Protein kinases in plants in the transduction of abiotic and biotic signals

Russian Journal of Plant Physiology

Volumn 49, Issue 1, 2002, Pages 107-119

  Hall, M A ^a   Novikova, G V ^b   Moshkov, I E ^b   Mur, L A J ^a   Smith, A R ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

Author keywords

Abiotic and biotic stresses; Monomeric G proteins; Protein kinases; Signal transduction

Indexed keywords

EID: 0036111312     PISSN: 10214437     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1013724614446     Document Type: Article

References (108)

1. Cohen, P., Hormones, Second Messengers and the Reversible Phosphorylation of Proteins, BioEssay, 1985, vol. 2, pp. 63-67.
2. Hunter, T., A Thousand and One Protein Kinases, Cell, 1987, vol. 50, pp. 823-829.
3. Hunter, T., Protein Kinases and Phosphatases: The Yin and Yang of Protein Phosphorylation and Signaling, Cell, 1995, vol. 80, pp. 225-236.
4. Hunter, T., Oncoprotein Networks, Cell, 1997, vol. 88, pp. 333-346.
5. Dickens, M., Rogers, J.S., Cavanagh, J., Raitano, A., Xia, Z.G., Halpern, J.R., Greenberg, M.E., Sawyers, C.L., and Davis, R.J., A Cytoplasmic Inhibitor of the JNK Signal Transduction Pathway, Science, 1997, vol. 277, pp. 693-696.
6. Schaeffer, H.J., Catling, A.D., Eblen, S.T., Collier, L.S., Krause, A., and Weber, M.J., MP1: A MEK Binding Partner that Enhances Enzymatic Activation of the MAP Kinase Cascade, Science, 1998, vol. 281, pp. 1668-1671.
7. Choi, K.-Y., Satterberg, B., Lyons, D.M., and Elion, E.A., Ste5 Tethers Multiple Protein Kinases in the MAP Kinase Cascade Required for Mating in S. cerevisiae, Cell, 1994, vol. 78, pp. 499-512.
8. Marcus, S., Polverino, A., Barr, M., and Wigler, M., Complexes between STE5 and Components of the Pheromone-Responsive Mitogen-Activated Protein Kinase Module, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 7762-7766.
9. Treisman, R., Regulation of Transcription by MAP Kinase Cascades, Curr. Opin. Cell Biol., 1996, vol. 8, pp. 205-215.
10. Marshall, C.J., Specificity of Receptor Tyrosine Kinase Signaling: Transient versus Sustained Extracellular Signal-Regulated Kinase Activation, Cell, 1995, vol. 80, pp. 179-185.
11. Proud, C.G., Translation: Turned on by Insulin, Nature, 1994, vol. 371, pp. 747-748.
12. Sturgill, T.W., Ray, L.B., Erickson, E., and Maller, J.L., Insulin-Stimulated MAP-2 Kinase Phosphorylates and Activates Ribosomal Protein S6 Kinase-II, Nature, 1988, vol. 334, pp. 715-718.
13. Haycock, J.W., Ahn, N.G., Cobb, M.H., and Krebs, E.G., ERK1 and ERK2, Two Microtubule-Associated Protein 2 Kinases, Mediate the Phosphorylation of Tyrosine Hydroxylase at Serine-31 in situ, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 2365-2369.
14. Lin, L.L., Wartmann, M., Lin, A.Y., Knopf, J.L., Seth, A., and Davis, R.J., CPLA2 Is Phosphorylated and Activated by MAP Kinase, Cell, 1993, vol. 72, pp. 269-278.
15. Peraldi, P., Zhao, Z.H., Filloux, C., Fisher, E.H., and Vanobberghen, E., Protein Tyrosine Phosphatase 2C Is Phosphorylated and Inhibited by 44-kDa Mitogen-Activated Protein Kinase, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 5002-5006.
16. Halloran, S.M. and Vulliet, P.R., Microtubule-Associated Protein Kinase 2 Phosphorylates and Activates Tyrosine Hydroxylase Following Depolarization of Bovine Adrenal Chromaffin Cells, J. Biol. Chem., 1994, vol. 269, pp. 30960-30965.
17. Ray, L.B. and Sturgill, T.W., Rapid Stimulation by Insulin of a Serine Threonine Kinase in 3T3-L1 Adipocytes that Phosphorylates Microtubule-Associated Protein 2 in vitro, Proc. Natl. Acad. Sci. USA, 1987, vol. 84, pp. 1502-1506.
18. Erickson, A.K., Payne, D.M., Martino, P.A., Rossomando, A.J., Shabanowitz, J., Weber, M.J., Hunt, D.F., and Sturgill, T.W., Identification by Mass Spectrometry of Threonine-97 in Bovine Myelin Basic Protein as a Specific Phosphorylation Site for Mitogen-Activated Protein Kinase, J. Biol. Chem., 1990, vol. 265, pp. 19728-19735.
19. Reszka, A.A., Seger, R., Diltz, C.D., Krebs, E.G., and Fisher, E.H., Association of Mitogen-Activated Protein Kinase with the Microtubule Cytoskeleton, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 8881-8885.
20. Cohen, P., The Search for Physiological Substrates of MAP and SAP Kinases in Mammalian Cells, Trends Cell Biol., 1997, vol. 7, pp. 353-361.
21. Lu, Q., Paredes, M., Zhang, J., and Kosik, K.S., Basal Extracellular Signal-Regulated Kinase Activity Modulates Cell-Cell and Cell-Matrix Interactions, Mol. Cell. Biol., 1998, vol. 18, pp. 3257-3265.
22. Waskiewicz, A.J. and Cooper, J., Mitogen and Stress Response Pathways, MAP Kinase Cascades and Phosphatase Regulation in Mammals and Yeast, Curr. Opin. Cell Biol., 1995, vol. 7, pp. 798-802.
23. Brewster, J.L., deValoir, T., Dwyer, N.D., Winter, E., and Gustin, M.C., An Osmosensing Signal Transduction Pathway in Yeast, Science, 1993, vol. 259, pp. 1760-1763.
24. Galcheva-Gargova, Z., Derijard, B., Wu, I., and Davis, R., An Osmosensing Signal Transduction Pathway in Mammalian Cells, Science, 1994, vol. 265, pp. 806-808.
25. Han, J., Lee, J.-D., Bibbs, L., and Ulevitch, R.J., A MAP Kinase Targeted by Endotoxin and Hyperosmolarity in Mammalian Cells, Science, 1994, vol. 265, pp. 808-811.
26. Lewis, T.S., Shapiro, P.S., and Ahn, N.G., Signal Transduction through MAP Kinase Cascades, Adv. Cancer Res., 1998, vol. 74, pp. 49-139.
27. Widmann, C., Gibson, S., Jarpe, M.B., and Johnson, G.L., Mitogen-Activated Protein Kinase: Conservation of a Three-Kinase Module from Yeast to Human, Physiol. Rev., 1999, vol. 79, pp. 143-180.
28. Anderson, N.G., Ping, L.I., Marsden, L.A., Williams, N., Roberts, T.M., and Sturgill, T.W., Raf-1 Is a Potential Substrate for Mitogen-Activated Protein Kinase in vivo, Biochem. J., 1991, vol. 277, pp. 573-576.
29. Brunet, A., Pages, G., and Pouyssegur, J., Growth Factor-Stimulated MAP Kinase Induces Rapid Retrophosphorylation and Inhibition of MAP Kinase Kinase (MEK1), FEBS Lett., 1994, vol. 346, pp. 299-303.
30. Saito, Y., Gomez, N., Campbell, D.G., Ashworth, A., Marshall, C.J., and Cohen, P., The Threonine Residues in MAP Kinase Kinase 1 Phosphorylated by MAP Kinase in vitro Are Also Phosphorylated in Nerve Growth Factor-Stimulated Rat Pheochromocytoma (PC12) Cells, FEBS Lett., 1994, vol. 341, pp. 119-124.
31. Cherniack, A.D., Klarlund, J.K., and Czech, M.P., Phosphorylation of the Ras Nucleotide Exchange Factor Son of Sevenless by Mitogen-Activated Protein Kinase, J. Biol. Chem., 1994, vol. 269, pp. 4717-4720.
32. Buday, L., Warne, P.H., and Downward, J., Down-Regulation of the Ras Activation Pathway by MAP Kinase Phosphorylation of Sos, Oncogene, 1995, vol. 11, pp. 1327-1331.
33. Rozakis-Adcock, M., van der Geer, P., Mbamalu, G., and Pawson, T., MAP Kinase Phosphorylation of MSOS1 Promotes Dissociation of MSOS1-SHC and MSOS1-EGF Receptor Complexes, Oncogene, 1995, vol. 11, pp. 1417-1426.
34. Chen, D., Waters, S.B., Holt, K.H., and Pessin, J.E., SOS Phosphorylation and Disassociation of the Grb2-SOS Complex by the ERK and JNK Signaling Pathways, J. Biol. Chem., 1996, vol. 271, pp. 6328-6332.
35. Holt, K.H., Kasson, B.G., and Pessin, J.E., Insulin Stimulation of a MEK-Dependent but ERK-Independent SOS Protein Kinase, Mol. Cell Biol., 1996, vol. 16, pp. 577-583.
36. Waters, S.B., Holt, K.H., Ross, S.E., Syu, L.J., Guan, K.L., Saltiel, A.R., Koretzky, G.A., and Pessin, J.E., Desensitization of Ras Activation by a Feedback Dissociation of the SOS-Grb2 Complex, J. Biol. Chem., 1995, vol. 270, pp. 20883-20886.
37. Ferrell, J.E., Jr., Tripping the Switch Fantastic: How a Protein Kinase Cascade Can Convert Graded Inputs into Switch-Like Outputs, Trends Biochem. Sci., 1996, vol. 21, pp. 460-466.
38. Keyse, S.M., Protein Phosphatases and the Regulation of MAP Kinase Activity, Semin. Cell Dev. Biol., 1998, vol. 9, pp. 143-152.
39. Chant, J. and Stowers, L., GTPase Cascades Choreographing Cellular Behavior: Movement, Morphogenesis and More, Cell, 1995, vol. 81, pp. 1-4.
40. Denhardt, D.T., Signal Transduction Protein Phosphorylation Cascades Mediated by Ras/Rho Proteins in the Mammalian Cell: The Potential for Multiplex Signalling, Biochem. J., 1996, vol. 318, pp. 729-747.
41. Kovtun, Y., Chiu, W.-L., Tena, G., and Sheen, J., Functional Analysis of Oxidative Stress-Activated Mitogen-Activated Protein Kinase Cascade in Plants, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 2940-2945.
42. Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., Yamaguchi-Shinozaki, K., Masumoto, K., and Shinozaki, K., A Gene Encoding a Mitogen-Activated Protein Kinase Kinase Kinase Is Induced Simultaneously with a Gene for a Mitogen-Activated Protein Kinase and S6 Ribosomal Protein Kinase by Touch, Cold, and Water Stress in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 763-769.
43. Jonak, C., Kiegerl, S., Ligterink, W., Barker, P.J., Huskisson, N.S., and Hirt, H., Stress Signaling in Plants: A Mitogen-Activated Protein Kinase Pathway Is Activated by Cold and Drought, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 11274-11279.
44. Wilson, C., Voronin, V., Touraev, A., Vicente, O., and Heberle-Bors, E., A Developmentally Regulated MAP Kinase Activated by Hydration in Tobacco Pollen, Plant Cell, 1997, vol. 9, pp. 2093-2100.
45. Cazalé, A.-C., Rouet-Mayer, M.-A., Barbier-Brygoo, H., Mathien, Y., and Lauriére, C., Oxidative Burst and Hypoosmotic Stress in Tobacco Cell Suspensions, Plant Physiol., 1998, vol. 116, pp. 659-669.
46. Cazalé, A.-C., Droillard, M.-J., Wilson, C., Heberle-Bors, E., Barbier-Brygoo, H., and Lauriére, C., MAP Kinase Activation by Hypoosmotic Stress of Tobacco Cell Suspensions: Towards the Oxidative Burst Response? Plant J., 1999, vol. 19, pp. 297-307.
47. Börge, L., Ligterink, W., Heberle-Bors, E., and Hirt, H., Mechanosensors in Plants, Nature, 1996, vol. 383, pp. 489-490.
48. Mikolajczyk, M., Awotunde, O.S., Muszyńska, G., Klessig, D., and Dobrowolska, G., Osmotic Stress Induces Rapid Activation of a Salicylic Acid-Induced Protein Kinase and a Homolog of Protein Kinase ASK1 in Tobacco Cells, Plant Cell, 2000, vol. 12, pp. 165-178.
49. Usami, S., Banno, H., Ito, Y., Nishihama, R., and Machida, Y., Cutting Activates a 46-Kilodalton Protein Kinase in Plants, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 8660-8664.
50. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., and Ohashi, Y., Tobacco MAP Kinase: A Possible Mediator in Wound Signal Transduction Pathways, Science, 1995, vol. 270, pp. 1988-1992.
51. Bögre, L., Ligterink, W., Meskiene, I., Barker, P.J., Heberle-Bors, E., Huskisson, N.S., and Hirt, H., Wounding Induces the Rapid and Transient Activation of a Specific MAP Kinase Pathway, Plant Cell, 1997, vol. 9, pp. 75-83.
52. Meskiene, I., Bögre, L., Glaser, W., Balog, J., Brandstötter, M., Zwerger, K., Ammerer, G., and Hirt, H., MP2C, a Plant Protein Phosphatase 2C, Functions as a Negative Regulator of Mitogen-Activated Protein Kinase Pathways in Yeast and Plants, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 1938-1943.
53. Seo, S., Sano, H., and Ohashi, Y., Jasmonate-Based Wound Signal Transduction Requires Activation of WIPK, a Tobacco Mitogen-Activated Protein Kinase, Plant Cell, 1999, vol. 11, pp. 289-298.
54. Suzuki, K. and Shinshi, H., Transient Activation and Tyrosine Phosphorylation of a Protein Kinase in Tobacco Cells Treated with a Fungal Elicitor, Plant Cell, 1995, vol. 7, pp. 639-647.
55. Ligterink, W., Kroj, T., zur Nieden, U., Hirt, H., and Scheel, D., Receptor-Mediated Activation of a MAP Kinase in Pathogen Defense of Plants, Science, 1997, vol. 276, pp. 2054-2057.
56. Stratmann, J.W. and Ryan, C.A., Myelin Basic Protein Kinase Activity in Tomato Leaves Is Induced Systemically by Wounding and Increases in Response to Systemin and Oligosaccharide Elicitors, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 11085-11089.
57. Lebrun-Garsia, A., Ouaked, F., Chiltz, A., and Pugin, A., Activation of MAPK Homologues by Elicitors in Tobacco Cells, Plant J., 1998, vol. 15, pp. 773-781.
58. Zhang, S. and Klessig, D.F., Salicylic Acid Activates a 48-kD MAP Kinase in Tobacco, Plant Cell, 1997, vol. 9, pp. 809-824.
59. Zhang, S., Du, H., and Klessig, D.F., Activation of the Tobacco SIP Kinase by Both a Cell Wall-Derived Carbohydrate Elicitor and Purified Proteinaceous Elicitor from Phytophthora spp., Plant Cell, 1998, vol. 10, pp. 435-449.
60. Zhang, S. and Klessig, D.F., The Tobacco Wounding-Activated Mitogen-Activated Protein Kinase Is Encoded by SIPK, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 7225-7230.
61. Zhang, S. and Klessig, D.F., Resistance Gene N-Mediated de novo Synthesis and Activation of a Tobacco Mitogen-Activated Protein Kinase by Tobacco Mosaic Virus Infection, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 7433-7438.
62. Lee, S.H., Lee, M.H., Chung, W.I., and Liu, J.R., WAPK, a Ser/Thr Protein Kinase Gene of Nicotiana tabacum, Is Uniquely Regulated by Wounding, Abscisic Acid and Methyl Jasmonate, Mol. Gen. Genet., 1998, vol. 259, pp. 516-522.
63. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H., and Jones, J.D.G., Rapid Avr9- and Cf-9-Dependent Activation of MAP Kinases in Tobacco Cell Cultures and Leaves: Convergence of Resistance Gene, Elicitor, Wound, and Salicylate Responses, Plant Cell, 1999, vol. 11, pp. 273-287.
64. Rajasekhar, V.K., Lamb, C., and Dixon, R.A., Early Events in the Signal Pathway for the Oxidative Burst in Soybean Cell Exposed to Avirulent Pseudomonas syringae pv. glycinea, Plant Physiol., 1999, vol. 120, pp. 1137-1146.
65. 2 Activates a MAP Kinase-Like Enzyme in Arabidopsis thaliana Suspension Cultures, J. Exp. Bot., 1999, vol. 50, pp. 1863-1866.
66. Kumar, D. and Klessig, D.F., Differential Induction of Tobacco MAP Kinases by the Defense Signals Nitric Oxide, Salicylic Acid, Ethylene, and Jasmonic Acid, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 347-351.
67. Raz, V. and Fluhr, R., Calcium Requirement for Ethylene-Dependent Responses, Plant Cell, 1992, vol. 4, pp. 1123-1130.
68. Raz, V. and Fluhr, R., Ethylene Signal Is Transduced via Protein Phosphorylation Events in Plants, Plant Cell, 1993, vol. 5, pp. 523-530.
69. Novikova, G.V., Moshkov, I.E., Smith, A.R., and Hall, M.A., Ethylene and Phosphorylation of Pea Epicotyl Proteins, Cellular and Molecular Aspects of the Plant Hormone Ethylene, Peche, J.C., Lataché, A., and Balagué, C., Eds., Dordrecht: Kluwer, 1993, pp. 371-372.
70. He, C.-J., Morgan, P.W., and Drew, M.C., Transduction of the Ethylene Signal Is Required for Cell Death and Lysis in the Root Cortex of Maize during Aerenchyma Formation Induced by Hypoxia, Plant Physiol., 1996, vol. 112, pp. 463-472.
71. Novikova, G.V., Moshkov, I.E., Smith, A.R., Kulaeva, O.N., and Hall, M.A., The Effect of Ethylene and Cytokinin on Guanosine 5′-Triphosphate Binding and Protein Phosphorylation in Leaves of Arabidopsis thaliana, Planta, 1999, vol. 208, pp. 239-246.
72. Kieber, J.J., Rothenberg, M., Roman, G., Feldman, K.A., and Ecker, J.R., CTR1, a Negative Regulator of the Ethylene Response Pathway in Arabidopsis, Encodes a Member of the Raf Family of Protein Kinases, Cell, 1993, vol. 72, pp. 427-441.
73. Hua, J. and Meyerowitz, E.M., Ethylene Responses Are Negatively Regulated by a Receptor Gene Family in Arabidopsis thaliana, Cell, 1998, vol. 94, pp. 261-271.
74. Clark, K.L., Larsen, P.B., Wang, X., and Chang, C., Association of the Arabidopsis CTR1 Raf-Like Kinase with the ETR1 and ERS Ethylene Receptors, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 5401-5406.
75. Kovtun, Y., Chiu, W.-L., Zeng, W., and Sheen, J., Suppression of Auxin Signal Transduction by a MAPK Cascade in Higher Plants, Nature, 1998, vol. 395, pp. 716-720.
76. Hall, M.A., Smith, A.R., Novikova, G.V., and Moshkov, I.E., Ethylene Signal Transduction in Relation to Hormone Sensitivity, Plant Biol., 1999, vol. 1, pp. 46-56.
77. Novikova, G.V., Moshkov, I.E., Smith, A.R., and Hall, M.A., The Effect of Ethylene on MAPKinase-Like Activity in Arabidopsis thaliana, FEBS Lett., vol. 474, pp. 29-32.
78. ras by Endothelin-1 Sequentially Activates the ERK Cascade and Phosphatidylinositol 3-Kinase, EMBO J., 1997, vol. 16, pp. 6439-6451.
79. Sessa, G., Raz, V., Savaldi, S., and Fluhr, R., PK12, a Plant Dual-Specificity Protein Kinase of the LAMMER Family, Is Regulated by the Hormone Ethylene, Plant Cell, 1996, vol. 8, pp. 2223-2234.
80. Smith, A.R., Moshkov, I.E., Novikova, G.V., and Hall, M.A., The Effect of Ethylene and Cytokinin on GTP Binding and MAP Kinase Activity in Arabidopsis thaliana, Biology and BioTechnology of the Plant Hormone Ethylene II, Kanellis, A.K. et al., Eds., Dordrecht: Kluwer, 1999, pp. 77-84.
81. Bokoch, G.M., Interplay between Ras-Related and Heterotrimeric GTP Binding Proteins: Life-Styles of the Big and Little, FASEB J., 1996, vol. 10, pp. 1290-1295.
82. Novikova, G.V., Moshkov, I.E., Smith, A.R., and Hall, M.A., The Effect of Ethylene on GTP Binding in Extracts from Pea Seedlings, Planta, 1997, vol. 201, pp. 1-8.
83. Tan, P.B.O. and Kim, S.K., Signaling Specificity the RTK/RAS/MAP Kinase Pathway in Metazoans, Trends Genet., 1999, vol. 15, pp. 145-149.
84. Mizoguchi, T., Gotoh, Y., Nishida, E., Yamaguchi-Shinozaki, K., Hayashida, N., Iwasaki, H., Kamada, H., and Shinozaki, K., Characterization of Two cDNAs that Encode MAP Kinase Homologues in Arabidopsis thaliana and Analysis of the Possible Role of Auxin in Activating Such Kinase Activity in Cultured Cells, Plant J., 1994, vol. 5, pp. 111-122.
85. Knetsch, M.L.W., Wang, M., Snaar-Jagalska, B.E., and Heimovaara-Dijkstra, S., Abscisic Acid Induces Mitogen-Activated Protein Kinase Activation in Barley Aleurone Protoplasts, Plant Cell, 1996, vol. 8, pp. 1061-1067.
86. Leung, J., Bouvier-Durand, M., Morris, P.-C., Guerrier, D., Chefdor, F., and Giraudat, J., Arabidopsis ABA-Response Gene ABI1: Features of a Calcium-Modulated Protein Phosphatase, Science, 1994, vol. 264, pp. 1448-1452.
87. Leung, J., Merlot, S., and Giraudat, J., The Arabidopsis Abscisic Acid-Insensitive (ABI2) and ABI1 Genes Encode Redundant Protein Phosphatase 2C Involved in Abscisic Acid Signal Transduction, Plant Cell, 1997, vol. 9, pp. 759-771.
88. Bertauche, N., Leung, J., and Giraudat, J., Protein Phosphatase Activity of Abscisic Acid Insensitive 1 (ABI1) Protein from Arabidopsis thaliana, Eur. J. Biochem., 1996, vol. 241, pp. 193-200.
89. Rodriguez, P.L., Leube, M.P., and Grill, E., ABI2, a Second Protein Phosphatase 2C Involved in Abscisic Acid Signal Transduction in Arabidopsis thaliana, FEBS Lett., 1998, vol. 421, pp. 185-190.
90. + Channels Is Suspended by abil-1, a Mutant Arabidopsis Gene Encoding a Putative Protein Phosphatase, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 9520-9524.
91. Grabov, A., Leung, J., Giraudat, J., and Blatt, M.R., Alteration of Anion Channel Kinetics in Wild-Type and abil-1 Transgenic Nicotiana benthamiana Guard Cells by Abscisic Acid, Plant J., 1997, vol. 12, pp. 203-213.
92. Pei, Z.-M., Kuchitsu, K., Ward, J.M., Schwarz, M., and Schroeder, J.I., Differential Abscisic Acid Regulation of Guard Cell Slow Anion Channels in Arabidopsis Wild-Type and abi1 and abi2 Mutants, Plant Cell, 1997, vol. 9, pp. 409-423.
93. Heimovaara-Dijkstra, S., Nieland, T.J.F., van der Meulen, R.M., and Wang, M., Abscisic Acid-Induced Gene Expression Requires the Activity of Protein(s) Sensitive to the Protein-Tyrosine Phosphatase Inhibitor Phenylarsine Oxide, Plant Growth Regul., 1996, vol. 18, pp. 115-123.
94. Milarski, K.L. and Saltiel, A.R., Expression of Catalytically Inactive Syp Phosphatase in 3T3 Cells Blocks Stimulation of Mitogen-Activated Protein Kinase by Insulin, J. Biol. Chem., 1994, vol. 269, pp. 21239-21243.
95. Xiao, S., Rose, D.W., Sasaoka, T., Maegawa, H., Burke, T.R., Roller, P.P., Shoelson, S.E., and Olefsky, J.M., Syp (SH-PTP2) Is a Positive Mediator of Growth Factor-Stimulated Mitogenic Signal Transduction, J. Biol. Chem., 1994, vol. 269, pp. 21244-21248.
96. ras, Biochem. Biophys. Res. Commun., 1995, vol. 214, pp. 737-743.
97. Huttly, A.K. and Phillips, A.L., Gibberellin-Regulated Expression in Oat Aleurone Cells of Two Kinases that Show Homology to MAP Kinase and a Ribosomal Protein Kinase, Plant Mol. Biol., 1995, vol. 27, pp. 1043-1052.
98. Zegzouti, H., Jones, B., Frasse, P., Marty, C., Maitre, B., Latché, A., Pech, J.-C., and Bouzayen, M., Ethylene-Regulated Gene Expression in Tomato Fruit: Characterization of Novel Ethylene-Responsive and Ripening-Related Genes Isolated by Differential Display, Plant J., 1999, vol. 18, pp. 589-600.
99. Terryn, N., Arias, M.B., Engler, G., Tiré, C., Villarroel, R., van Montagu, M., and Inzé, D., rha1, a Gene Encoding a Small GTP Binding Protein from Arabidopsis, Is Expressed Primarily in Developing Guard Cells, Plant Cell, 1993, vol. 5, pp. 1761-1769.
100. Li, H., Lin, Y., Heath, R., Zhu, M., and Yang, Z., Control of Pollen Tube Tip Growth by a Rop GTPase-Dependent Pathway that Leads to the Tip-Localized Calcium Influx, Plant Cell, 1999, vol. 11, pp. 1731-1742.
101. Lin, Y. and Yang, Z., Inhibition of Pollen Tube Elongation by Microinjected Anti-Rop1Ps Antibodies Suggests a Crucial Role for Rho-Type GTPases in the Control of Tip Growth, Plant Cell, 1997, vol. 9, pp. 1647-1659.
102. Li, H., Wu, G., Ware, D., Davis, K.R., and Yang, Z., Arabidopsis Rho-Related GTPases: Differential Gene Expression in Pollen and Polar Localization in Fission Yeast, Plant Physiol., 1998, vol. 118, pp. 407-417.
103. Kost, B., Lemichez, E., Spielhofer, P., Hong, Y., Tolias, K., Carpenter, C., and Chua, N.-H., Rac Homologues and Compartmentalized Phosphatidylinositol 4,5-Bisphosphate Act in a Common Pathway to Regulate Polar Pollen Tube Growth, J. Cell Biol., 1999, vol. 145, pp. 317-330.
104. Hirt, H., Connecting Oxidative Stress, Auxin, and Cell Cycle Regulation through a Plant Mitogen-Activated Protein Kinase Pathway, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 2405-2407.
105. Ciardi, J.A., Tieman, D.M., Lund, S.T., Jones, J.B., Stall, R.E., and Klee, H., Response to Xanthomonas campestris pv. vesicatoria in Tomato Involves Regulation of Ethylene Receptor Gene Expression, Plant Physiol., 2000, vol. 123, pp. 81-92.
106. 3, J. Immunol., 1997, vol. 159, pp. 2586-2598.
107. Mulligan, G.J., Wong, J., and Jacks, T., p130 Is Dispensable in Peripheral T Lymphocytes: Evidence for Functional Compensation by p107 and pRB, Mol. Cell. Biol., 1998, vol. 18, pp. 206-220.
108. Minkoff, R., Bale, E.S., Kerr, C.A., and Struss, W.E., Antisense Oligonucleotide Blockade of Connexin Expression during Embryonic Bone Formation: Evidence of Functional Compensation within a Multigene Family, Dev. Genet., 1999, vol. 24, pp. 43-56.