Decoding Ca2+ signals through plant protein kinases

Annual Review of Plant Biology

Volumn 55, Issue , 2004, Pages 263-288

  Harper, Jeffrey R ^a   Breton, Ghislain ^a   Harmon, Alice ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Autoinhibition; CCaMK; CDPK; CRK; SnRK

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM; PROTEIN KINASE;

ARABIDOPSIS; CALCIUM SIGNALING; CLASSIFICATION; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; PLANT; REVIEW;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM; CALCIUM SIGNALING; PLANTS; PROTEIN KINASES;

ARABIDOPSIS;

EID: 3242727833     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.55.031903.141627     Document Type: Review

References (102)

1. Adams JA. 2003. Activation loop phosphorylation and catalysis in protein kinases: Is there functional evidence for the autoinhibitor model? Biochemistry 42:601-7
2. 2+-regulated kinases. EMBO J. 20:1051-63
3. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, et al. 2001. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053-57
4. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, et al. 2000. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338-42
5. 2+-dependent protein kinase with oil bodies during seed development in Santalum album L.: its biochemical characterization and significance. Plant Cell Physiol. 44:367-76
6. Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, et al. 2002. Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: Phosphorylation of sucrose synthase is a possible factor. Plant Cell 14:619-28
7. Assmann SM, Wang XQ. 2001. From milliseconds to millions of years: guard cells and environmental responses. Curr. Opin. Plant Biol. 4:421-28
8. Bayley PM, Findlay WA, Martin SR. 1996. Target recognition by calmodulin: dissecting the kinetics and affinity of interaction using short peptide sequences. Protein Sci. 5:1215-28
9. Blaydes JP, Vojtesek B, Bloomberg GB, Hupp TR. 2000. The development and use of phospho-specific antibodies to study protein phosphorylation. Methods Mol. Biol. 99:177-89
10. 2+-binding proteins. Biochem. J. 353:1-12
11. Camoni L, Harper JF, Palmgren MG. 1998. 14-3-3 proteins activate a plant calcium-dependent protein kinase (CDPK). FEBS Lett. 430:381-84
12. Chaudhuri S, Seal A, DasGupta M. 1999. Autophosphorylation-dependent activation of a calcium-dependent protein kinase from groundnut. Plant Physiol. 120:859-66
13. Cheng SH, Willmann MR, Chen HC, Sheen J. 2002. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129:469-85
14. Dammann C, Ichida A, Hong B, Romanowsky SM, Hrabak EM, et al. 2003. Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol. 132:1840-48
15. Davis RJ. 1993. The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 268:14553-56
16. 2+ oscillations. Science 279:227-30
17. Edelman AM, Blumenthal DK, Krebs EG. 1987. Protein serine/threonine kinases. Annu. Rev. Biochem. 56:567-613
18. Estruch JJ, Kadwell S, Merlin E, Crossland L. 1994. Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc. Natl. Acad. Sci. USA 91:8837-41
19. Evans NH, McAinsh MR, Hetherington AM. 2001. Calcium oscillations in higher plants. Curr. Opin. Plant Biol. 4:415-20
20. Farmer PK, Choi JH. 1999. Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (Dc-CPK1) from carrot (Daucus carota L.). Biochim. Biophys. Acta 1434:6-17
21. Fasano JM, Massa GD, Gilroy S. 2002. Ionic signaling in plant responses to gravity and touch. J. Plant Growth Regul. 21:71-88
22. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, et al. 2002. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20:301-5
23. Furumoto T, Ogawa N, Hata S, Izui K. 1996. Plant calcium-dependent protein kinase-related kinases (CRKs) do not require calcium for their activities. FEBS Lett. 396:147-51
24. Gerber SA, Rush J, Stemman O, Kirschner MW, Gygi SP. 2003. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. USA 100:6940-45
25. Goldberg J, Nairn AC, Kuriyan J. 1996. Structural basis for the autoinhibition of calcium/calmodulin-dependent protein kinase I. Cell 84:875-87
26. Gong D, Gong Z, Guo Y, Chen X, Zhu JK. 2002. Biochemical and functional characterization of PKS11, a novel Arabidopsis protein kinase. J. Biol. Chem. 277:28340-50
27. Gong D, Gong Z, Guo Y, Zhu JK. 2002. Expression, activation, and biochemical properties of a novel Arabidopsis protein kinase. Plant Physiol. 129:225-34
28. Gong D, Guo Y, Jagendorf AT, Zhu JK. 2002. Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance. Plant Physiol. 130:256-64
29. Gong D, Zhang C, Chen X, Gong Z, Zhu J-K. 2002. Constitutive activation and transgenic evaluation of the function of an Arabidopsis PKS protein kinase. J. Biol. Chem. 277:42088-96
30. Guo Y, Halfter U, Ishitani M, Zhu JK. 2001. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383-400
31. Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK. 2002. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev. Cell 3:233-44
32. Halford NG, Hardie DG. 1998. SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol. Biol. 37:735-48
33. Halfter U, Ishitani M, Zhu JK. 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. USA 97:3735-40
34. Harmon AC, Gribskov M, Gubrium E, Harper JF. 2001. The CDPK superfamily of protein kinases. New Phytol. 151:175-83
35. 2+ signal? Trends Plant Sci. 5:154-59
36. Harmon AC, Yoo BC, McCaffery C. 1994. Pseudosubstrate inhibition of CDPK, a protein kinase with a cahnodulin-like domain. Biochemistry 33:7278-87
37. Harper JF, Huang JF, Lloyd SJ. 1994. Genetic identification of an autoinhibitor in CDPK, a protein kinase with a cahnodulin-like domain. Biochemistry 33:7267-77
38. Hetherington AM. 2001. Guard cell signaling. Cell 107:711-14
39. Honys D, Twell D. 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132:640-52
40. 2+/CaM-dependent kinases: from activation to function. Annu. Rev. Pharmacol. Toxicol. 41:471-505
41. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, et al. 2003. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132:666-80
42. Hua W, Liang S, Lu Y. 2003. A tobacco calmodulin-binding protein kinase differentially regulated by calmodulin isoforms. Biochem. J. 376:291-302
43. Huang J-F. 1996. Intramolecular regulation of a calcium-dependent protein kinase with a calmodulin-like regulatory domain. PhD thesis. Scripps Research Inst. 134 pp.
44. 2+-dependent protein kinase involves intramolecular binding of a calmodulin-like regulatory domain. Biochemistry 35:13222-30
45. Huang JZ, Hardin SC, Huber SC. 2001. Identification of a novel phosphorylation motif for CDPKs: phosphorylation of synthetic peptides lacking basic residues at P-3/P-4. Arch. Biochem. Biophys. 393:61-66
46. Huang JZ, Huber SC. 2001. Phosphorylation of synthetic peptides by a CDPK and plant SNF1-related protein kinase. Influence of proline and basic amino acid residues at selected positions. Plant Cell Physiol. 42:1079-87
47. 2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc. Natl. Acad. Sci. USA 97:6224-29
48. Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK. 2000. SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667-78
49. Kim KN, Cheong YH, Gupta R, Luan S. 2000. Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol. 124:1844-53
50. Knighton DR, Zheng JH, Ten Eyck LF, Ashford VA, Xuong NH, et al. 1991. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:407-14
51. Kobe B, Heierhorst J, Feil SC, Parker MW, Benian GM, et al. 1996. Giant protein kinases: domain interactions and structural basis of autoregulation. EMBO J. 15:6810-21
52. Komina O, Zhou Y, Sarath G, Chollet R. 2002. In vivo and in vitro phosphorylation of membrane and soluble forms of soybean nodule sucrose synthase. Plant Physiol. 129:1664-73
53. Kudla J, Xu Q, Harter K, Gruissem W, Luan S. 1999. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA 96:4718-23
54. Kumar S, Tamura K, Jakobsen IB, Nei M. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-45
55. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A. 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14:2627-41
56. Lee JY, Yoo BC, Harmon AC. 1998. Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. Biochemistry 37:6801-9
57. Lee SS, Cho HS, Yoon GM, Ahn JW, Kim HH, Pai HS. 2003. Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J. 33:825-40
58. Lindzen E, Choi JH. 1995. A carrot cDNA encoding an atypical protein kinase homologous to plant calcium-dependent protein kinases. Plant Mol. Biol. 28:785-97
59. Liu Z, Xia M, Poovaiah BW. 1998. Chimeric calcium/calmodulin-dependent protein kinase in tobacco: differential regulation by calmodulin isoforms. Plant Mol. Biol. 38:889-97
60. Lu SX, Hrabak EM. 2002. An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol. 128:1008-21
61. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. 2002. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14(Suppl):S389-S400
62. MacCoss MJ, McDonald WH, Saraf A, Sadygov R, Clark JM, et al. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. USA 99:7900-5
63. Martin ML, Busconi L. 2001. A rice membrane-bound calcium-dependent protein kinase is activated in response to low temperature. Plant Physiol. 125:1442-49
64. Martin SR, Bayley PM, Brown SE, Porumb T, Zhang M, Ikura M. 1996. Spectroscopic characterization of a high-affinity calmodulin-target peptide hybrid molecule. Biochemistry 35:3508-17
65. Newton AC. 2003. Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem J. 370:361-71
66. Nozawa A, Koizumi N, Sano H. 2001. An arabidopsis SNF1-related protein kinase, AtSR1, interacts with a calcium-binding protein, AtCBL2, of which transcripts respond to light. Plant Cell Physiol. 42:976-81
67. Patharkar OR, Cushman JC. 2000. A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. Plant J. 24:679-91
68. Patil S, Takezawa D, Poovaiah BW. 1995. Chimeric plant calcium/calmodulin-dependent protein-kinase gene with a neural visinin-like calcium-binding domain. Proc. Natl. Acad. Sci. USA 92:4897-901
69. Pearson RB, Kemp BE. 1991. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200:62-81
70. Pical C, Fredlund KM, Petit PX, Sommarin M, Moller IM. 1993. The outer membrane of plant mitochondria contains a calcium-dependent protein kinase and multiple phosphoproteins. FEBS Lett. 336:347-51
71. 2+-dependent protein kinase (CDPK) from Dunaliella tertiolecta (Chlorophyta). J. Phycol. 36:545-52
72. Ramachandiran S, Takezawa D, Wang W, Poovaiah BW. 1997. Functional domains of plant chimeric calcium/calmodulin-dependent protein kinase: regulation by autoinhibitory and visinin-like domains. J. Biochem. (Tokyo) 121:984-90
73. Resh MD. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451:1-16
74. Roberts DM, Harmon AC. 1992. Calcium-modulated proteins - Targets of intracellular calcium signals in higher plants. Annu. Rev. Plant Physiol. Mol. Biol. 43:375-414
75. Romeis T. 2001. Protein kinases in the plant defense response. Curr. Opin. Plant Biol. 4:407-14
76. Romeis T, Ludwig AA, Martin R, Jones JDG. 2001. Calcium-dependent protein kinases play an essential role in a plant defense response. EMBO J. 20:5556-67
77. Romeis T, Piedras P, Jones JDG. 2000. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12:803-15
78. Rudd JJ, Franklin-Tong VE. 2003. Signais and targets of the self-incompatibility response in pollen of Papaver rhoeas. J. Exp. Bot. 54:141-48
79. Saha P, Singh M. 1995. Characterization of a winged bean (Psophocarpus-tetragonolobus) protein-kinase with calmodulin-like domain regulation by autophosphorylation. Biochem. J. 30:205-10
80. Saijo Y, Hata S, Sheen J, Izui K. 1997. cDNA cloning and prokaryotic expression of maize calcium-dependent protein kinases. Biochim. Biophys. Acta 1350:109-14
81. Sanders D, Pelloux J, Brownlee C, Harper JF. 2002. Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401-S17
82. 2+/Calmodulin-dependent protein kinase. Role of the neural visinin-like domain in regulating autophosphorylation and calmodulin affinity. J. Biol. Chem. 275:30417-22
83. Sathyanarayanan PV, Poovaiah BW. 2002. Autophosphorylation-dependent inactivation of plant chimeric calcium/calmodulin-dependent protein kinase. Eur. J. Biochem. 269:2457-63
84. 2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900-2
85. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, et al. 1999. Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393-405
86. Subbaiah CC, Sachs MM. 2003. Molecular and cellular adaptations of maize to flooding stress. Ann. Bot. (London) 91:119-27
87. Szczegielniak J, Liwosz A, Jurkowski I, Loog M, Dobrowolska G, et al. 2000. Calcium-dependent protein kinase from maize seedlings activated by phospholipids. Eur. J. Biochem. 267:3818-27
88. Takezawa D, Ramachandiran S, Paranjape V, Poovaiah B. 1996. Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J. Biol. Chem. 271:8126-32
89. Tang GQ, Hardin SC, Dewey R, Huber SC. 2003. A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds. Plant J. 34:77-93
90. Tchieu JH, Fana F, Fink JL, Harper J, Nair TM, et al. 2003. The plantsP and plantsT functional genomics databases. Nucleic Acids Res. 31:342-44
91. 2+-dependent protein kinase is disrupted by insertions in the tether that connects the calmodulin-like domain to the kinase. Biochemistry 39:4004-11
92. Wang D, Harper JF, Gribskov M. 2003. Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae. Plant Physiol. 132:2152-65
93. 2+/calmodulin-dependent protein kinase. Plant Sci. 81:227-35
94. Watillon B, Kettmann R, Boxus P, Burny A. 1993. A calcium/calmodulin- binding serine/threonine protein kinase homologous to the mammalian type II calcium/calmodulin-dependent protein kinase is expressed in plant cells. Plant Physiol. 101:1381-84
95. Watillon B, Kettmann R, Boxus P, Burny A. 1995. Structure of a calmodulin-binding protein kinase gene from apple. Plant Physiol. 108:847-48
96. Xing T, Wang XJ, Malik K, Miki BL. 2001. Ectopic expression of an Arabidopsis calmodulin-like domain protein kinase-enhanced NADPH oxidase activity and oxidative burst in tomato protoplasts. Mol. Plant Microbe Interact. 14:1261-64
97. Xiong L, Schumaker KS, Zhu JK. 2002. Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165-S83
98. Yoo BC, Lee JY, Lucas WJ. 2002. Analysis of the complexity of protein kinases within the phloem sieve tube system. Characterization of Cucurbita maxima calrnodulin-like domain protein kinase 1. J. Biol. Chem. 277:15325-32
99. Zhang L, Liu BF, Liang S, Jones RL, Lu YT. 2002. Molecular and biochemical characterization of a calcium/calmodulin-binding protein kinase from rice. Biochem. J. 368:145-57
100. Zhang L, Lu YT. 2003. Calmodulin-binding protein kinases in plants. Trends Plant Sci. 8:123-27
101. 2+-dependent protein kinase. FEBS Lett. 410:126-30
102. Zhang XQ, Lund AA, Sarath G, Cerny RL, Roberts DM, Chollet R. 1999. Soybean nodule sucrose synthase (nodulin-100): further analysis of its phosphorylation using recombinant and authentic root-nodule enzymes. Arch. Biochem. Biophys. 371:70-82