.E., Binder, B.M., Schaller, E.G. and Bleecker, A.B. (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science, 283, 396-398.
40. Sakai, H., Hua, J., Chen, Q.G., Chang, C., Medrano, L.J., Bleecker, A.B. and Meyerowitz, E.M. (1998) ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA, 95, 5812-5817.
41. Schaller, G.E. and Bleecker, A.B. (1995) Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science, 270, 1809-1811.
42. Schaller, G.E. and Kieber, J.J. (2002) Ethylene. In The Arabidopsis Book (Somerville, C.R. and Meyerowitz, E.M., eds). Rockville, MD: American Society of Plant Physiologists. DOI/10.1199/tab.0071. http://www.aspb.org.
43. Schaller, G.E., Ladd, A.N., Lanahan, M.B., Spanbauer, J.M. and Bleecker, A.B. (1995) The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer. J. Biol. Chem. 270, 12526-12530.
44. Schiestl, R.H. and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16, 339-346.
45. Stanton, V.P., Jr, Nichols, D.W., Laudano, A.P. and Cooper, G.M. (1989) Definition of the human Raf amino-terminal regulatory region by deletion mutagenesis. Mol. Cell Biol. 9, 639-647.
46. Stepanova, A.N. and Ecker, J.R. (2000) Ethylene signaling: from mutants to molecules. Curr. Opin. Plant Biol. 3, 353-360.
47. Stokoe, D., Macdonald, S.G., Cadwallader, K., Symons, M. and Hancock, J.F. (1994) Activation of Raf as a result of recruitment to the plasma membrane. Science, 26, 1463-1467.
48. Summers, M.D. and Smith, G. (1987) A Manual of Methods for Baculovirus Vector and Insect Cell Culture Procedures. College Station, TX: Texas Agricultural Experimental Station.
49. Tena, G., Asai, T., Chiu, W.-L. and Sheen, J. (2001) Plant mitogen-activated protein kinase signaling cascades. Curr. Opin. Plant Biol. 4, 392-400.
50. Vogel, J.P., Woeste, K.W., Theologis, A. and Kieber, J.J. (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl. Acad. Sci. USA, 95, 4766-4771.
51. Vojtek, A.B., Hollenberg, S.M. and Cooper, J.A. (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell, 74, 205-214.
52. Woeste, K. and Kieber, J.J. (2000) A strong loss-of-function allele of RAN1 results in constitutive activation of ethylene responses as well as a rosette-lethal phenotype. Plant Cell, 12, 443-455.