The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein

EMBO Journal

Volumn 18, Issue 7, 1999, Pages 1996-2007

  Rodríguez Concepción, Manuel ^a   Yalovsky, Shaul ^a   Zik, Moriyah ^b   Fromm, Hillel ^b   Gruissem, Wilhelm ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Calmodulin; Isoprenoid; Membrane; Nucleus; Prenylation

Indexed keywords

CALCIUM ION; CALMODULIN; ISOPRENOID; MEMBRANE PROTEIN; MUTANT PROTEIN; NUCLEAR PROTEIN; SUGAR;

ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT; PRENYLATION; PRIORITY JOURNAL; PROTEIN PROCESSING;

EID: 0041896859     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.7.1996     Document Type: Article

References (73)

1. Ach, R.A., Taranto, P. and Gruissem, W. (1997) A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals. Plant Cell, 9, 1595-1606.
2. Alberts, A.W. et al. (1980) Mevinolin: a highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc. Natl Acad. Sci. USA, 77, 3957-3961.
3. Ames, J.B., Ishima, R., Tanaka, T., Gordon, J.I., Stryer, L. and Ikura, M. (1997) Molecular mechanics of calcium-myristoyl switches. Nature, 389, 198-202.
4. 2+-ATPases in the vacuolar and plasma membranes in cauliflower. Plant Physiol., 114, 999-1007.
5. Baum, G., Lev-Yadun, S., Fridmann, Y., Arazi, T., Katsnelson, H., Zik, M. and Fromm, H. (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J., 15, 2988-2996.
6. BoekeJ, D., Trueheart, J., Natsoulis, G. and Fink, G.R. (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol., 154, 164-175.
7. Burgess, W.H., Jemiolo, D.K. and Kretsinger, R.H. (1980) Interaction of calcium and calmodulin in the presence of sodium dodecyl sulfate. Biochim. Biophys. Acta, 623, 257-270.
8. Bush, D.S. (1995) Calcium regulation in plant cells and its role in signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol., 46, 95-122.
9. Caplin, B.E., Hettich, L.A. and Marshall, M.S. (1994) Substrate characterization of the Saccharomyces cerevisiae protein farnesyltransferase and type-I protein geranylgeranyltransferase. Biochim. Biophys. Acta, 1205, 39-48.
10. Casey, P.J., Solski, P.A., Der, C.J. and Buss, J.E. (1989) p21ras is modified by a farnesyl isoprenoid. Proc. Natl Acad. Sci. USA, 86, 8323-8327.
11. Cates, C.A., Michael, R.L., Stayrook, K.R., Harvey, K.A., Burke, Y.D., Randall, S.K., Crowell, P.L. and Crowell, D.N. (1996) Prenylation of oncogenic human PTPCAAX protein tyrosine phosphatases. Cancer Lett., 110, 49-55.
12. Chapman, J., Kavanagh, T. and Baulcombe, D. (1992) Potato virus X as a vector for gene expression in plants. Plant J., 2, 549-557.
13. Chiu, W.-L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. and Sheen, J. (1996) Engineered GFP as a vital reporter in plants. Curr. Biol., 6, 325-330.
14. Clarke, S. (1992) Protein isoprenylation and methylation at carboxy-terminal cysteine residues. Annu. Rev. Biochem., 61, 355-386.
15. Collinge, M. and Trewavas, A.J. (1989) The location of calmodulin in the pea plasma membrane. J. Biol. Chem., 264, 8865-8872.
16. Cutler, S., Ghassemian, M., Bonetta, D., Cooney, S. and McCourt, P. (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science, 273, 1239-1241.
17. Davis, T.N., Urdea, M.S., Masiarz, F.R. and Thorner, J. (1986) Isolation of the yeast calmodulin gene: calmodulin is an essential protein. Cell, 47, 423-431.
18. Deisseroth, K., Heist, E.K. and Tsien, R.W. (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature, 392, 198-202.
19. De Smedt, F., Boom, A., Pesesse, X., Schiffmann, S.N. and Emeux, C. (1996) Post-translational modification of human brain type I inositol-1,4,5-trisphosphate 5-phosphatase by farnesylation. J. Biol. Chem., 271, 10419-10424.
20. Dickinson, C.D., Altabella, T. and Chrispeels, M.J. (1991) Slow-growth phenotype of transgenic tomato expressing apoplastic invertase. Plant Physiol., 95, 420-425.
21. Finn, B.E. and Forsén, S. (1995) The evolving model of calmodulin structure, function and activation. Structure, 3, 7-11.
22. Fraichard, A., Perotti, E., Gavin, O. and Chanson, A. (1996) Subcellular localization, distribution and expression of calmodulin in Zea mays roots. Plant Sci., 118, 157-165.
23. 35S-labeled recombinant calmodulin as a probe. Plant Mol. Biol. Rep., 10, 199-206.
24. Gadbut, A.P., Wu, L., Tang, D., Papageorge, A., Watson, J.A. and Galper, J.B. (1997) Induction of the cholesterol metabolic pathway regulates the farnesylation of RAS in embryonic chick heart cells: a new role for Ras in regulating the expression of muscarinic receptors and G proteins. EMBO J., 16, 7250-7260.
25. Gelb, M. (1997) Protein prenylation, et cetera: signal transduction in two dimensions. Science, 275, 1750-1751.
26. Gillaspy, G., Ben-David, H. and Gruissem, W. (1993) Fruits: a developmental perspective. Plant Cell, 5, 1439-1451.
27. Glomset, J.A. and Farnsworth, C.C. (1994) Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu. Rev. Cell. Biol., 10, 181-205.
28. Goldstein, J.L. and Brown, M.S. (1990) Regulation of the mevalonate pathway. Nature, 343, 425-430.
29. Görlich, D. and Mattaj, W. (1996) Nucleocytoplasmic transport. Science, 271, 1513-1518.
30. Halford, N.F. and Hardie, D.G. (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol. Biol., 37, 735-748.
31. Hancock, J.F., Paterson, H. and Marshall, C.J. (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell, 63, 133-139.
32. Hancock, J.F., Cadwallader, K., Paterson, H. and Marshall, C.A. (1991) CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J., 10, 4033-4039.
33. Heineke, D., Sonnewald, U., Büssis, D., Günter, G., Leidreiter, K., Wilke, I., Raschke, K., Willmitzer, L. and Heldt, H.W. (1992) Apoplastic expression of yeast-derived invertase in potato. Plant Physiol., 100, 301-308.
34. Herbers, K., Moenke, G., Badur, R. and Sonnewald, U. (1995) A simplified procedure for the subtractive cDNA cloning of photoassimilate-responding genes: isolation of cDNAs encoding a new class of pathogenesis-related proteins. Plant Mol. Biol., 29, 1027-1038.
35. Inglese, J., Koch, W.J., Caron, M.G. and Lefkowitz, R.J. (1992a) Isoprenylation in regulation of signal transduction by G-protein-coupled receptor kinases. Nature, 359, 147-150.
36. Inglese, J., Koch, W.J., Caron, M.G. and Lefkowitz, R.J. (1992b) Isoprenylation of a protein kinase: requirement of farnesylation/ α-carboxyl methylation for full enzymatic activity of rhodopsin kinase. J. Biol. Chem., 267, 1422-1425.
37. James, G.L., Goldstein, J.L. and Brown, M.S. (1995) Polylysine and CVIM sequences of K-RasB dictate specificity of prenylation and confer resistance to benzodiazepine peptidomimetic in vitro. J. Biol. Chem., 270, 6221-6226.
38. Jelesko, J.G., Jenkins, S.M., Rodríguez-Concepción, M. and Gruissem, W. (1999) Regulation of tomato HMG1 during cell proliferation and growth. Planta, in press.
39. Jones, R.W., Jackson, A.O. and Morris, T.J. (1990) Defective-interfering RNAs and elevated temperatures inhibit replication of tomato bushy stunt virus in inoculated protoplasts. Virology, 176, 539-545.
40. Kuroda, Y., Suzuki, N. and Kataoka, T. (1993) The effect of posttranslational modifications on the interaction of Ras2 with adenylyl cyclase. Science, 259, 683-686.
41. Kurosaki, K., Kaburaki, H. and Nishi, A. (1994) Involvement of plasma membrane-located calmodulin in the response decay of cyclic nucleotide-gated cation channel of cultured carrot cells. FEBS Lett., 340, 193-196.
42. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
43. Lerchl, J., Geigenberger, P., Stitt, M. and Sonnewald, U. (1995) Impaired photoassimilate partitioning caused by phloem-specific removal of pyrophosphate can be complemented by a phloem-specific cytosolic yeast-derived invertase in transgenic plants. Plant Cell, 7, 259-270.
44. Loraine, A.E., Yalovsky, S., Fabry, S. and Gruissem, W. (1996) Tomato Rab1 A homologs as molecular tools for studying Rab geranylgeranyl transferase in plant cells. Plant Physiol., 110, 1337-1347.
45. Marshall, C.J. (1993) Protein prenylation: a mediator of protein-protein interactions. Science, 259, 1865-1866.
46. McLean, B.G., Zupan, J. and Zambryski, P.C. (1995) Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell. 7, 2101-2114.
47. Moores, S.L., Schaber, M.D., Mosser, S.D., Rands, E., O'Hara, M.B., Garsky, V.M., Marshall, M.S., Pompliano, D.L. and Gibbs, J.B. (1991) Sequence dependence of protein isoprenylation. J. Biol. Chem., 266, 14603-14610.
48. Ohto, M.A. and Nakamura, K. (1995) Sugar-induced increase of calcium-dependent protein kinases associated with the plasma membrane in leaf tissues of tobacco. Plant Physiol., 109, 973-981.
49. Pei, Z.M., Ghassemian, M., Kwak, C.M., McCourt, P. and Schroeder, J.I. (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science, 282, 287-290.
50. Pfeffer, S.R., Dirac-Svejstrup, A.B. and Soldati, T. (1995) Rab GDP dissociation inhibitor: putting Rab GTPases in the right place. J. Biol. Chem., 270, 17057-17059.
51. Porfiri, E., Evans, T., Chardin, P. and Hancock, J.F. (1994) Prenylation of ras proteins is required for efficient hSOSl-promoted guanine nucleotide exchange. J. Biol. Chem., 269, 22672-22677.
52. Qian, D., Zhou, D., Ju, R., Cramer, C.L. and Yang, Z. (1996) Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control. Plant Cell, 8, 2381-2394.
53. Riesmeier, J.W., Willmitzer, L. and Frommer, W.B. (1994) Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J., 13, 1-7.
54. Roberts, D.M., Besl, L., Oh, S.-H., Masterson, R.V., Schell, J. and Stacey, G. (1992) Expression of a calmodulin methylation mutant affects the growth and development of transgenic tobacco plants. Proc. Natl Acad. Sci. USA, 89, 8394-8398.
55. Rodríguez-Concepción, M. and Gruissem, W. (1999) Arachidonic acid alters tomato HMG expression and fruit growth, and induces HMGR-independent lycopene accumulation. Plant Physiol., 119, 41-48.
56. Rodríguez-Concepción, M., Yalovsky, S. and Gruissem, W. (1999) Protein prenylation in plants: old friends and new targets. Plant Mol. Biol., in press.
57. Sakamoto, K. and Nagatani, A. (1996) Nuclear localization activity of phytochrome B. Plant J., 10, 859-868.
58. Schafer, W.R. and Rine, J. (1992) Protein prenylation: genes, enzymes, targets and functions. Annu. Rev. Genet., 30, 209-237.
59. Smeekens, S. and Rook, F. (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol., 115, 7-13.
60. Snedden, W.A. and Fromm, H. (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci., 3, 299-304.
61. Snedden, W.A., Koutsia, N., Baum, G. and Fromm, H. (1996) Activation of a recombinant petunia glutamate decarboxylase by calcium-calmodulin or by a monoclonal antibody which recognizes the calmodulin binding domain. J. Biol. Chem., 271, 4148-4153.
62. Sonnewald, U. (1992) Expression of E.coli inorganic pyrophosphatase in transgenic plants alters photoassimilate partitioning. Plant J., 2, 571-581.
63. Szymanski, D.B., Liao, B. and Zielinski, R. (1996) Calmodulin isoforms differentially enhance the binding of cauliflower nuclear proteins and recombinant TGA3 to a region derived from the Arabidopsis Cam-3 promoter. Plant Cell, 8, 1069-1077.
64. Trainin, T., Shmuel, M. and Delmer, D.P. (1996) In vitro prenylation of the small GTPase Rac13 on cotton. Plant Physiol., 112, 1491-1497.
65. Trewavas, A.J. and Malho, R. (1997) Signal perception and transduction: the origin of the phenotype. Plant Cell, 9, 1181-1195.
66. von Schaewen, A., Stitt, M., Schmidt, R., Sonnewald, U. and Willmitzer, L. (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J., 9, 3033-3044.
67. Xu, H. and Heath, M.C. (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell, 10, 585-597.
68. Yalovsky, S., Loraine, A.E. and Gruissem, W. (1996) Specific prenylation of tomato Rab proteins by geranylgeranyl type-II transferase requires a conserved cysteine-cysteine motif. Plant Physiol., 110, 1349-1359.
69. Yalovsky, S., Trueblood, C.E., Callan, K.L., Narita, J.O., Jenkins, S.M., Rine, J. and Gruissem, W. (1997) Plant farnesyltransferase can restore yeast ras signaling and mating. Mol. Cell. Biol., 17, 1986-1994.
70. Zhang, F.L. and Casey, P.J. (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem., 65, 241-269.
71. Zhu, J.-K., Bressan, R.A. and Hasegawa, P.M. (1993) Isoprenylation of the plant molecular chaperone Anj1 facilitates membrane association and function at high temperature. Proc. Natl Acad. Sci. USA, 90, 8557-8561.
72. Zielinski, R.N. (1998) Calmodulin and calmodulin-binding proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 49, 697-725.
73. Zimmermann, S., Nürnberger, T., Frachisse, J.M., Wirtz, W., Guern, J., Hedrich, R. and Scheel, D. (1997) Receptor-mediated activation of a plant calcium-permeable ion channel involved in pathogen defense. Proc. Natl Acad. Sci. USA, 94, 2751-2755.