Plant Physiology 132:666-680 (2003)
© 2003 American Society of Plant Biologists
RESEARCH PAPERS ON SYSTEMS BIOLOGY/GENOMICS/BIOINFORMATICS
The Arabidopsis CDPK-SnRK Superfamily of Protein Kinases
Estelle M. Hrabak*,
Catherine W.M. Chan,
Michael Gribskov,
Jeffrey F. Harper,
Jung H. Choi,
Nigel Halford,
Jörg Kudla,
Sheng Luan,
Hugh G. Nimmo,
Michael R. Sussman,
Martine Thomas,
Kay Walker-Simmons,
Jian-Kang Zhu and
Alice C. Harmon
Department of Plant Biology and Program in Genetics, University of New Hampshire, 46 College Road, Durham, New Hampshire 03824 (E.M.H.); Biotechnology Center, University of Wisconsin, 425 Henry Mall, Madison, Wisconsin 53706 (C.W.M.C., M.R.S.); San Diego Supercomputer Center, University of California, 9500 Gilman Drive, La Jolla, California 92093–0537 (M.G.); Department of Cell Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037 (J.F.H.); School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332 (J.H.C.); Institute for Arable Crops Research-Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol BS41 9AF, United Kingdom (N.H.); Molekulare Botanik, Universität Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany (J.K.); Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (S.L.); Plant Molecular Science Group, Division of Biochemistry and Molecular Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom (H.G.N.); Laboratoire de Biologie du Developement des Plantes, Institut de Biotechnologie des Plantes, Unité Mixte de Recherche Centre National de la Recherche Scientifique 8618, Universite de Paris-Sud, Orsay, France (M.T.); United States Department of Agriculture, Agriculture Research Service, Room 4–2210, George Washington Carver Building, 5601 Sunnyside Avenue, Beltsville, Maryland 20705–5139 (K.W.-S.); Department of Plant Sciences, University of Arizona, 303 Forbes, Tucson, Arizona 85721 (J.-K.Z.); and Department of Botany, Plant Molecular and Cellular Biology Program, P.O. Box 118526, University of Florida, Gainesville, Florida 32611–8526 (A.C.H.)
The CDPK-SnRK superfamily consists of seven types of serine-threonine protein kinases: calcium-dependent protein kinase (CDPKs), CDPK-related kinases (CRKs), phosphoenolpyruvate carboxylase kinases (PPCKs), PEP carboxylase kinase-related kinases (PEPRKs), calmodulin-dependent protein kinases (CaMKs), calcium and calmodulin-dependent protein kinases (CCaMKs), and SnRKs. Within this superfamily, individual isoforms and subfamilies contain distinct regulatory domains, subcellular targeting information, and substrate specificities. Our analysis of the Arabidopsis genome identified 34 CDPKs, eight CRKs, two PPCKs, two PEPRKs, and 38 SnRKs. No definitive examples were found for a CCaMK similar to those previously identified in lily (Lilium longiflorum) and tobacco (Nicotiana tabacum) or for a CaMK similar to those in animals or yeast. CDPKs are present in plants and a specific subgroup of protists, but CRKs, PPCKs, PEPRKs, and two of the SnRK subgroups have been found only in plants. CDPKs and at least one SnRK have been implicated in decoding calcium signals in Arabidopsis. Analysis of intron placements supports the hypothesis that CDPKs, CRKs, PPCKs and PEPRKs have a common evolutionary origin; however there are no conserved intron positions between these kinases and the SnRK subgroup. CDPKs and SnRKs are found on all five Arabidopsis chromosomes. The presence of closely related kinases in regions of the genome known to have arisen by genome duplication indicates that these kinases probably arose by divergence from common ancestors. The PlantsP database provides a resource of continuously updated information on protein kinases from Arabidopsis and other plants.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.102.011999.
Note Added in Proof
Two additional references may be of interest to readers.
Kim K-N, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium-sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 14: 411–423
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: S389–S400
1 This work was supported by the National Science Foundation (grant nos. DBI–9975808 and MCB-9973770 to A.C.H., IBN–9728563 to M.R.S., IBN–9416038 and MCB–9723539 to J.F.H., and DBI–9975808 to E.M.H., A.C.H., J.F.H., and M.G.), by the Deutsche Forschungsgemeinschaft (grant nos. Ku 931/3–2 and Ku931/4–1 to J.K.); by the U.S. Department of Agriculture (grant nos. 95–37304-2364 to M.R.S. and 98–35304–6510 to E.M.H.), and by the National Institutes of Health (grant no. R01GM59138 to J.K.Z.).
* Corresponding author; e-mail emhrabak{at}cisunix.unh.edu; fax 603–862–3784.
Received July 31, 2002;
returned for revision October 2, 2002;
accepted February 17, 2003.
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|
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|
|
|
|
|
|
|
F. Alferez, G. Y. Zhong, and J. K. Burns
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|
|
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|
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|
|
|
|
|
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|
|
|
|
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|
|
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|
|
|
|
|
|
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|
|
|
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|
|
|
|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
|
H.-i. Choi, H.-J. Park, J. H. Park, S. Kim, M.-Y. Im, H.-H. Seo, Y.-W. Kim, I. Hwang, and S. Y. Kim
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139(4):
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|
|
|
|
|
|
|
M. Glinski and W. Weckwerth
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October 1, 2005;
4(10):
1614 - 1625.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. A. Hemsley, A. C. Kemp, and C. S. Grierson
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17(9):
2554 - 2563.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. H. Ok, H. J. Jeong, J. M. Bae, J.-S. Shin, S. Luan, and K.-N. Kim
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Plant Physiology,
September 1, 2005;
139(1):
138 - 150.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Asano, N. Tanaka, G. Yang, N. Hayashi, and S. Komatsu
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February 1, 2005;
46(2):
356 - 366.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Umezawa, R. Yoshida, K. Maruyama, K. Yamaguchi-Shinozaki, and K. Shinozaki
SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana
PNAS,
December 7, 2004;
101(49):
17306 - 17311.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Boudsocq, H. Barbier-Brygoo, and C. Lauriere
Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana
J. Biol. Chem.,
October 1, 2004;
279(40):
41758 - 41766.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Nagata, S. Iizumi, K. Satoh, H. Ooka, J. Kawai, P. Carninci, Y. Hayashizaki, Y. Otomo, K. Murakami, K. Matsubara, et al.
Comparative Analysis of Plant and Animal Calcium Signal Transduction Element Using Plant Full-Length cDNA Data
Mol. Biol. Evol.,
October 1, 2004;
21(10):
1855 - 1870.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Kelner, I. Pekala, S. Kaczanowski, G. Muszynska, D. G. Hardie, and G. Dobrowolska
Biochemical Characterization of the Tobacco 42-kD Protein Kinase Activated by Osmotic Stress
Plant Physiology,
October 1, 2004;
136(2):
3255 - 3265.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. W. Chehab, O. R. Patharkar, A. D. Hegeman, T. Taybi, and J. C. Cushman
Autophosphorylation and Subcellular Localization Dynamics of a Salt- and Water Deficit-Induced Calcium-Dependent Protein Kinase from Ice Plant
Plant Physiology,
July 1, 2004;
135(3):
1430 - 1446.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kobayashi, S. Yamamoto, H. Minami, Y. Kagaya, and T. Hattori
Differential Activation of the Rice Sucrose Nonfermenting1-Related Protein Kinase2 Family by Hyperosmotic Stress and Abscisic Acid
PLANT CELL,
May 1, 2004;
16(5):
1163 - 1177.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Gong, Y. Guo, K. S. Schumaker, and J.-K. Zhu
The SOS3 Family of Calcium Sensors and SOS2 Family of Protein Kinases in Arabidopsis
Plant Physiology,
March 1, 2004;
134(3):
919 - 926.
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Levy, C. Bres, R. Geurts, B. Chalhoub, O. Kulikova, G. Duc, E.-P. Journet, J.-M. Ane, E. Lauber, T. Bisseling, et al.
A Putative Ca2+ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses
Science,
February 27, 2004;
303(5662):
1361 - 1364.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N.-H. Cheng, J. K. Pittman, J.-K. Zhu, and K. D. Hirschi
The Protein Kinase SOS2 Activates the Arabidopsis H+/Ca2+ Antiporter CAX1 to Integrate Calcium Transport and Salt Tolerance
J. Biol. Chem.,
January 23, 2004;
279(4):
2922 - 2926.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
U. Kolukisaoglu, S. Weinl, D. Blazevic, O. Batistic, and J. Kudla
Calcium Sensors and Their Interacting Protein Kinases: Genomics of the Arabidopsis and Rice CBL-CIPK Signaling Networks
Plant Physiology,
January 1, 2004;
134(1):
43 - 58.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Boisson, C. Giglione, and T. Meinnel
Unexpected Protein Families Including Cell Defense Components Feature in the N-Myristoylome of a Higher Eukaryote
J. Biol. Chem.,
October 31, 2003;
278(44):
43418 - 43429.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Dammann, A. Ichida, B. Hong, S. M. Romanowsky, E. M. Hrabak, A. C. Harmon, B. G. Pickard, and J. F. Harper
Subcellular Targeting of Nine Calcium-Dependent Protein Kinase Isoforms from Arabidopsis
Plant Physiology,
August 1, 2003;
132(4):
1840 - 1848.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
