Biochemical regulation of in vivo function of plant calcium-dependent protein kinases (CDPK)

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 7, 2013, Pages 1582-1589

  Liese, Anja ^a   Romeis, Tina ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

(Auto) phosphorylation; Calcium signaling; CDPK; EF hand; Protein kinase; Stress signal transduction

Indexed keywords

CALCIUM PROTEIN KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ABIOTIC STRESS; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; BINDING AFFINITY; BIOTIC STRESS; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME SUBSTRATE; HYDROGEN BOND; HYDROPHOBICITY; IN VIVO STUDY; INHIBITION KINETICS; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, PLANT; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLANTS; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 84878241131     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.10.024     Document Type: Review

References (77)

1. Knight H. Calcium signaling during abiotic stress in plants. Int. Rev. Cytol. 1999, vol. 195:269-324. Academic Press. W.J. Kwang (Ed.).
2. Sanders D., Brownlee C., Harper J.F. Communicating with calcium. Plant Cell 1999, 11:691-706.
3. Kudla J., Batistič O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563.
4. Dodd A.N., Kudla J., Sanders D. The language of calcium signaling. Annu. Rev. Plant Biol. 2010, 61:593-620.
5. Knight H., Knight M.R. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 2001, 6:262-267.
6. 2+ signalling systems. Trends Plant Sci. 1998, 3:32-36.
7. McAinsh M.R., Pittman J.K. Shaping the calcium signature. New Phytol. 2010, 181:275-294.
8. 2+ signalling pathways in plant cells. New Phytol. 2001, 151:7-33.
9. Webb A.A.R., McAinsh M.R., Taylor J.E., Hetherington A.M. Calcium ions as intracellular second messengers in higher plants. Adv. Bot. Res. 1996, vol. 22:45-96. Academic Press. J.A. Callow (Ed.).
10. Sanders D., Pelloux J., Brownlee C., Harper J.F. Calcium at the crossroads of signaling. Plant Cell 2002, 14:S401-S417.
11. Scrase-Field S.A.M.G., Knight M.R. Calcium: just a chemical switch?. Curr. Opin. Plant Biol. 2003, 6:500-506.
12. Christodoulou J., Malmendal A., Harper J.F., Chazin W.J. Evidence for differing roles for each lobe of the calmodulin-like domain in a calcium-dependent protein kinase. J. Biol. Chem. 2004, 279:29092-29100.
13. Chandran V., Stollar E.J., Lindorff-Larsen K., Harper J.F., Chazin W.J., Dobson C.M., Luisi B.F., Christodoulou J. Structure of the regulatory apparatus of a calcium-dependent protein kinase (CDPK): a novel mode of calmodulin-target recognition. J. Mol. Biol. 2006, 357:400-410.
14. Rutschmann F., Stalder U., Piotrowski M., Oecking C., Schaller A. LeCPK1, a calcium-dependent protein kinase from tomato. Plasma membrane targeting and biochemical characterization. Plant Physiol. 2002, 129:156-168.
15. Wernimont A.K., Artz J.D., Finerty P., Lin Y.-H., Amani M., Allali-Hassani A., Senisterra G., Vedadi M., Tempel W., Mackenzie F., Chau I., Lourido S., Sibley L.D., Hui R. Structures of apicomplexan calcium-dependent protein kinases reveal mechanism of activation by calcium. Nat. Struct. Mol. Biol. 2010, 17:596-601.
16. Wernimont A.K., Amani M., Qiu W., Pizarro J.C., Artz J.D., Lin Y.-H., Lew J., Hutchinson A., Hui R. Structures of parasitic CDPK domains point to a common mechanism of activation. Proteins 2011, 79:803-820.
17. Cheng S.-H., Willmann M.R., Chen H.-C., Sheen J. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 2002, 129:469-485.
18. 2+-dependent protein kinase is important for substrate recognition. Plant Cell 2010, 22:1592-1604.
19. Witte C.-P., Keinath N., Dubiella U., Demoulière R., Seal A., Romeis T. Tobacco calcium-dependent protein kinases are differentially phosphorylated in vivo as part of a kinase cascade that regulates stress response. J. Biol. Chem. 2010, 285:9740-9748.
20. Weljie A.M., Clarke T.E., Juffer A.H., Harmon A.C., Vogel H.J. Comparative modeling studies of the calmodulin-like domain of calcium-dependent protein kinase from soybean. Proteins 2000, 39:343-357.
21. Yoo B.-C., Harmon A.C. Intramolecular binding contributes to the activation of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 1996, 35:12029-12037.
22. Harmon A.C., Yoo B.C., McCaffery C. Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 1994, 33:7278-7287.
23. Harper J.F., Huang J.F., Lloyd S.J. Genetic identification of an autoinhibitor in CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 1994, 33:7267-7277.
24. Klimecka M., Muszynska G. Structure and functions of plant calcium-dependent protein kinases. Acta Biochim. Pol. 2007, 54:219-233.
25. Romeis T., Ludwig A.A., Martin R., Jones J.D.G. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 2001, 20:5556-5567.
26. 2+-dependent protein kinase CPK3 is required for sphingolipid-induced cell death in Arabidopsis. Cell Death Differ. 2012, (advance online publication). 10.1038/cdd.2012.114.
27. Ojo K.K., Larson E.T., Keyloun K.R., Castaneda L.J., DeRocher A.E., Inampudi K.K., Kim J.E., Arakaki T.L., Murphy R.C., Zhang L., Napuli A.J., Maly D.J., Verlinde C.L.M.J., Buckner F.S., Parsons M., Hol W.G.J., Merritt E.A., Van Voorhis W.C. Toxoplasma gondii calcium-dependent protein kinase 1 is a target for selective kinase inhibitors. Nat. Struct. Mol. Biol. 2010, 17:602-607.
28. 2+-regulatory region from soybean calcium-dependent protein kinase-α. J. Biol. Chem. 2004, 279:35494-35502.
29. 2+ signal?. Trends Plant Sci. 2000, 5:154-159.
30. Zhao Y., Pokutta S., Maurer P., Lindt M., Franklin R.M., Kappes B. Calcium-binding properties of a calcium-dependent protein kinase from Plasmodium falciparum and the significance of individual calcium-binding sites for kinase activation. Biochemistry 1994, 33:3714-3721.
31. Franz S., Ehlert B., Liese A., Kurth J., Cazalé A.-C., Romeis T. Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol. Plant 2011, 4:83-96.
32. 2+ signals through plant protein kinases. Annu. Rev. Plant Biol. 2004, 55:263-288.
33. Boudsocq M., Droillard M.-J., Regad L., Laurière C. Characterization of Arabidopsis calcium-dependent protein kinases: activated or not by calcium?. Biochem. J. 2012, 447:291-299.
34. Lee J.-Y., Yoo B.-C., Harmon A.C. Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybeane. Biochemistry 1998, 37:6801-6809.
35. 2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 2007, 405:199-221.
36. Grabarek Z. Structural basis for diversity of the EF-hand calcium-binding proteins. J. Mol. Biol. 2006, 359:509-525.
37. Sigrist C.J.A., Cerutti L., de Castro E., Langendijk-Genevaux P.S., Bulliard V., Bairoch A., Hulo N. PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 2010, 38:D161-D166.
38. 2+ affinities. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8023-8028.
39. Kanchiswamy C., Takahashi H., Quadro S., Maffei M., Bossi S., Bertea C., Zebelo S., Muroi A., Ishihama N., Yoshioka H., Boland W., Takabayashi J., Endo Y., Sawasaki T., Arimura G.-I. Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol. 2010, 10:97.
40. Chaudhuri S., Seal A., DasGupta M. Autophosphorylation-dependent activation of a calcium-dependent protein kinase from groundnut. Plant Physiol. 1999, 120:859-866.
41. Harmon A.C., Putnam-Evans C., Cormier M.J. A calcium-dependent but calmodulin-independent protein kinase from soybean. Plant Physiol. 1987, 83:830-837.
42. Saha P., Singh M. Characterization of a winged bean (Psophocarpus tetragonolobus) protein kinase with calmodulin-like domain: regulation by autophosphorylation. Biochem. J. 1995, 305:205-210.
43. Romeis T., Piedras P., Jones J.D.G. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 2000, 12:803-816.
44. Nühse T.S., Stensballe A., Jensen O.N., Peck S.C. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 2004, 16:2394-2405.
45. de la Fuente S., van Bentem D., Anrather I., Dohnal E., Roitinger E., Csaszar J., Joore J., Buijnink A., Carreri C., Forzani Z.J., Lorkovic A., Barta D., Lecourieux A., Verhounig C., Jonak H. Hirt Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis. J. Proteome Res. 2008, 7:2458-2470.
46. Witte C.P., Noël L., Gielbert J., Parker J., Romeis T. Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol. Biol. 2004, 55:135-147.
47. Hegeman A.D., Rodriguez M., Han B.W., Uno Y., Phillips G.N.J., Hrabak E.M., Cushman J.C., Harper J.F., Harmon A.C., Sussman M.R. A phyloproteomic characterization of in vitro autophosphorylation in calcium-dependent protein kinases. Proteomics 2006, 6:3649-3664.
48. Chehab E.W., Patharkar O.R., Hegeman A.D., Taybi T., Cushman J.C. Autophosphorylation and subcellular localization dynamics of a salt- and water deficit-induced calcium-dependent protein kinase from ice plant. Plant Physiol. 2004, 135:1430-1446.
49. Belin C., de Franco P.-O., Bourbousse C., Chaignepain S., Schmitter J.-M., Vavasseur A., Giraudat J., Barbier-Brygoo H., Thomine S. Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol. 2006, 141:1316-1327.
50. Yang K.-Y., Liu Y., Zhang S. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:741-746.
51. Vlad F., Rubio S., Rodrigues A., Sirichandra C., Belin C., Robert N., Leung J., Rodriguez P.L., Laurière C., Merlot S. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 2009, 21:3170-3184.
52. Boudsocq M., Droillard M.J., Barbier-Brygoo H., Laurière C. Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol. Biol. 2007, 63:491-503.
53. Jin H., Liu Y., Yang K.-Y., Kim C.Y., Baker B., Zhang S. Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J. 2003, 33:719-731.
54. Ludwig A.A., Romeis T., Jones J.D.G. CDPK-mediated signalling pathways: specificity and cross-talk. J. Exp. Bot. 2004, 55:181-188.
55. Tena G., Boudsocq M., Sheen J. Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 2011, 14:519-529.
56. Harper J.F., Harmon A.C. Plants, symbiosis and parasites: a calcium signalling connection. Nat. Rev. Mol. Cell Biol. 2005, 6:555-566.
57. Lu S.X., Hrabak E.M. An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol. 2002, 128:1008-1021.
58. Patharkar O., Cushman J.C. A novel coiled-coil protein co-localizes and interacts with a calcium-dependent protein kinase in the common ice plant during low-humidity stress. Planta 2006, 225:57-73.
59. Patharkar O.R., Cushman J.C. A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. Plant J. 2000, 24:679-691.
60. Raichaudhuri A., Bhattacharyya R., Chaudhuri S., Chakrabarti P., DasGupta M. Domain analysis of a groundnut calcium-dependent protein kinase. J. Biol. Chem. 2006, 281:10399-10409.
61. 2+ sensor protein kinases. Nature 2010, 464:418-422.
62. Curran A., Chang I.-F., Chang C.-L., Garg S., Miguel R.M., Barron Y.D., Li Y., Romanowsky S., Cushman J.C., Gribskov M., Harmon A., Harper J.F. Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Front. Plant Sci. 2011, 2.
63. Ludwig A.A., Saitoh H., Felix G., Freymark G., Miersch O., Wasternack C., Boller T., Jones J.D.G., Romeis T. Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10736-10741.
64. Kobayashi M., Ohura I., Kawakita K., Yokota N., Fujiwara M.I., Shimamoto K., Doke N., Yoshioka H. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 2007, 19:1065-1080.
65. Kobayashi M., Yoshioka M., Asai S., Nomura H., Kuchimura K., Mori H., Doke N., Yoshioka H. StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst. New Phytol. 2012, 196:223-237.
66. Geiger D., Maierhofer T., Al-Rasheid K.A.S., Scherzer S., Mumm P., Liese A., Ache P., Wellmann C., Marten I., Grill E., Romeis T., Hedrich R. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci. Signal. 2011, 4. (ra32).
67. Vahisalu T., Kollist H., Wang Y.-F., Nishimura N., Chan W.-Y., Valerio G., Lamminmaki A., Brosche M., Moldau H., Desikan R., Schroeder J., Kangasjarvi J. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 2008, 452:487-491.
68. Ma Y., Szostkiewicz I., Korte A., Moes D., Yang Y., Christmann A., Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 2009, 324:1064-1068.
69. Park S.-Y., Fung P., Nishimura N., Jensen D.R., Fujii H., Zhao Y., Lumba S., Santiago J., Rodrigues A., Chow T.-F.F., Alfred S.E., Bonetta D., Finkelstein R., Provart N.J., Desveaux D., Rodriguez P.L., McCourt P., Zhu J.-K., Schroeder J.I., Volkman B.F., Cutler S.R. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 2009, 324:1068-1071.
70. Koornneef M., Reuling G., Karssen C.M. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol. Plant. 1984, 61:377-383.
71. Leung J., Bouvier-Durand M., Morris P.C., Guerrier D., Chefdor F., Giraudat J. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 1994, 264:1448-1452.
72. Meyer K., Leube M.P., Grill E. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 1994, 264:1452-1455.
73. Rodriguez P.L., Benning G., Grill E. ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett. 1998, 421:185-190.
74. Brandt B., Brodsky D.E., Xue S., Negi J., Iba K., Kangasjärvi J., Ghassemian M., Stephan A.B., Hu H., Schroeder J.I. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10593-10598.
75. Scherzer S., Maierhofer T., Al-Rasheid K.A.S., Geiger D., Hedrich R. Multiple calcium-dependent kinases modulate ABA-activated guard cell anion channels. Mol. Plant 2012, (advance online publication). 10.1093/mp/sss1084.
76. 2+)-permeable channels and stomatal closure. PLoS Biol. 2006, 4:e327.
77. Munemasa S., Hossain M.A., Nakamura Y., Mori I.C., Murata Y. The Arabidopsis calcium-dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiol. 2011, 155:553-561.