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PMID: 14730064 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks.

Plant physiology ·Vol. 134 ·No. 1 ·2004-01-00 ·Pages 43-58

Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J

Abstract

Calcium signals mediate a multitude of plant responses to external stimuli and regulate a wide range of physiological processes. Calcium-binding proteins, like calcineurin B-like (CBL) proteins, represent important relays in plant calcium signaling. These proteins form a complex network with their target kinases being the CBL-interacting protein kinases (CIPKs). Here, we present a comparative genomics analysis of the full complement of CBLs and CIPKs in Arabidopsis and rice (Oryza sativa). We confirm the expression and transcript composition of the 10 CBLs and 25 CIPKs encoded in the Arabidopsis genome. Our identification of 10 CBLs and 30 CIPKs from rice indicates a similar complexity of this signaling network in both species. An analysis of the genomic evolution suggests that the extant number of gene family members largely results from segmental duplications. A phylogenetic comparison of protein sequences and intron positions indicates an early diversification of separate branches within both gene families. These branches may represent proteins with different functions. Protein interaction analyses and expression studies of closely related family members suggest that even recently duplicated representatives may fulfill different functions. This work provides a basis for a defined further functional dissection of this important plant-specific signaling system.

MeSH Terms
Amino Acid Sequence Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Calcium Signaling Calcium-Binding Proteins/genetics,metabolism Chromosome Mapping Chromosomes, Plant/genetics Evolution, Molecular Exons Genes, Plant Genomics Introns Molecular Sequence Data Multigene Family Oryza/genetics,metabolism Phylogeny Protein Kinases/genetics,metabolism Sequence Homology, Amino Acid Signal Transduction Species Specificity
Chemicals
Arabidopsis Proteins CBL protein, Arabidopsis Calcium-Binding Proteins Protein Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kolukisaoglu Uner
Abteilung Pflanzenphysiologie, Universität Rostock, Albert-Einstein-Strasse 3, 18051 Rostock, Germany.
Weinl Stefan
Blazevic Dragica
Batistic Oliver
Kudla Jörg
References (54)
54 references, click to expand
  1. Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases.
    Plant Physiol. 2000 Dec;124(4):1844-53 PMID: 11115898
  2. The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis.
    Plant Physiol. 2003 Mar;131(3):1169-77 PMID: 12644668
  3. Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis.
    Plant Cell. 1999 Dec;11(12):2393-405 PMID: 10590166
  4. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3730-4 PMID: 10725382
  5. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3735-40 PMID: 10725350
  6. CDPKs - a kinase for every Ca2+ signal?
    Trends Plant Sci. 2000 Apr;5(4):154-9 PMID: 10740296
  7. Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4168-73 PMID: 10759555
  8. Diverse response of rice and maize genes encoding homologs of WPK4, an SNF1-related protein kinase from wheat, to light, nutrients, low temperature and cytokinins.
    Mol Gen Genet. 2000 Mar;263(2):359-66 PMID: 10778756
  9. Extensive duplication and reshuffling in the Arabidopsis genome.
    Plant Cell. 2000 Jul;12(7):1093-101 PMID: 10899976
  10. SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding.
    Plant Cell. 2000 Sep;12(9):1667-78 PMID: 11006339
  11. EF-hand calcium-binding proteins.
    Curr Opin Struct Biol. 2000 Dec;10(6):637-43 PMID: 11114499
  12. Two novel genes encoding SNF-1 related protein kinases from Arabidopsis thaliana: differential accumulation of AtSR1 and AtSR2 transcripts in response to cytokinins and sugars, and phosphorylation of sucrose synthase by AtSR2.
    Mol Gen Genet. 2001 Jan;264(5):674-81 PMID: 11212922
  13. The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases.
    EMBO J. 2001 Mar 1;20(5):1051-63 PMID: 11230129
  14. Signal processing and transduction in plant cells: the end of the beginning?
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):307-14 PMID: 11283728
  15. Abiotic stress signalling pathways: specificity and cross-talk.
    Trends Plant Sci. 2001 Jun;6(6):262-7 PMID: 11378468
  16. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance.
    Plant Cell. 2001 Jun;13(6):1383-400 PMID: 11402167
  17. Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana.
    EMBO J. 2001 Sep 3;20(17):4730-41 PMID: 11532937
  18. Dissecting calcium oscillators in plant cells.
    Trends Plant Sci. 2001 Sep;6(9):395-7 PMID: 11544110
  19. Combining genetics and cell biology to crack the code of plant cell calcium signaling.
    Sci STKE. 2001 Oct 2;2001(102):re13 PMID: 11584126
  20. Calcium oscillations in higher plants.
    Curr Opin Plant Biol. 2001 Oct;4(5):415-20 PMID: 11597499
  21. Calcium-dependent protein kinases play an essential role in a plant defence response.
    EMBO J. 2001 Oct 15;20(20):5556-67 PMID: 11597999
  22. Instead of binding calcium, one of the EF-hand structures in guanylyl cyclase activating protein-2 is required for targeting photoreceptor guanylyl cyclase.
    J Biol Chem. 2001 Dec 21;276(51):48143-8 PMID: 11584009
  23. The PROSITE database, its status in 2002.
    Nucleic Acids Res. 2002 Jan 1;30(1):235-8 PMID: 11752303
  24. Calcium-binding proteins: intracellular sensors from the calmodulin superfamily.
    Biochem Biophys Res Commun. 2002 Jan 18;290(2):615-23 PMID: 11785943
  25. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).
    Science. 2002 Apr 5;296(5565):79-92 PMID: 11935017
  26. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
    Science. 2002 Apr 5;296(5565):92-100 PMID: 11935018
  27. Expression, activation, and biochemical properties of a novel Arabidopsis protein kinase.
    Plant Physiol. 2002 May;129(1):225-34 PMID: 12011353
  28. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants.
    Plant Cell. 2002;14 Suppl:S389-400 PMID: 12045290
  29. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events.
    Nature. 2003 Mar 27;422(6930):433-8 PMID: 12660784
  30. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis.
    Plant Cell. 2003 Apr;15(4):809-34 PMID: 12671079
  31. Annotation of the Arabidopsis genome.
    Plant Physiol. 2003 Jun;132(2):461-8 PMID: 12805579
  32. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice.
    Plant Physiol. 2003 Jun;132(2):618-28 PMID: 12805592
  33. The Arabidopsis CDPK-SnRK superfamily of protein kinases.
    Plant Physiol. 2003 Jun;132(2):666-80 PMID: 12805596
  34. CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis.
    Plant Cell. 2003 Aug;15(8):1833-45 PMID: 12897256
  35. The calcium sensor CBL1 integrates plant responses to abiotic stresses.
    Plant J. 2003 Nov;36(4):457-70 PMID: 14617077
  36. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  37. Reversible palmitoylation of the protein-tyrosine kinase p56lck.
    J Biol Chem. 1993 Apr 25;268(12):8669-74 PMID: 8473310
  38. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  39. Cloning and sequencing of a novel serine/threonine protein kinase in Arabidopsis thaliana.
    Plant Physiol. 1994 Nov;106(3):1229-30 PMID: 7824653
  40. Palmitoylation of either Cys-3 or Cys-5 is required for the biological activity of the Lck tyrosine protein kinase.
    Mol Cell Biol. 1995 Dec;15(12):6914-22 PMID: 8524258
  41. Ca2+-dependent protein kinases and stress signal transduction in plants.
    Science. 1996 Dec 13;274(5294):1900-2 PMID: 8943201
  42. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  43. Molecular mechanics of calcium-myristoyl switches.
    Nature. 1997 Sep 11;389(6647):198-202 PMID: 9296500
  44. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  45. A calcium sensor homolog required for plant salt tolerance.
    Science. 1998 Jun 19;280(5371):1943-5 PMID: 9632394
  46. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4718-23 PMID: 10200328
  47. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins.
    Biochim Biophys Acta. 1999 Aug 12;1451(1):1-16 PMID: 10446384
  48. Calcium at the crossroads of signaling.
    Plant Cell. 2002;14 Suppl:S401-17 PMID: 12045291
  49. Biochemical and functional characterization of PKS11, a novel Arabidopsis protein kinase.
    J Biol Chem. 2002 Aug 2;277(31):28340-50 PMID: 12029080
  50. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis.
    Dev Cell. 2002 Aug;3(2):233-44 PMID: 12194854
  51. Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance.
    Plant Physiol. 2002 Sep;130(1):256-64 PMID: 12226505
  52. Family business: the multidrug-resistance related protein (MRP) ABC transporter genes in Arabidopsis thaliana.
    Planta. 2002 Nov;216(1):107-19 PMID: 12430019
  53. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis.
    Plant Cell. 2003 Feb;15(2):411-23 PMID: 12566581
  54. The neuronal calcium sensor family of Ca2+-binding proteins.
    Biochem J. 2001 Jan 1;353(Pt 1):1-12 PMID: 11115393
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2004-01-00
Pages
43-58
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC316286
Subset
IM
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