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The Age of Protein Kinases

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Plant Kinases

Part of the book series: Methods in Molecular Biology ((MIMB,volume 779))

Abstract

Major progress has been made in unravelling of regulatory mechanisms in eukaryotic cells. Modification of target protein properties by reversible phosphorylation events has been found to be one of the most prominent cellular control processes in all organisms. The phospho-status of a protein is dynamically controlled by protein kinases and counteracting phosphatases. Therefore, monitoring of kinase and phosphatase activities, identification of specific phosphorylation sites, and assessment of their functional significance are of crucial importance to understand development and homeostasis. Recent advances in the area of molecular biology and biochemistry, for instance, mass spectrometry-based phosphoproteomics or fluorescence spectroscopical methods, open new possibilities to reach an unprecidented depth and a proteome-wide understanding of phosphorylation processes in plants and other species. In addition, the growing number of model species allows now deepening evolutionary insights into signal transduction cascades and the use of kinase/phosphatase systems. Thus, this is the age where we move from an understanding of the structure and function of individual protein modules to insights how these proteins are organized into pathways and networks. In this introductory chapter, we briefly review general definitions, methodology, and current concepts of the molecular mechanisms of protein kinase function as a foundation for this methods book. We briefly review biochemistry and structural biology of kinases and provide selected examples for the role of kinases in biological systems.

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References

  1. Boyer, P.D., and Krebs, E.G. (1986) The enzymes. Vol. XVII, Control by phosphorylation, part A: general features, specific enzymes (I), Academic Press, Orlando, Fla.

    Google Scholar 

  2. IUPAC-IUB Commission on Biochemical Nomenclature (CBN), T. (1977) Nomenclature of phosphorus-containing compounds of biochemical importance. (Recommendations 1976) IUPAC-IUB Commission on Biochemical Nomenclature. Hoppe Seylers Z Physiol Chem 358, 599–616.

    Google Scholar 

  3. Manning, G., Plowman, G. D., Hunter, T., and Sudarsanam, S. (2002) Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27, 514–20.

    Article  PubMed  CAS  Google Scholar 

  4. Chevalier, D., and Walker, J. C. (2005) Functional genomics of protein kinases in plants. Brief Funct Genomic Proteomic 3, 362–71.

    Article  PubMed  CAS  Google Scholar 

  5. Hubbard, M. J., and Cohen, P. (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem Sci 18, 172–7.

    Article  PubMed  CAS  Google Scholar 

  6. Ahn, N. G., and Resing, K. A. (2001) Toward the phosphoproteome. Nat Biotechnol 19, 317–8.

    Article  PubMed  CAS  Google Scholar 

  7. Duclos, B., Marcandier, S., and Cozzone, A. J. (1991) Chemical properties and separation of phosphoamino acids by thin-layer chromatography and/or electrophoresis. Methods Enzymol 201, 10–21.

    Article  PubMed  CAS  Google Scholar 

  8. Hunter, T. (1996) Tyrosine phosphorylation: past, present and future. Biochem Soc Trans 24, 307–27.

    Article  PubMed  CAS  Google Scholar 

  9. Ding, S.J., Qian, W. J., and Smith, R. D. (2007) Quantitative proteomic approaches for studying phosphotyrosine signaling. Expert Rev Proteomics 4, 13–23.

    Article  PubMed  CAS  Google Scholar 

  10. Zhang, Y., Wolf-Yadlin, A., and White, F.M. (2007) Quantitative proteomic analysis of phosphotyrosine-mediated cellular signaling networks. Methods Mol Biol 359, 203–12.

    Article  PubMed  CAS  Google Scholar 

  11. Seet, B.T., Dikic, I., Zhou, M. M., and Pawson, T. (2006) Reading protein modifications with interaction domains. Nat Rev Mol Cell Biol 7, 473–83.

    Article  PubMed  CAS  Google Scholar 

  12. Sugiyama, N., Nakagami, H., Mochida, K., Daudi, A., Tomita, M., Shirasu, K., and Ishihama, Y. (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4.

    Google Scholar 

  13. Riano-Pachon, D. M., Kleessen, S., Neigenfind, J., Durek, P., Weber, E., Engelsberger, W. R., Walther, D., Selbig, J., Schulze, W. X., and Kersten, B. (2010) Proteome-wide survey of phosphorylation patterns affected by nuclear DNA polymorphisms in Arabidopsis thaliana. BMC Genomics 11, 411.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Nakagami, H., Sugiyama, N., Mochida, K., Daudi, A., Yoshida, Y., Toyoda, T., Tomita, M., Ishihama, Y., and Shirasu, K. (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153, 1161–74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Sugiyama, N., Masuda, T., Shinoda, K., Nakamura, A., Tomita, M., and Ishihama, Y. (2007) Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol Cell Proteomics 6, 1103–9.

    Article  PubMed  CAS  Google Scholar 

  16. Molina, H., Horn, D. M., Tang, N., Mathivanan, S., and Pandey, A. (2007) Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc Natl Acad Sci U S A 104, 2199–204.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. de la Fuente van Bentem, S., and Hirt, H. (2009) Protein tyrosine phosphorylation in plants: More abundant than expected? Trends Plant Sci 14, 71–6.

    Article  CAS  Google Scholar 

  18. Smith, R. D., and Walker, J. C. (1996) Plant Protein Phosphatases. Annu Rev Plant Physiol Plant Mol Biol 47, 101–125.

    Article  PubMed  CAS  Google Scholar 

  19. Luan, S. (2003) Protein phosphatases in plants. Annu Rev Plant Biol 54, 63–92.

    Article  PubMed  CAS  Google Scholar 

  20. Wei, Y. F., and Matthews, H. R. (1991) Identification of phosphohistidine in proteins and purification of protein-histidine kinases. Methods Enzymol 200, 388–414.

    Article  PubMed  CAS  Google Scholar 

  21. Serber, Z., and Ferrell, J. E., Jr. (2007) Tuning bulk electrostatics to regulate protein function. Cell 128, 441–4.

    Article  PubMed  CAS  Google Scholar 

  22. Strickfaden, S. C., Winters, M. J., Ben-Ari, G., Lamson, R. E., Tyers, M., and Pryciak, P. M. (2007) A mechanism for cell-cycle regulation of MAP kinase signaling in a yeast differentiation pathway. Cell 128, 519–31.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Johnson, L. N., and Barford, D. (1993) The effects of phosphorylation on the structure and function of proteins. Annu Rev Biophys Biomol Struct 22, 199–232.

    Article  PubMed  CAS  Google Scholar 

  24. Groban, E. S., Narayanan, A., and Jacobson, M. P. (2006) Conformational changes in protein loops and helices induced by post-translational phosphorylation. PLoS Comput Biol 2, e32.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Mandell, D. J., Chorny, I., Groban, E. S., Wong, S. E., Levine, E., Rapp, C. S., and Jacobson, M. P. (2007) Strengths of hydrogen bonds involving phosphorylated amino acid side chains. J Am Chem Soc 129, 820–7.

    Article  PubMed  CAS  Google Scholar 

  26. Lu, P. J., Zhou, X. Z., Shen, M., and Lu, K. P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283, 1325–8.

    Article  PubMed  CAS  Google Scholar 

  27. Rubin, S. M., Gall, A. L., Zheng, N., and Pavletich, N. P. (2005) Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release. Cell 123, 1093–106.

    Article  PubMed  CAS  Google Scholar 

  28. Russo, A. A., Jeffrey, P. D., and Pavletich, N. P. (1996) Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat Struct Biol 3, 696–700.

    Article  PubMed  CAS  Google Scholar 

  29. Johnson, L. N., and O’Reilly, M. (1996) Control by phosphorylation. Curr Opin Struct Biol 6, 762–9.

    Article  PubMed  CAS  Google Scholar 

  30. Welburn, J. P., Tucker, J. A., Johnson, T., Lindert, L., Morgan, M., Willis, A., Noble, M. E., and Endicott, J. A. (2007) How tyrosine 15 phosphorylation inhibits the activity of cyclin-dependent kinase 2-cyclin A. J Biol Chem 282, 3173–81.

    Article  PubMed  CAS  Google Scholar 

  31. Hurley, J. H., Dean, A. M., Thorsness, P. E., Koshland, D. E., Jr., and Stroud, R. M. (1990) Regulation of isocitrate dehydrogenase by phosphorylation involves no long-range conformational change in the free enzyme. J Biol Chem 265, 3599–602.

    Article  PubMed  CAS  Google Scholar 

  32. Pawson, T., and Gish, G. D. (1992) SH2 and SH3 domains: from structure to function. Cell 71, 359–62.

    Article  PubMed  CAS  Google Scholar 

  33. Pawson, T. (1995) Protein modules and signalling networks. Nature 373, 573–80.

    Article  PubMed  CAS  Google Scholar 

  34. Hunter, T. (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225–36.

    Article  PubMed  CAS  Google Scholar 

  35. Johnson, L. N., Noble, M. E., and Owen, D. J. (1996) Active and inactive protein kinases: structural basis for regulation. Cell 85, 149–58.

    Article  PubMed  CAS  Google Scholar 

  36. Olah, G. A., Mitchell, R. D., Sosnick, T. R., Walsh, D. A., and Trewhella, J. (1993) Solution structure of the cAMP-dependent protein kinase catalytic subunit and its contraction upon binding the protein kinase inhibitor peptide. Biochemistry 32, 3649–57.

    Article  PubMed  CAS  Google Scholar 

  37. Liao, J. J. (2007) Molecular recognition of protein kinase binding pockets for design of potent and selective kinase inhibitors. J Med Chem 50, 409–24.

    Article  PubMed  CAS  Google Scholar 

  38. Liu, Y., and Gray, N. S. (2006) Rational design of inhibitors that bind to inactive kinase conformations. Nat Chem Biol 2, 358–64.

    Article  PubMed  CAS  Google Scholar 

  39. Johnson, L. N. (2009) The regulation of protein phosphorylation. Biochem Soc Trans 37, 627–41.

    Article  PubMed  CAS  Google Scholar 

  40. Huse, M., and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275–82.

    Article  PubMed  CAS  Google Scholar 

  41. Nolen, B., Taylor, S., and Ghosh, G. (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15, 661–75.

    Article  PubMed  CAS  Google Scholar 

  42. Kannan, N., and Neuwald, A. F. (2004) Evolutionary constraints associated with functional specificity of the CMGC protein kinases MAPK, CDK, GSK, SRPK, DYRK, and CK2alpha. Protein Sci 13, 2059–77.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Hanks, S. K., and Hunter, T. (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. Faseb J 9, 576–96.

    Article  PubMed  CAS  Google Scholar 

  44. Taylor, S. S., Radzio-Andzelm, E., and Hunter, T. (1995) How do protein kinases discriminate between serine/threonine and tyrosine? Structural insights from the insulin receptor protein-tyrosine kinase. Faseb J 9, 1255–66.

    Article  PubMed  CAS  Google Scholar 

  45. Johnson, L. N., Lowe, E. D., Noble, M. E., and Owen, D. J. (1998) The Eleventh Datta Lecture. The structural basis for substrate recognition and control by protein kinases. FEBS Lett 430, 1–11.

    Article  PubMed  CAS  Google Scholar 

  46. Morgan, D. O. (2007) The cell cycle: principles of control, New Science Press Ltd in association with Oxford University Press, London.

    Google Scholar 

  47. Hanks, S. K., Quinn, A. M., and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52.

    Article  PubMed  CAS  Google Scholar 

  48. Niefind, K., Yde, C. W., Ermakova, I., and Issinger, O. G. (2007) Evolved to be active: sulfate ions define substrate recognition sites of CK2alpha and emphasise its exceptional role within the CMGC family of eukaryotic protein kinases. J Mol Biol 370, 427–38.

    Article  PubMed  CAS  Google Scholar 

  49. Schulze-Gahmen, U., De Bondt, H. L., and Kim, S. H. (1996) High-resolution crystal structures of human cyclin-dependent kinase 2 with and without ATP: bound waters and natural ligand as guides for inhibitor design. J Med Chem 39, 4540–6.

    Article  PubMed  CAS  Google Scholar 

  50. Adams, J. A. (2001) Kinetic and catalytic mechanisms of protein kinases. Chem Rev 101, 2271–90.

    Article  PubMed  CAS  Google Scholar 

  51. 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. Methods Enzymol 200, 38–62.

    Article  PubMed  CAS  Google Scholar 

  52. Nigg, E. A. (1993) Targets of cyclin-dependent protein kinases. Curr Opin Cell Biol 5, 187–93.

    Article  PubMed  CAS  Google Scholar 

  53. Songyang, Z., Blechner, S., Hoagland, N., Hoekstra, M. F., Piwnica-Worms, H., and Cantley, L. C. (1994) Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 4, 973–82.

    Article  PubMed  CAS  Google Scholar 

  54. Bardwell, L., and Thorner, J. (1996) A conserved motif at the amino termini of MEKs might mediate high-affinity interaction with the cognate MAPKs. Trends Biochem Sci 21, 373–4.

    Article  PubMed  CAS  Google Scholar 

  55. Jeffrey, P. D., Russo, A. A., Polyak, K., Gibbs, E., Hurwitz, J., Massague, J., and Pavletich, N. P. (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376, 313–20.

    Article  PubMed  CAS  Google Scholar 

  56. Brown, N. R., Noble, M. E., Endicott, J. A., and Johnson, L. N. (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat Cell Biol 1, 438–43.

    Article  PubMed  CAS  Google Scholar 

  57. De Bondt, H. L., Rosenblatt, J., Jancarik, J., Jones, H. D., Morgan, D. O., and Kim, S. H. (1993) Crystal structure of cyclin-dependent kinase 2. Nature 363, 595–602.

    Article  PubMed  Google Scholar 

  58. Zhang, F., Strand, A., Robbins, D., Cobb, M. H., and Goldsmith, E. J. (1994) Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature 367, 704–11.

    Article  PubMed  CAS  Google Scholar 

  59. Adams, J. A., McGlone, M. L., Gibson, R., and Taylor, S. S. (1995) Phosphorylation modulates catalytic function and regulation in the cAMP-dependent protein kinase. Biochemistry 34, 2447–54.

    Article  PubMed  CAS  Google Scholar 

  60. Dissmeyer, N., Nowack, M. K., Pusch, S., Stals, H., Inze, D., Grini, P. E., and Schnittger, A. (2007) T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell 19, 972–85.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Pusch, S., Harashima, H., and Schnittger, A. (submitted) Identification and in vivo characterization of enzyme-substrate interactions by bimolecular fluorescence complementation assays.

    Google Scholar 

  62. Morgan, D. O., and De Bondt, H. L. (1994) Protein kinase regulation: insights from crystal structure analysis. Curr Opin Cell Biol 6, 239–46.

    Article  PubMed  CAS  Google Scholar 

  63. Macdonald, N., Welburn, J. P., Noble, M. E., Nguyen, A., Yaffe, M. B., Clynes, D., Moggs, J. G., Orphanides, G., Thomson, S., Edmunds, J. W., Clayton, A. L., Endicott, J. A., and Mahadevan, L. C. (2005) Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Mol Cell 20, 199–211.

    Article  PubMed  CAS  Google Scholar 

  64. Filippakopoulos, P., Kofler, M., Hantschel, O., Gish, G. D., Grebien, F., Salah, E., Neudecker, P., Kay, L. E., Turk, B. E., Superti-Furga, G., Pawson, T., and Knapp, S. (2008) Structural coupling of SH2-kinase domains links Fes and Abl substrate recognition and kinase activation. Cell 134, 793–803.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Ubersax, J. A., and Ferrell, J. E., Jr. (2007) Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8, 530–41.

    Article  PubMed  CAS  Google Scholar 

  66. Cheek, S., Zhang, H., and Grishin, N. V. (2002) Sequence and structure classification of kinases. J Mol Biol 320, 855–81.

    Article  PubMed  CAS  Google Scholar 

  67. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912–34.

    Article  CAS  PubMed  Google Scholar 

  68. Caenepeel, S., Charydczak, G., Sudarsanam, S., Hunter, T., and Manning, G. (2004) The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci U S A 101, 11707–12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Ptacek, J., and Snyder, M. (2006) Charging it up: global analysis of protein phosphorylation. Trends Genet 22, 545–54.

    Article  PubMed  CAS  Google Scholar 

  70. The Arabidopsis Genome Initiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815.

    Article  Google Scholar 

  71. International Rice Genome Sequencing Project. (2005) The map-based sequence of the rice genome. Nature 436, 793–800.

    Article  CAS  Google Scholar 

  72. Krupa, A., Anamika, K., and Srinivasan, N. (2006) Genome-wide comparative analyses of domain organisation of repertoires of protein kinases of Arabidopsis thaliana and Oryza sativa. Gene 380, 1–13.

    Article  PubMed  CAS  Google Scholar 

  73. Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K., Thibaud-Nissen, F., Malek, R. L., Lee, Y., Zheng, L., Orvis, J., Haas, B., Wortman, J., and Buell, C. R. (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35, D883–7.

    Article  PubMed  CAS  Google Scholar 

  74. Gribskov, M., Fana, F., Harper, J., Hope, D. A., Harmon, A. C., Smith, D. W., Tax, F. E., and Zhang, G. (2001) PlantsP: a functional genomics database for plant phosphorylation. Nucleic Acids Res 29, 111–3.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Tchieu, J. H., Fana, F., Fink, J. L., Harper, J., Nair, T. M., Niedner, R. H., Smith, D. W., Steube, K., Tam, T. M., Veretnik, S., Wang, D., and Gribskov, M. (2003) The PlantsP and PlantsT Functional Genomics Databases. Nucleic Acids Res 31, 342–4.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Champion, A., Kreis, M., Mockaitis, K., Picaud, A., and Henry, Y. (2004) Arabidopsis kinome: after the casting. Funct Integr Genomics 4, 163–87.

    Article  PubMed  CAS  Google Scholar 

  77. Hunter, T., and Plowman, G. D. (1997) The protein kinases of budding yeast: six score and more. Trends Biochem Sci 22, 18–22.

    Article  PubMed  CAS  Google Scholar 

  78. Dardick, C., Chen, J., Richter, T., Ouyang, S., and Ronald, P. (2007) The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol 143, 579–86.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Atkinson, H. J., Morris, J. H., Ferrin, T. E., and Babbitt, P. C. (2009) Using sequence similarity networks for visualization of relationships across diverse protein superfamilies. PLoS One 4, e4345.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Hardie, D. G. (1999) PLANT PROTEIN SERINE/THREONINE KINASES: Classification and Functions. Annu Rev Plant Physiol Plant Mol Biol 50, 97–131.

    Article  PubMed  CAS  Google Scholar 

  81. Champion, A., Picaud, A., and Henry, Y. (2004) Reassessing the MAP3K and MAP4K relationships. Trends Plant Sci 9, 123–9.

    Article  PubMed  CAS  Google Scholar 

  82. Menges, M., de Jager, S. M., Gruissem, W., and Murray, J. A. (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41, 546–66.

    Article  PubMed  CAS  Google Scholar 

  83. Pitzschke, A., Schikora, A., and Hirt, H. (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12, 421–6.

    Article  PubMed  CAS  Google Scholar 

  84. Fiil, B. K., Petersen, K., Petersen, M., and Mundy, J. (2009) Gene regulation by MAP kinase cascades. Curr Opin Plant Biol 12, 615–21.

    Article  PubMed  CAS  Google Scholar 

  85. Andreasson, E., and Ellis, B. (2010) Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci 15, 106–113.

    Article  PubMed  CAS  Google Scholar 

  86. Sterky, F., Bhalerao, R. R., Unneberg, P., Segerman, B., Nilsson, P., Brunner, A. M., Charbonnel-Campaa, L., Lindvall, J. J., Tandre, K., Strauss, S. H., Sundberg, B., Gustafsson, P., Uhlen, M., Bhalerao, R. P., Nilsson, O., Sandberg, G., Karlsson, J., Lundeberg, J., and Jansson, S. (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci U S A 101, 13951–6.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Tuskan, G. A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R. R., Bhalerao, R. P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., Busov, V., Campbell, M., Carlson, J., Chalot, M., Chapman, J., Chen, G. L., Cooper, D., Coutinho, P. M., Couturier, J., Covert, S., Cronk, Q., Cunningham, R., Davis, J., Degroeve, S., Dejardin, A., Depamphilis, C., Detter, J., Dirks, B., Dubchak, I., Duplessis, S., Ehlting, J., Ellis, B., Gendler, K., Goodstein, D., Gribskov, M., Grimwood, J., Groover, A., Gunter, L., Hamberger, B., Heinze, B., Helariutta, Y., Henrissat, B., Holligan, D., Holt, R., Huang, W., Islam-Faridi, N., Jones, S., Jones-Rhoades, M., Jorgensen, R., Joshi, C., Kangasjarvi, J., Karlsson, J., Kelleher, C., Kirkpatrick, R., Kirst, M., Kohler, A., Kalluri, U., Larimer, F., Leebens-Mack, J., Leple, J. C., Locascio, P., Lou, Y., Lucas, S., Martin, F., Montanini, B., Napoli, C., Nelson, D. R., Nelson, C., Nieminen, K., Nilsson, O., Pereda, V., Peter, G., Philippe, R., Pilate, G., Poliakov, A., Razumovskaya, J., Richardson, P., Rinaldi, C., Ritland, K., Rouze, P., Ryaboy, D., Schmutz, J., Schrader, J., Segerman, B., Shin, H., Siddiqui, A., Sterky, F., Terry, A., Tsai, C. J., Uberbacher, E., Unneberg, P., et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596–604.

    Article  PubMed  CAS  Google Scholar 

  88. International Brachypodium Initiative, T. (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463, 763–8.

    Article  CAS  Google Scholar 

  89. The French-Italian Public Consortium for Grapevine Genome Characterization. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463–467.

    Article  CAS  Google Scholar 

  90. Shiu, S. H., and Bleecker, A. B. (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A 98, 10763–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Shiu, S. H., Karlowski, W. M., Pan, R., Tzeng, Y. H., Mayer, K. F., and Li, W. H. (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220–34.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Dardick, C., and Ronald, P. (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog 2, e2.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. McCarty, D. R., and Chory, J. (2000) Conservation and innovation in plant signaling pathways. Cell 103, 201–9.

    Article  PubMed  CAS  Google Scholar 

  94. Wang, D., Harper, J. F., and Gribskov, M. (2003) Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae. Plant Physiol 132, 2152–65.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Luan, S. (2002) Tyrosine phosphorylation in plant cell signaling. Proc Natl Acad Sci U S A 99, 11567–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Carpi, A., Di Maira, G., Vedovato, M., Rossi, V., Naccari, T., Floriduz, M., Terzi, M., and Filippini, F. (2002) Comparative proteome bioinformatics: identification of a whole complement of putative protein tyrosine kinases in the model flowering plant Arabidopsis thaliana. Proteomics 2, 1494–503.

    Article  PubMed  CAS  Google Scholar 

  97. Rudrabhatla, P., Reddy, M. M., and Rajasekharan, R. (2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 60, 293–319.

    Article  PubMed  CAS  Google Scholar 

  98. Miranda-Saavedra, D., and Barton, G. J. (2007) Classification and functional annotation of eukaryotic protein kinases. Proteins 68, 893–914.

    Article  PubMed  CAS  Google Scholar 

  99. Pawson, T., and Scott, J. D. (2005) Protein phosphorylation in signaling – 50 years and counting. Trends Biochem Sci 30, 286–90.

    Article  PubMed  CAS  Google Scholar 

  100. Deshaies, R. J. (1999) SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15, 435–67.

    Article  PubMed  CAS  Google Scholar 

  101. Seeger, M., Kraft, R., Ferrell, K., Bech-Otschir, D., Dumdey, R., Schade, R., Gordon, C., Naumann, M., and Dubiel, W. (1998) A novel protein complex involved in signal transduction possessing similarities to 26S proteasome subunits. Faseb J 12, 469–78.

    Article  PubMed  CAS  Google Scholar 

  102. Naumann, M., Bech-Otschir, D., Huang, X., Ferrell, K., and Dubiel, W. (1999) COP9 signalosome-directed c-Jun activation/stabilization is independent of JNK. J Biol Chem 274, 35297–300.

    Article  PubMed  CAS  Google Scholar 

  103. Bech-Otschir, D., Kraft, R., Huang, X., Henklein, P., Kapelari, B., Pollmann, C., and Dubiel, W. (2001) COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. Embo J 20, 1630–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Willems, A. R., Lanker, S., Patton, E. E., Craig, K. L., Nason, T. F., Mathias, N., Kobayashi, R., Wittenberg, C., and Tyers, M. (1996) Cdc53 targets phosphorylated G1 cyclins for degradation by the ubiquitin proteolytic pathway. Cell 86, 453–63.

    Article  PubMed  CAS  Google Scholar 

  105. Lanker, S., Valdivieso, M. H., and Wittenberg, C. (1996) Rapid degradation of the G1 cyclin Cln2 induced by CDK-dependent phosphorylation. Science 271, 1597–601.

    Article  PubMed  CAS  Google Scholar 

  106. Vlach, J., Hennecke, S., and Amati, B. (1997) Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. Embo J 16, 5334–44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Uhle, S., Medalia, O., Waldron, R., Dumdey, R., Henklein, P., Bech-Otschir, D., Huang, X., Berse, M., Sperling, J., Schade, R., and Dubiel, W. (2003) Protein kinase CK2 and protein kinase D are associated with the COP9 signalosome. Embo J 22, 1302–12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Nowack, M. K., Grini, P. E., Jakoby, M. J., Lafos, M., Koncz, C., and Schnittger, A. (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38, 63–7.

    Article  PubMed  CAS  Google Scholar 

  109. Iwakawa, H., Shinmyo, A., and Sekine, M. (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45, 819–31.

    Article  PubMed  CAS  Google Scholar 

  110. Meyerson, M., Enders, G. H., Wu, C. L., Su, L. K., Gorka, C., Nelson, C., Harlow, E., and Tsai, L. H. (1992) A family of human cdc2-related protein kinases. Embo J 11, 2909–17.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Wang, H., Ngwenyama, N., Liu, Y., Walker, J. C., and Zhang, S. (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19, 63–73.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Lampard, G. R., Macalister, C. A., and Bergmann, D. C. (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322, 1113–6.

    Article  PubMed  CAS  Google Scholar 

  113. Zhang, S., and Klessig, D. F. (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6, 520–7.

    Article  PubMed  CAS  Google Scholar 

  114. Jonak, C., Okresz, L., Bogre, L., and Hirt, H. (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5, 415–24.

    Article  PubMed  CAS  Google Scholar 

  115. Romeis, T. (2001) Protein kinases in the plant defence response. Curr Opin Plant Biol 4, 407–14.

    Article  PubMed  CAS  Google Scholar 

  116. Bethke, G., Unthan, T., Uhrig, J. F., Poschl, Y., Gust, A. A., Scheel, D., and Lee, J. (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci U S A 106, 8067–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Joo, S., Liu, Y., Lueth, A., and Zhang, S. (2008) MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J 54, 129–40.

    Article  PubMed  CAS  Google Scholar 

  118. Yoo, S. D., Cho, Y. H., Tena, G., Xiong, Y., and Sheen, J. (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451, 789–95.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Torii, K. U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R. F., and Komeda, Y. (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8, 735–46.

    PubMed  PubMed Central  CAS  Google Scholar 

  120. Clark, S. E., Williams, R. W., and Meyerowitz, E. M. (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575–85.

    Article  PubMed  CAS  Google Scholar 

  121. Roe, J. L., Rivin, C. J., Sessions, R. A., Feldmann, K. A., and Zambryski, P. C. (1993) The Tousled gene in A. thaliana encodes a protein kinase homolog that is required for leaf and flower development. Cell 75, 939–50.

    Article  PubMed  CAS  Google Scholar 

  122. Jinn, T. L., Stone, J. M., and Walker, J. C. (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14, 108–17.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Torii, K. U. (2000) Receptor kinase activation and signal transduction in plants: an emerging picture. Curr Opin Plant Biol 3, 361–7.

    Article  PubMed  CAS  Google Scholar 

  124. Kim, T. W., and Wang, Z. Y. (2010) Brassinosteroid Signal Transduction from Receptor Kinases to Transcription Factors. Annu Rev Plant Biol 61, 1–23.24.

    Article  CAS  Google Scholar 

  125. Nasrallah, J. B. (2000) Cell-cell signaling in the self-incompatibility response. Curr Opin Plant Biol 3, 368–73.

    Article  PubMed  CAS  Google Scholar 

  126. Becraft, P. W. (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18, 163–92.

    Article  PubMed  CAS  Google Scholar 

  127. Hematy, K., and Hofte, H. (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11, 321–8.

    Article  PubMed  CAS  Google Scholar 

  128. 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, 539–44.

    Article  PubMed  CAS  Google Scholar 

  129. Higuchi, M., Pischke, M. S., Mahonen, A. P., Miyawaki, K., Hashimoto, Y., Seki, M., Kobayashi, M., Shinozaki, K., Kato, T., Tabata, S., Helariutta, Y., Sussman, M. R., and Kakimoto, T. (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci U S A 101, 8821–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. Hua, J., and Meyerowitz, E. M. (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94, 261–71.

    Article  PubMed  CAS  Google Scholar 

  131. Zhao, X. C., Qu, X., Mathews, D. E., and Schaller, G. E. (2002) Effect of ethylene pathway mutations upon expression of the ethylene receptor ETR1 from Arabidopsis. Plant Physiol 130, 1983–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Wang, W., Hall, A. E., O’Malley, R., and Bleecker, A. B. (2003) Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc Natl Acad Sci U S A 100, 352–7.

    Article  PubMed  CAS  Google Scholar 

  133. Deng, Y., Dong, H., Mu, J., Ren, B., Zheng, B., Ji, Z., Yang, W.-C., Liang, Y., and Zuo, J. (2010) Arabidopsis Histidine Kinase CKI1 Acts Upstream of HISTIDINE PHOSPHOTRANSFER PROTEINS to Regulate Female Gametophyte Development and Vegetative Growth. Plant Cell, tpc.108.065128.

    Google Scholar 

  134. Hunter, T. (2000) Signaling – 2000 and beyond. Cell 100, 113–27.

    Article  PubMed  CAS  Google Scholar 

  135. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J. D., Jacq, C., Johnston, M., Louis, E. J., Mewes, H. W., Murakami, Y., Philippsen, P., Tettelin, H., and Oliver, S. G. (1996) Life with 6000 genes. Science 274, 546, 563–7.

    Google Scholar 

  136. King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., Marr, M., Pincus, D., Putnam, N., Rokas, A., Wright, K. J., Zuzow, R., Dirks, W., Good, M., Goodstein, D., Lemons, D., Li, W., Lyons, J. B., Morris, A., Nichols, S., Richter, D. J., Salamov, A., Sequencing, J. G., Bork, P., Lim, W. A., Manning, G., Miller, W. T., McGinnis, W., Shapiro, H., Tjian, R., Grigoriev, I. V., and Rokhsar, D. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Goldberg, J. M., Manning, G., Liu, A., Fey, P., Pilcher, K. E., Xu, Y., and Smith, J. L. (2006) The dictyostelium kinome – analysis of the protein kinases from a simple model organism. PLoS Genet 2, e38.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Bradham, C. A., Foltz, K. R., Beane, W. S., Arnone, M. I., Rizzo, F., Coffman, J. A., Mushegian, A., Goel, M., Morales, J., Geneviere, A. M., Lapraz, F., Robertson, A. J., Kelkar, H., Loza-Coll, M., Townley, I. K., Raisch, M., Roux, M. M., Lepage, T., Gache, C., McClay, D. R., and Manning, G. (2006) The sea urchin kinome: a first look. Dev Biol 300, 180–93.

    Article  PubMed  CAS  Google Scholar 

  139. Plowman, G. D., Sudarsanam, S., Bingham, J., Whyte, D., and Hunter, T. (1999) The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms. Proc Natl Acad Sci U S A 96, 13603–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  140. Manning, G. (2005) Genomic overview of protein kinases. WormBook, 1–19.

    Google Scholar 

  141. C. elegans Sequencing Consortium, T. (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–8.

    Google Scholar 

  142. Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F., George, R. A., Lewis, S. E., Richards, S., Ashburner, M., Henderson, S. N., Sutton, G. G., Wortman, J. R., Yandell, M. D., Zhang, Q., Chen, L. X., Brandon, R. C., Rogers, Y. H., Blazej, R. G., Champe, M., Pfeiffer, B. D., Wan, K. H., Doyle, C., Baxter, E. G., Helt, G., Nelson, C. R., Gabor, G. L., Abril, J. F., Agbayani, A., An, H. J., Andrews-Pfannkoch, C., Baldwin, D., Ballew, R. M., Basu, A., Baxendale, J., Bayraktaroglu, L., Beasley, E. M., Beeson, K. Y., Benos, P. V., Berman, B. P., Bhandari, D., Bolshakov, S., Borkova, D., Botchan, M. R., Bouck, J., Brokstein, P., Brottier, P., Burtis, K. C., Busam, D. A., Butler, H., Cadieu, E., Center, A., Chandra, I., Cherry, J. M., Cawley, S., Dahlke, C., Davenport, L. B., Davies, P., de Pablos, B., Delcher, A., Deng, Z., Mays, A. D., Dew, I., Dietz, S. M., Dodson, K., Doup, L. E., Downes, M., Dugan-Rocha, S., Dunkov, B. C., Dunn, P., Durbin, K. J., Evangelista, C. C., Ferraz, C., Ferriera, S., Fleischmann, W., Fosler, C., Gabrielian, A. E., Garg, N. S., Gelbart, W. M., Glasser, K., Glodek, A., Gong, F., Gorrell, J. H., Gu, Z., Guan, P., Harris, M., Harris, N. L., Harvey, D., Heiman, T. J., Hernandez, J. R., Houck, J., Hostin, D., Houston, K. A., Howland, T. J., Wei, M. H., Ibegwam, C., et al. (2000) The genome sequence of Drosophila melanogaster. Science 287, 2185–95.

    Article  PubMed  Google Scholar 

  143. Mouse Genome Sequencing Consortium, T., Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J. F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P., Antonarakis, S. E., Attwood, J., Baertsch, R., Bailey, J., Barlow, K., Beck, S., Berry, E., Birren, B., Bloom, T., Bork, P., Botcherby, M., Bray, N., Brent, M. R., Brown, D. G., Brown, S. D., Bult, C., Burton, J., Butler, J., Campbell, R. D., Carninci, P., Cawley, S., Chiaromonte, F., Chinwalla, A. T., Church, D. M., Clamp, M., Clee, C., Collins, F. S., Cook, L. L., Copley, R. R., Coulson, A., Couronne, O., Cuff, J., Curwen, V., Cutts, T., Daly, M., David, R., Davies, J., Delehaunty, K. D., Deri, J., Dermitzakis, E. T., Dewey, C., Dickens, N. J., Diekhans, M., Dodge, S., Dubchak, I., Dunn, D. M., Eddy, S. R., Elnitski, L., Emes, R. D., Eswara, P., Eyras, E., Felsenfeld, A., Fewell, G. A., Flicek, P., Foley, K., Frankel, W. N., Fulton, L. A., Fulton, R. S., Furey, T. S., Gage, D., Gibbs, R. A., Glusman, G., Gnerre, S., Goldman, N., Goodstadt, L., Grafham, D., Graves, T. A., Green, E. D., Gregory, S., Guigo, R., Guyer, M., Hardison, R. C., Haussler, D., Hayashizaki, Y., Hillier, L. W., Hinrichs, A., Hlavina, W., Holzer, T., Hsu, F., Hua, A., Hubbard, T., Hunt, A., Jackson, I., Jaffe, D. B., Johnson, L. S., Jones, M., Jones, T. A., Joy, A., Kamal, M., et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–62.

    Article  CAS  Google Scholar 

  144. Rat Genome Sequencing Project Consortium, T., Gibbs, R. A., Weinstock, G. M., Metzker, M. L., Muzny, D. M., Sodergren, E. J., Scherer, S., Scott, G., Steffen, D., Worley, K. C., Burch, P. E., Okwuonu, G., Hines, S., Lewis, L., DeRamo, C., Delgado, O., Dugan-Rocha, S., Miner, G., Morgan, M., Hawes, A., Gill, R., Celera, Holt, R. A., Adams, M. D., Amanatides, P. G., Baden-Tillson, H., Barnstead, M., Chin, S., Evans, C. A., Ferriera, S., Fosler, C., Glodek, A., Gu, Z., Jennings, D., Kraft, C. L., Nguyen, T., Pfannkoch, C. M., Sitter, C., Sutton, G. G., Venter, J. C., Woodage, T., Smith, D., Lee, H. M., Gustafson, E., Cahill, P., Kana, A., Doucette-Stamm, L., Weinstock, K., Fechtel, K., Weiss, R. B., Dunn, D. M., Green, E. D., Blakesley, R. W., Bouffard, G. G., De Jong, P. J., Osoegawa, K., Zhu, B., Marra, M., Schein, J., Bosdet, I., Fjell, C., Jones, S., Krzywinski, M., Mathewson, C., Siddiqui, A., Wye, N., McPherson, J., Zhao, S., Fraser, C. M., Shetty, J., Shatsman, S., Geer, K., Chen, Y., Abramzon, S., Nierman, W. C., Havlak, P. H., Chen, R., Durbin, K. J., Egan, A., Ren, Y., Song, X. Z., Li, B., Liu, Y., Qin, X., Cawley, S., Worley, K. C., Cooney, A. J., D’Souza, L. M., Martin, K., Wu, J. Q., Gonzalez-Garay, M. L., Jackson, A. R., Kalafus, K. J., McLeod, M. P., Milosavljevic, A., Virk, D., Volkov, A., Wheeler, D. A., Zhang, Z., Bailey, J. A., et al. (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428, 493–521.

    Google Scholar 

  145. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., Gocayne, J. D., Amanatides, P., Ballew, R. M., Huson, D. H., Wortman, J. R., Zhang, Q., Kodira, C. D., Zheng, X. H., Chen, L., Skupski, M., Subramanian, G., Thomas, P. D., Zhang, J., Gabor Miklos, G. L., Nelson, C., Broder, S., Clark, A. G., Nadeau, J., McKusick, V. A., Zinder, N., Levine, A. J., Roberts, R. J., Simon, M., Slayman, C., Hunkapiller, M., Bolanos, R., Delcher, A., Dew, I., Fasulo, D., Flanigan, M., Florea, L., Halpern, A., Hannenhalli, S., Kravitz, S., Levy, S., Mobarry, C., Reinert, K., Remington, K., Abu-Threideh, J., Beasley, E., Biddick, K., Bonazzi, V., Brandon, R., Cargill, M., Chandramouliswaran, I., Charlab, R., Chaturvedi, K., Deng, Z., Di Francesco, V., Dunn, P., Eilbeck, K., Evangelista, C., Gabrielian, A. E., Gan, W., Ge, W., Gong, F., Gu, Z., Guan, P., Heiman, T. J., Higgins, M. E., Ji, R. R., Ke, Z., Ketchum, K. A., Lai, Z., Lei, Y., Li, Z., Li, J., Liang, Y., Lin, X., Lu, F., Merkulov, G. V., Milshina, N., Moore, H. M., Naik, A. K., Narayan, V. A., Neelam, B., Nusskern, D., Rusch, D. B., Salzberg, S., Shao, W., Shue, B., Sun, J., Wang, Z., Wang, A., Wang, X., Wang, J., Wei, M., Wides, R., Xiao, C., Yan, C., et al. (2001) The sequence of the human genome. Science 291, 1304–51.

    Article  PubMed  CAS  Google Scholar 

  146. Nuhse, T. S., Stensballe, A., Jensen, O. N., and Peck, S. C. (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16, 2394–405.

    Article  PubMed  PubMed Central  Google Scholar 

  147. Schnable, P. S., Ware, D., Fulton, R. S., Stein, J. C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T. A., Minx, P., Reily, A. D., Courtney, L., Kruchowski, S. S., Tomlinson, C., Strong, C., Delehaunty, K., Fronick, C., Courtney, B., Rock, S. M., Belter, E., Du, F., Kim, K., Abbott, R. M., Cotton, M., Levy, A., Marchetto, P., Ochoa, K., Jackson, S. M., Gillam, B., Chen, W., Yan, L., Higginbotham, J., Cardenas, M., Waligorski, J., Applebaum, E., Phelps, L., Falcone, J., Kanchi, K., Thane, T., Scimone, A., Thane, N., Henke, J., Wang, T., Ruppert, J., Shah, N., Rotter, K., Hodges, J., Ingenthron, E., Cordes, M., Kohlberg, S., Sgro, J., Delgado, B., Mead, K., Chinwalla, A., Leonard, S., Crouse, K., Collura, K., Kudrna, D., Currie, J., He, R., Angelova, A., Rajasekar, S., Mueller, T., Lomeli, R., Scara, G., Ko, A., Delaney, K., Wissotski, M., Lopez, G., Campos, D., Braidotti, M., Ashley, E., Golser, W., Kim, H., Lee, S., Lin, J., Dujmic, Z., Kim, W., Talag, J., Zuccolo, A., Fan, C., Sebastian, A., Kramer, M., Spiegel, L., Nascimento, L., Zutavern, T., Miller, B., Ambroise, C., Muller, S., Spooner, W., Narechania, A., Ren, L., Wei, S., Kumari, S., Faga, B., Levy, M. J., McMahan, L., Van Buren, P., Vaughn, M. W., et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112–5.

    Article  PubMed  CAS  Google Scholar 

  148. Hardie, R. E. G., and Hanks, S. (1995) The Protein Kinase Factsbook. Protein-Serine Kinases, Academic Press, London.

    Google Scholar 

  149. Bartova, I., Koca, J., and Otyepka, M. (2008) Functional flexibility of human cyclin-dependent kinase-2 and its evolutionary conservation. Protein Sci 17, 22–33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  150. Heazlewood, J. L., Durek, P., Hummel, J., Selbig, J., Weckwerth, W., Walther, D., and Schulze, W. X. (2008) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36, D1015–21.

    Article  PubMed  CAS  Google Scholar 

  151. Durek, P., Schmidt, R., Heazlewood, J. L., Jones, A., MacLean, D., Nagel, A., Kersten, B., and Schulze, W. X. (2009) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Res 38, D828–34.

    Google Scholar 

  152. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G. V., and Provart, N. J. (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2, e718.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Kikuchi, S., Satoh, K., Nagata, T., Kawagashira, N., Doi, K., Kishimoto, N., Yazaki, J., Ishikawa, M., Yamada, H., Ooka, H., Hotta, I., Kojima, K., Namiki, T., Ohneda, E., Yahagi, W., Suzuki, K., Li, C. J., Ohtsuki, K., Shishiki, T., Otomo, Y., Murakami, K., Iida, Y., Sugano, S., Fujimura, T., Suzuki, Y., Tsunoda, Y., Kurosaki, T., Kodama, T., Masuda, H., Kobayashi, M., Xie, Q., Lu, M., Narikawa, R., Sugiyama, A., Mizuno, K., Yokomizo, S., Niikura, J., Ikeda, R., Ishibiki, J., Kawamata, M., Yoshimura, A., Miura, J., Kusumegi, T., Oka, M., Ryu, R., Ueda, M., Matsubara, K., Kawai, J., Carninci, P., Adachi, J., Aizawa, K., Arakawa, T., Fukuda, S., Hara, A., Hashizume, W., Hayatsu, N., Imotani, K., Ishii, Y., Itoh, M., Kagawa, I., Kondo, S., Konno, H., Miyazaki, A., Osato, N., Ota, Y., Saito, R., Sasaki, D., Sato, K., Shibata, K., Shinagawa, A., Shiraki, T., Yoshino, M., Hayashizaki, Y., and Yasunishi, A. (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301, 376–9.

    Article  PubMed  Google Scholar 

  154. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., Stevenson, D. K., Zimmerman, J., Barajas, P., Cheuk, R., Gadrinab, C., Heller, C., Jeske, A., Koesema, E., Meyers, C. C., Parker, H., Prednis, L., Ansari, Y., Choy, N., Deen, H., Geralt, M., Hazari, N., Hom, E., Karnes, M., Mulholland, C., Ndubaku, R., Schmidt, I., Guzman, P., Aguilar-Henonin, L., Schmid, M., Weigel, D., Carter, D. E., Marchand, T., Risseeuw, E., Brogden, D., Zeko, A., Crosby, W. L., Berry, C. C., and Ecker, J. R. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–7.

    Article  PubMed  Google Scholar 

  155. Till, B. J., Reynolds, S. H., Greene, E. A., Codomo, C. A., Enns, L. C., Johnson, J. E., Burtner, C., Odden, A. R., Young, K., Taylor, N. E., Henikoff, J. G., Comai, L., and Henikoff, S. (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res 13, 524–30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  156. Till, B. J., Colbert, T., Tompa, R., Enns, L. C., Codomo, C. A., Johnson, J. E., Reynolds, S. H., Henikoff, J. G., Greene, E. A., Steine, M. N., Comai, L., and Henikoff, S. (2003) High-throughput TILLING for functional genomics. Methods Mol Biol 236, 205–20.

    PubMed  CAS  Google Scholar 

  157. Henikoff, S., Till, B. J., and Comai, L. (2004) TILLING. Traditional mutagenesis meets functional genomics. Plant Physiol 135, 630–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  158. Krupa, A., Abhinandan, K. R., and Srinivasan, N. (2004) KinG: a database of protein kinases in genomes. Nucleic Acids Res 32, D153–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  159. Martin, D. M., Miranda-Saavedra, D., and Barton, G. J. (2009) Kinomer v. 1.0: a database of systematically classified eukaryotic protein kinases. Nucleic Acids Res 37, D244–50.

    Article  PubMed  CAS  Google Scholar 

  160. Diella, F., Cameron, S., Gemund, C., Linding, R., Via, A., Kuster, B., Sicheritz-Ponten, T., Blom, N., and Gibson, T. J. (2004) Phospho.ELM: a database of experimentally verified phosphorylation sites in eukaryotic proteins. BMC Bioinformatics 5, 79.

    Article  PubMed  PubMed Central  Google Scholar 

  161. Smith, C. M., Shindyalov, I. N., Veretnik, S., Gribskov, M., Taylor, S. S., Ten Eyck, L. F., and Bourne, P. E. (1997) The protein kinase resource. Trends Biochem Sci 22, 444–6.

    Article  PubMed  CAS  Google Scholar 

  162. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–402.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  163. Marchler-Bauer, A., Anderson, J. B., DeWeese-Scott, C., Fedorova, N. D., Geer, L. Y., He, S., Hurwitz, D. I., Jackson, J. D., Jacobs, A. R., Lanczycki, C. J., Liebert, C. A., Liu, C., Madej, T., Marchler, G. H., Mazumder, R., Nikolskaya, A. N., Panchenko, A. R., Rao, B. S., Shoemaker, B. A., Simonyan, V., Song, J. S., Thiessen, P. A., Vasudevan, S., Wang, Y., Yamashita, R. A., Yin, J. J., and Bryant, S. H. (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31, 383–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  164. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S. R., Griffiths-Jones, S., Howe, K. L., Marshall, M., and Sonnhammer, E. L. (2002) The Pfam protein families database. Nucleic Acids Res 30, 276–80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  165. Bairoch, A., Apweiler, R., Wu, C. H., Barker, W. C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R., Magrane, M., Martin, M. J., Natale, D. A., O’Donovan, C., Redaschi, N., and Yeh, L. S. (2005) The Universal Protein Resource (UniProt). Nucleic Acids Res 33, D154–9.

    Article  PubMed  CAS  Google Scholar 

  166. Admiraal, S. J., and Herschlag, D. (1995) Mapping the transition state for ATP hydrolysis: implications for enzymatic catalysis. Chem Biol 2, 729–39.

    Article  PubMed  CAS  Google Scholar 

  167. Lindqvist, Y., Schneider, G., and Vihko, P. (1994) Crystal structures of rat acid phosphatase complexed with the transition-state analogs vanadate and molybdate. Implications for the reaction mechanism. Eur J Biochem 221, 139–42.

    Article  PubMed  CAS  Google Scholar 

  168. Xu, W., Harrison, S. C., and Eck, M. J. (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595–602.

    Article  PubMed  CAS  Google Scholar 

  169. Tsai, J., Lee, J. T., Wang, W., Zhang, J., Cho, H., Mamo, S., Bremer, R., Gillette, S., Kong, J., Haass, N. K., Sproesser, K., Li, L., Smalley, K. S., Fong, D., Zhu, Y. L., Marimuthu, A., Nguyen, H., Lam, B., Liu, J., Cheung, I., Rice, J., Suzuki, Y., Luu, C., Settachatgul, C., Shellooe, R., Cantwell, J., Kim, S. H., Schlessinger, J., Zhang, K. Y., West, B. L., Powell, B., Habets, G., Zhang, C., Ibrahim, P. N., Hirth, P., Artis, D. R., Herlyn, M., and Bollag, G. (2008) Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci U S A 105, 3041–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  170. Zheng, J., Trafny, E. A., Knighton, D. R., Xuong, N. H., Taylor, S. S., Ten Eyck, L. F., and Sowadski, J. M. (1993) 2.2 A refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Crystallogr D Biol Crystallogr 49, 362–5.

    Article  PubMed  CAS  Google Scholar 

  171. Chen, P., Luo, C., Deng, Y., Ryan, K., Register, J., Margosiak, S., Tempczyk-Russell, A., Nguyen, B., Myers, P., Lundgren, K., Kan, C. C., and O’Connor, P. M. (2000) The 1.7 A crystal structure of human cell cycle checkpoint kinase Chk1: implications for Chk1 regulation. Cell 100, 681–92.

    Article  PubMed  CAS  Google Scholar 

  172. Chandran, V., Stollar, E. J., Lindorff-Larsen, K., Harper, J. F., Chazin, W. J., Dobson, C. M., Luisi, B. F., and Christodoulou, J. (2006) Structure of the regulatory apparatus of a calcium-dependent protein kinase (CDPK): a novel mode of calmodulin-target recognition. J Mol Biol 357, 400–10.

    Article  PubMed  CAS  Google Scholar 

  173. Yde, C. W., Ermakova, I., Issinger, O. G., and Niefind, K. (2005) Inclining the purine base binding plane in protein kinase CK2 by exchanging the flanking side-chains generates a preference for ATP as a cosubstrate. J Mol Biol 347, 399–414.

    Article  PubMed  CAS  Google Scholar 

  174. Canagarajah, B. J., Khokhlatchev, A., Cobb, M. H., and Goldsmith, E. J. (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90, 859–69.

    Article  PubMed  CAS  Google Scholar 

  175. Bellon, S., Fitzgibbon, M. J., Fox, T., Hsiao, H. M., and Wilson, K. P. (1999) The structure of phosphorylated p38gamma is monomeric and reveals a conserved activation-loop conformation. Structure 7, 1057–65.

    Article  PubMed  CAS  Google Scholar 

  176. Dajani, R., Fraser, E., Roe, S. M., Young, N., Good, V., Dale, T. C., and Pearl, L. H. (2001) Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 105, 721–32.

    Article  PubMed  CAS  Google Scholar 

  177. Squire, C. J., Dickson, J. M., Ivanovic, I., and Baker, E. N. (2005) Structure and inhibition of the human cell cycle checkpoint kinase, Wee1A kinase: an atypical tyrosine kinase with a key role in CDK1 regulation. Structure 13, 541–50.

    Article  PubMed  CAS  Google Scholar 

  178. DeLano, W. L. (2005), DeLano Scientific LLC, San Carlos, CA, USA.

    Google Scholar 

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Acknowledgments

We thank Karsten Niefind, Emily Mc Callum, and Anna Richter for critical reading and helpful comments on the manuscript. This work was supported by an Action Thématique et Incitative sur Programme (ATIP) grant from the Centre National de la Recherche Scientifique to A.S.

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Correspondence to Nico Dissmeyer .

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Appendix A

Appendix A

ABA:

Abscissic acid

AGC:

Group consisting of the cyclic nucleotide-dependent family (PKA, PKG), the PKC family and the ribosomal S6 kinase family

AHK2/3:

ARABIDOPSIS HISTIDINE KINASE 2/3

APC/C:

Anaphase-promoting complex/cyclosome

APK:

Atypical PK

βARK:

G-protein-coupled β-adrenergic RK

ATM:

Ataxia telangiectasia mutated kinase

ATR:

Ataxia telangiectasia and Rad3-related kinase

BiFC:

Bimolecular fluorescence complementation

BR:

Brassinosteroid

BRI1:

BRASSINOSTEROID INSENSITIVE 1 receptor kinase

Cak:

Cdk-activating kinase

CAKAK:

Cak-activating kinase

CaM:

Calmodulin

CaMII:

Ca2+/CaM-dependent kinase II

CaMK:

Ca2+/CaM-regulated kinase

CaMK:

Group consisting of CaMK interacting proteins and SNF1 proteins

CaMKK:

CAMK kinase

cAMP:

Cyclic adenosine monophosphate

cAPK:

cAMP-dependent PK

Cdc:

Cell division control

Cdk:

Cyclin-dependent (protein) kinase

CDPK:

Ca2+-dependent PK/CaM-like domain PK

cGMP:

Cyclic guanosine monophosphate

CK1/2:

Protein kinase 1/2, name derived from Casein Kinase 1/2

CKI1:

CYTOKININ-INSENSITIVE 1

CKL/CLK:

Cdk-like kinases

CLV1:

CLAVATA 1

CPK1:

Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE 1

CRE1:

CYTOKININ RESPONSE 1

CTR1:

CONSTITUTIVE TRIPLE RESPONSE 1

DNA-PK:

DNA-dependent protein kinase

DSK:

Dual-specificity kinase

DYRK:

Dual-specificity Tyr-regulated kinase

EEF2K:

Elongation factor-2 (eEF-2) kinase

EF:

Elongation factor

EGFR:

Epidermal growth factor receptor

EIN4:

ETHYLENE INSENSITIVE 4

EPK:

Eukaryotic PK

ERK:

Extracellular signal-regulated kinase (MAPK)

ERS1/2:

ETHYLENE SENSOR 1/2

ETR1/2:

ETHYLENE RESPONSE 1/2

GSK:

Glycogen synthase kinase

IRAK:

Interleukin-1 receptor associated kinase

JAK/STAT:

Janus family of TK/signal transducer and activator of transcription

LAMMER:

Subfamily of kinases possessing a LAMMER (or related) amino acid sequence

LCK:

Lymphocyte-specific PTK

LRR:

Leucine-rich repeat

MAP2K:

MAPK kinase, MAP kinase kinase, MAPKK, now MEK in plants and MKK in Arabidopsis*

MAP3K:

MAP2K kinase, MAP kinase kinase kinase, MAPKKK, also known as MEKK*

MAP4K:

MAP3K kinase, MAP kinase kinase kinase kinase, MAPKKKK*

MAPK:

Mitogen-activated PK; now MPK in plants*

MAPKK:

MAPK kinase*

MAPKKK:

MAPKK kinase*

MEK:

MAP/ERK kinase, MAPKK, also known as MKK/MAP2K*

MEKK:

MEK kinase, MAPKKK, canonical MAP3K*

MHCK:

Myosin heavy chain kinase

Mik1:

Schizosaccharomyces pombe mitotic inhibitor kinase 1

MKK:

New name for Arabidopsis MEK/MAP2K/MAPKK*

MKK:

New name for Arabidopsis MAP2K*

MLK:

Mixed lineage kinase

MLK:

Mixed lineage kinase

MPK:

New name for Arabidopsis MAPK*

mTOR:

Molecular target of rapamycin

Myt1:

Membrane-associated Tyr/Thr PK 1

NEK:

NIMA/NIM-A related kinase (NRK)

NIMA:

“Never in mitosis A” (NIM-A)

PDGFR:

Platelet-derived growth factor receptor

PDHK:

Pyruvate dehydrogenase (acetyl-transferring) kinase

PEPRK:

PPCK-related kinases

PhK:

Phosphorylase kinase

PIKK:

Phosphatidyl inositol 3′ kinase-related kinase

PK:

Protein kinase

PKA, C, G:

Cyclic nucleotide-regulated protein kinase A, C, or G

PKA/B/C:

Protein kinase A/B/C

PKACα:

PKA catalytic subunit α

PKAK1:

Pyruvate dehydrogenase kinase

PKL:

Protein kinase-like

PPCK:

Phosphoenolpyruvate carboxylase kinase

PPK1:

Phosphatidylinositol-4-phosphate 5′ kinase

Prk:

Phosphoribulokinase

PRKIN:

Protein kinase also called MHK

PSTK:

Protein serine/threonine kinase

Pti1:

Pto-interacting 1

PTK:

Protein–tyrosine kinases

Raf:

“Rapidly growing fibrosarcoma or rat fibrosarcoma,” cellular homolog of oncogene products from murine sarcoma virus, or cellular homolog of v-raf, the transforming gene from an avian retrovirus (MAP3K)

Rb:

Retinoblastoma protein

RD:

Kinase kinase containing invariant Asp residue as catalytic base preceded by an Arg

RGC:

Receptor guanylate cyclase

RIO:

Right open reading frame

RK:

Receptor kinase

RLK:

Receptor-like kinase (protein Ser/Thr RLK)

ROS:

Reactive oxygen species

RTK:

Receptor Tyr kinase

SH:

Hydrosulphide or sulfhydryl group (in Cys)

SHAGGY:

GSK from Drosophila

SI:

Self-incompatibility

SILAC:

Stable isotope labelling

SLG:

S-locus glycoprotein

SMG-1:

Suppressor of morphogenesis in genitalia-1

SNF1:

Sucrose non-fermenting 1

SnRK:

SNF1-related kinase

SRK:

S-receptor-like kinase

STE:

Family including MAP2K, MAP4K, CDCs, MEKK, and related sequences; kinase group consisting of Sterile 20 and p21Ras-activated PK (MAP4K)

TGFβ:

Transforming growth factor-β

TGFβR1:

Transforming growth factor-β receptor kinase 1 (TGFBR1)

TK:

Tyr kinase

TKL:

Tyr kinase-like

TRPM:

Transient receptor potential ion channel melastatin

VEGFR:

Vascular endothelial growth factor receptor

WAK:

Cell wall-associated kinase

*New MAPK cascade nomenclature after (81)

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Dissmeyer, N., Schnittger, A. (2011). The Age of Protein Kinases. In: Dissmeyer, N., Schnittger, A. (eds) Plant Kinases. Methods in Molecular Biology, vol 779. Humana, Totowa, NJ. https://doi.org/10.1007/978-1-61779-264-9_2

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  • DOI: https://doi.org/10.1007/978-1-61779-264-9_2

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