Structure and functions of plant calcium-dependent protein kinases
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Calcium ions as second messengers play an essential role in many important cellular processes. In plants, transient changes in calcium content in the cytosol (calcium signatures) have been observed during growth, development and under stress conditions. Such diverse functions require many different calcium sensors. One of the largest and most differentiated group of calcium sensors are protein kinases, among them calcium-dependent protein kinases (CDPKs) which were identified only in plants and protists. CDPKs have a regulatory domain which is able to bind calcium ions. For regulation of CDPKs activities not only calcium ions but also specific phospholipids and autophosphorylation are responsible. CDPKs have many different substrates, which reflects the diversity of their functions. Potential protein substrates of CDPK are involved in carbon and nitrogen metabolism, phospholipid synthesis, defense responses, ion and water transport, cytoskeleton organization, transcription and hormone responses. Presently, participation of CDPKs in stress signal transduction pathways (e.g., cold, drought, high salinity, wounding) is intensively studied in many laboratories. An intriguing, but still not fully clarified problem is the cross-talk via CDPKs among different signaling pathways that enables signal integration at different levels and ensure appropriate downstream responses.
- Abbasi F, Onodera H, Toki S, Tanaka H, Komatu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55: 541-552.
- Abo-El-Saad M, Wu R (1995) A rice membrane calcium-dependent protein kinase is induced by gibberellin. Plant Physiol 108: 787-793.
- Allwood EG, Smertenko AP, Hussey PJ (2001) Phosphorylation of plant actin-depolymerising factor by calmodulin-like domain protein kinase. FEBS Lett 499: 97-100.
- Anil VS, Rao SK (2000) Calcium-mediated signaling during sandalwood somatic embryogenesis. Role for exogenous calcium as second messenger. Plant Physiol 123: 1301-1311.
- Anil VS, Rao SK (2001) Purification and characterization of a Ca2+-dependent protein kinase from sandalwood (Santalum album L.): evidence for Ca2+-induced conformational changes. Phytochemistry 58: 203-212.
- Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, Takano M, Sato M, Furuhashi H, Mujin T, Takaiwa F, 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: 619-628.
- Barker LDP, Templeton MD, Ferguson IB (1998) A 67-kDa plasma-membrane-bound Ca2+-stimulated protein kinase active in sink tissue of higher plants. Planta 205: 197-204.
- Berkowitz G, Zhang X, Mercier R, Leng Q, Lawton M (2000) Co-expression of a calcium-dependent protein kinase with inward rectified guard cell K+ channel KAT1 alters current parameters in Xenopus laevis oocytes. Plant Cell Physiol 41: 785-790.
- Botella JR, Arteca JM, Somodevilla M, Arteca RN (1996) Calcium-dependent protein kinase gene expression in response to physical and chemical stimuli in mungbean (Vigna radiata). Plant Mol Biol 30: 1129-1137.
- Camoni L, Harper JF, Palmgren MG (1998) 14-3-3 proteins activate a plant calcium-dependent protein kinase (CDPK). FEBS Lett 430: 381-384.
- Chaudhuri S, Seal A, Dasgupta M (1999) Autophosphorylation-dependent activation of calcium-dependent protein kinase from groundnut. Plant Physiol 120: 859-866.
- Cheng S-H, Sheen J, Gerrish C, Bolwell GP (2001) Molecural identification of phenylalanine ammonia-lyase as a substrate of a specific constitutively active Arabidopsis CDPK expressed in maize protoplasts. FEBS Lett 503: 185-188.
- Cheng S-H, Willmann MR, Chen H-Ch, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent kinase gene family. Plant Physiol 129: 469-485.
- Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661-677.
- Chico JM, Raíces M, Téllez-Iñón MT, Ulloa RM (2002) A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol 128: 256-270.
- Christodoulou J, Malmendal A, Harper JF, Chazin WJ (2004) Evidence for differing roles for each lobe of the calmodulin-like domein in a calcium-dependent protein kinase. J Biol Chem 279: 29092-29100.
- Dammann Ch, Ichida A, Hong B, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol 132: 1840-1848.
- Davletova S, Mészáros T, Miskolczi P, Oberschall A, Török K, Maryar Z, Dudits D, Deák M (2001) Auxin and heat shock activation of a novel member of the calmodulin like domain protein kinase gene family in cultured alfalfa cells. J Exp Bot 52: 215-221.
- Douglas P, Moorhead G, Hong Y, Morrice N, MacKintosh C (1998) Purification of a nitrate reductase kinase from Spinacea aleracea leaves, and its identification as a calmodulin-domain protein kinase. Planta 206: 435-442.
- Ellard-Ivey M, Hopkins RB, White TJ, Lomax TL (1999) Cloning, expression and N-terminal myristoylation of CpCPK1, a calcium-dependent protein kinase from zucchini (Cucurbita pepo L.). Plant Mol Biol 39: 199-208.
- Estruch JJ, Kadwell S, Merlin E, Crossland L (1994) Cloning and characterization of maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci USA 91: 8837-8841.
- Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4: 415-420.
- Farmer PK, Choi JM (1999) Calcium and phospholipid activation of recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.) Biochim Biophys Acta 1434: 6-17.
- Ganguly S, Singh M (1998) Characterization of a second calcium-dependent protein kinase from winged bean. Phytochemistry 48: 61-70.
- Ganguly S, Singh M (1999) Purification and characterization of a protein phosphatase from winged bean. Phytochemistry 52: 239-246.
- Grabski S, Arnoys E, Busch B, Schindler M (1998) Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiol 116: 279-290.
- Grover M, Sharma AK, Dhingra A, Maheshwari SC, Tyagi AK (1998) Regulation of plastid gene expression in rice involves calcium and protein phosphatases/kinases for signal transduction. Plant Science 137: 185-190.
- Harmon AC (2003) Calcium-regulated protein kinases of plants. Gravit Space Biol Bull 16: 83-90.
- Harmon AC, Lee J-Y, Yoo BC, Shao J (1996) Plant membrane-associated protein kinases. In: Membranes: Specialized Functions in Plant Cells (Smallwood M ed.) pp 137-150, Bios Scientific Publishers, Oxford.
- Harmon AC, Gribskov M, Harper JF (2000) CDPKs-a kinase for every signal? Trends Plant Sci 5: 154-159.
- Harmon AC, Gribskov M, Gubrium E, Harper JF (2001) The CDPK superfamily of protein kinases. New Phytologist 151: 175-183.
- Harper JF, Harmon AC (2005) Plants, symbiosis and parasites: a calcium signaling connection. Nat Rev Mol Cell Biol 6: 555-566.
- Harper JF, Binder BM, Sussman MR (1993) Calcium and lipid regulation of an Arabidopsis protein kinase expressed in Escherichia coli. Biochemistry 32: 3282-3290.
- Harper JF, Breton G, Harmon AC (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55: 263-288.
- Hegeman AD, Rodriguez M, Han B-W, Uno Y, Phillips GN Jr, Hrabak EM, Cushman JC, Harper JF, Harmon AC, Sussman MR (2006) A phyloproteomic characterization of in vitro autophosphorylation in calcium-dependent protein kinases. Proteomics 6: 3649-3664.
- Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17: 159-187.
- Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu J-K, Harmon A C (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132: 666-680.
- Huang JZ, Huber SC (2001) Phosphorylation of synthetic peptides by a CDPK and plant SNF-1-related protein kinase. Influence of proline and basic amino acid residues at selected positions. Plant Cell Physiol 42: 1079-1087.
- 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.
- Huber SC, Hardin SC (2004) Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels. Curr Opin Plant Biol 7: 318-322.
- Hwang I, Sze H, Harper JF (2000) A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97: 6224-6229.
- Jaworski K, Szmidt-Jaworska A, Tretyn A, Koncewicz J (2003) Biochemical evidence for a calcium-dependent protein kinase from Pharbitis nil and its involvement in photoperiodic flower induction. Phytochemistry 62: 1047-1055.
- Kawasaki H, Nakayama S, Kretsinger RH (1998) Classification and evolution of EF-hand proteins. Biometals 11: 277-295.
- Knight H, Knight MR (2000) Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis. J Exp Bot 51: 1679-1686.
- Knight H, Knight MR (2001) Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci 6: 262-267.
- Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489-503.
- Komatsu S, Li W, Konishi H, Yoshikawa M, Konisi T, Yang G (2001) Characterization of a Ca2+-dependent protein kinase from rice root: differential response to cold and regulation by abscisic acid. Biol Pharm Bull 24: 1316-1319.
- Kuntz C, Chang A, Faure JD, Clarke AE, Polya GM, Anderson MA (1996) Phosphorylation of a style S-RNases by Ca2+-dependent protein kinases from pollen tubes. Sex Plant Reprod 9: 25-34.
- Kwak S-H, Lee S-H (1997) The requirements for Ca2+, protein phosphorylation, and dephosphorylation for ethylene signal transduction in Pisum sativum L. Plant Cell Physiol 38: 1142-1149.
- Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57: 1341-1351.
- Lee J-Y, Yoo BC, Harmon AC (1998) Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. Biochemistry 37: 6801-6809.
- Lee SS, Cho HS, Yoon GM, Ahn J-W, Kim H-H, Pai H-S (2003) Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J 33: 825-840.
- León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52: 1-9.
- Li WG, Komatsu S (2000) Cold-induced calcium-dependent protein kinase(s) in rice (Oryza sativa L.) seedling stem tissues. Theor Appl Genet 101: 355-363.
- Li J, Lee YR, Assmann SM (1998) Guard cells posses a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol 116: 785-795.
- Loog M, Toomik R, Sak K, Muszyńska G, Järv J, Ek P (2000) Peptide phosphorylation by calcium-dependent protein kinase from maize seedlings. Eur J Biochem 267: 337-343.
- Lu SX, Hrabak EM (2002) An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol 128: 1008-1021.
- Ludwig AA, Romeis T, Jones JDG (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55: 181-188.
- Ludwig AA, Hiromasa S, Felix G, Fraymark G, Miersz O, Wasternack C, Boller T, Jones JDG, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signalling controls stress responses in plants. Proc Natl Acad Sci USA 102: 10736-10741.
- MacIntosh GC, Ulloa RM, Raíces M, Téllez-Iñón MT (1996) Changes in calcium-dependent protein kinase activity during in vitro tuberization in potato. Plant Physiol 112: 1541-1550.
- Maréchal E, Hiratsuka K, Delgado J, Nairn A, Qin J, Chait BT, Chua N-H (1999) Modulation of GT-1 DNA-binding activity by calcium-dependent phosphorylation. Plant Mol Biol 40: 373-386.
- Martin ML, Busconi L (2001) A rice membrane-bound calcium-dependent protein kinase is activated in response to low temperature. Plant Physiol 125: 1442-1449.
- McCubbin AG, Ritchie SM, Swanson SJ, Gilroy S (2004) The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar functions. Plant J 39: 206-218.
- McMichael RW Jr, Bachmann M, Huber SC (1995a) Spinach leaf sucrose-phosphate synthase and nitrate reductase are phosphorylated/inactivated by multiple protein kinases in vitro. Plant Physiol 108: 1077-1082.
- McMichael RW Jr, Kochansky J, Klein RR, Huber SC (1995b) Characterization of the substrate specificity of sucrose-phosphate synthase protein kinase. Arch Biochem Biophys 321: 71-75.
- Meshi T, Moda I, Minami M, Okanami M, Iwabuchi M (1998) Conserved Ser residues in the basic region of the bZIP-type transcription factor HBP-1a(17): importance in DNA binding and possibile targets for phosphorylation. Plant Mol Biol 36: 125-136.
- Moorhead G, Douglas P, Cotelle V, Harthill J, Morrice N, Meek S, Deiting U, Stitt M, Scarabel M, Aitken A, MacKintosh C (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J 18: 1-12.
- Morello L, Frattini M, Giani S, Christou P, Breviario D (2000) Overexpression of the calcium-dependent protein kinase OsCDPK2 in transgenic rice is expressed by light in leaves and disrupts seed development. Transgenic Res 9: 453-462.
- Moutinho A, Trewavas AJ, Malhó R (1998) Relocation of Ca2+-dependent protein kinase activity during pollen tube reorientation. Plant Cell 10: 1499-1509.
- Murillo I, Jaeck E, Cordero J, San Segundo B (2001) Transcriptional activation of maize calcium-dependent protein kinase gene in response to fungal elicitors and infection. Plant Mol Biol 45: 145-158.
- Nakai T, Konishi T, Zhang XQ, Chollet R, Tonouchi N, Tsuchida T, Yoshinaga F, Mori H, Sakai F, Hayashi T (1998) An increase in apparent affinity for sucrose of mung bean sucrose synthase is coused by in vitro phosphorylation or directed mutagenesis of Ser 11. Plant Cell Physiol 39: 1337-1341.
- Neumann GM, Thomas I, Polya GM (1996) Identification of the site on potato carboxy peptidase inhibitor that is phosphorylated by plant calcium-dependent protein kinase. Plant Science 114: 45-51.
- Ogawa N, Yabuta N, Ueno Y, Izui K (1998) Characterization of a maize Ca2+-dependent protein kinase phosphorylating phosphoenolpyruvate carboxylase. Plant Cell Physiol 39: 1010-1019.
- 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: 679-691.
- Patharkar OR, Cushman JC (2006) 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 225: 57-73.
- Raices M, Gargantini PR, Chinchilla D, Crespi M, Téllez-Iñón MT, Ulloa RM (2003) Regulation of CDPK isoforms during tuber development. Plant Mol Biol 52: 1011-1024.
- 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 121: 984-990.
- Reddy VS, Reddy ASN (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65: 1745-1776.
- Roberts DM, Harmon AC (1992) Calcium-modulated proteins-targets of intracellular calcium signals in higher plants. Annu Rev Plant Physiol Plant Mol Biol 43: 375-414.
- Rojo E, León J, Sánchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20: 135-142.
- 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: 803-815.
- Romeis T, Ludwig AA, Martin R, Jones JDG (2001) Calcium-dependent protein kinases play an essential role in a plant defence. EMBO J 20: 5556-5567.
- Rudd JJ, Franklin-Tong VE (2001) Unravelling response-specificity in Ca2+ signaling pathways in plant cells. New Phytologist 151: 7-33.
- Saha P, Singh M (1995) Characterization of a winged bean (Psophocarpus tetragonolobus) protein kinase with calmodulin-like domain: regulation by autophosphorylation. Biochem J 305: 205-210.
- Saijo Y, Hata S, Sheen J, Izui K (1997) cDNA cloning and prokaryotic expression of maize calcium-dependent protein kinases. Biochim Biophys Acta 1350: 109-114.
- Saijo Y, Hata S, Kyozuka J, Shimanoto K, Izui K (2000) Over-expession of a single Ca 2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23: 319-327.
- Sano T, Higaki T, Handa K, Kadota Y, Kuchitsu K, Hasezawa S, Hoffmann A, Endter J, Zimmermann U, Hedrich R, Roitsch T (2006) Calcium ions are involved in the delay of plant cell cycle progression by abiotic stresses. FEBS Lett 580: 597-602.
- Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14: S401-S417.
- Schaller GE, Harmon AC, Sussman MR (1992) Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat. Biochemistry 31: 1721-1727.
- Sebastià CH, Hardin SC, Clouse SD, Kieber JJ, Huber SC (2004) Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch Biochem Biophys 428: 81-91.
- Sehnke PC, Rosenquist M, Alsterfjord M, De Lille J, Sommarin M, Larsson C, Ferl RJ (2002) Evolution and isoform specificity of plant 14-3-3 proteins. Plant Mol Biol 50: 1011-1018.
- Sharma VK, Jain PK, Malik MK, Maheshwari SC, Khurana JP (1997) Light- and calcium-modulated phosphorylation of proteins from wheat seedlings. Phytochemistry 44: 781-786.
- Sharma A, Matsuoka M, Tanaka H, Komatu S (2001) Antisense inhibition of a BRI1 receptor reveals additional protein kinase signaling components downstream to the perception of brassinosteroids in rice. FEBS Lett 507: 346-350.
- Smertenko AI, Jiang Ch-J, Simmons NJ, Weeds AG, Davies DR, Hussey PJ (1998) Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by calcium-stimulated protein kinase and is essential for the control of functional activity. Plant J 14: 187-193.
- Szczegielniak J, Liwosz A, Jurkowski I, Loog M, Dobrowolska G, Ek P, Harmon AC, Muszyńska G (2000) Calcium-dependent protein kinase from maize seedlings activated by phospholipids. Eur J Biochem 267: 3818-3827.
- Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, Hormon AC, Muszyńska G (2005) A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol 139: 1970-1983.
- Tähtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M (1997) The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203: 442-447.
- Ullanat R, Javabaskaran C (2002) Distinct light-, cytokinin- and tissue-specific regulation of calcium dependent protein kinase gene expression in cucumber (Cucumber sativus). Plant Sci 162: 153-163.
- Urao T, Katagiri T, Mizoguchi T, Yamaguchi-Shinozaki K, Hayashida N, Shinozaki K (1994) Two genes that encode Ca2+-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol Gen Genet 244: 331-340.
- Watillon B, Kettman R, Boxus P, Burny A (1993) A calcium/calmodulin-binding serine/threonine protein kinase homologous to the mammalian type II calcium/calmodulin protein kinase is expressed in plant cells. Plant Physiol 101: 1381-1384.
- Yang W, Boss WF (1994) Regulation of phosphatidylinositol 4-kinase by protein activator PIK-A49. J Biol Chem 269: 3852-3857.
- Yang G, Shen S, Yang S, Komatsu S (2003) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced in response to cold and gibberellin. Plant Physiol Biochem 41: 369-374.
- Yoon GM, Cho HS, Ha HJ, Liu JR, Lee HP (1999) Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol Biol 39: 991-1001.
- Yu X-Ch, Li M-J, Gao G-F, Feng H-Z, Geng X-Q, Peng Ch-C, Zhu S-Y, Wang X-J, Shen Y-Y, Zhang D-P (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140: 558-579.
- Zhang XQ, Chollet R (1997) Seryl-phosphorylation of soybean nodule sucrose synthase (nodulin-100) by a Ca2+-dependent protein kinase. FEBS Lett 410: 126-130.
- Zhang M, Liang S, Lu Y-T (2005) Cloning and functional characterization of NtCPK4, a new tobacco calcium-dependent protein kinase. Biochem Biophys Acta 1729: 174-185.
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