Home LiteratureArticle Details
PMID: 10810151 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response.

The Plant cell ·Vol. 12 ·No. 5 ·2000-05-00 ·Pages 803-16

Romeis T, Piedras P, Jones JD

Abstract

In the Cf-9/Avr9 gene-for-gene interaction, the Cf-9 resistance gene from tomato confers resistance to the fungal pathogen Cladosporium fulvum, which expresses the corresponding pathogen-derived avirulence product Avr9. To understand R gene function and dissect the signaling mechanisms involved in the induction of plant defenses, we studied Cf-9/Avr9-dependent activation of protein kinases in transgenic Cf9 tobacco cell cultures. Using a modified in-gel kinase assay with histone as substrate, we identified a membrane-bound, calcium-dependent protein kinase (CDPK) that showed a shift in electrophoretic mobility from 68 to 70 kD within 5 min after Avr9 elicitor was added. This transition from the nonelicited to the elicited CDPK form was caused by a phosphorylation event and was verified when antibodies to CDPK were used for protein gel blot analysis. In addition, the interconversion of the corresponding CDPK forms could be induced in vitro in both directions by treatment with either phosphatase or ATP. In vitro protein kinase activity toward syntide-2 or histone with membrane extracts or gel-purified enzyme was dependent on Ca(2)+ content and was compromised by the calmodulin antagonist N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide (W-7) but not by its inactive isoform N-(6-aminohexyl)-1-naphthalenesulfonamide. In these assays, the CDPK activity in elicited samples, reflecting predominantly the phosphorylated 70-kD CDPK form, was greater than in nonelicited samples. Thus, Avr9/Cf-9-dependent phosphorylation and subsequent transition from the nonelicited to the elicited form correlate with the activation of a CDPK isoform after in vivo stimulation. Because that transition was not inhibited by W-7, the in vivo CDPK activation probably is not the result of autophosphorylation. Studies with pharmacological inhibitors indicated that the identified CDPK is independent of or is located upstream from a signaling pathway that is required for the Avr9-induced active oxygen species.

MeSH Terms
Enzyme Activation Fungal Proteins/genetics Membrane Glycoproteins/genetics Plant Proteins/genetics Plants/enzymology,genetics Plants, Genetically Modified Protein Kinases/metabolism
Chemicals
Fungal Proteins Membrane Glycoproteins Plant Proteins AVR9 protein, Cladosporium fulvum Protein Kinases calcium-dependent protein kinase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Romeis T
Sainsbury Laboratory, John Innes Centre, Norwich NR4 7UH, Norfolk, United Kingdom. tina.romeis@bbsrc.ac.uk
Piedras P
Jones J D
References (62)
62 references, click to expand
  1. Plant metabolism: enzyme regulation by 14-3-3 proteins.
    Curr Biol. 1996 Nov 1;6(11):1403-5 PMID: 8939587
  2. Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein.
    Plant Mol Biol. 1999 Mar;39(5):991-1001 PMID: 10344204
  3. Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7433-8 PMID: 9636167
  4. Binding of 14-3-3 protein to the plasma membrane H(+)-ATPase AHA2 involves the three C-terminal residues Tyr(946)-Thr-Val and requires phosphorylation of Thr(947).
    J Biol Chem. 1999 Dec 17;274(51):36774-80 PMID: 10593986
  5. The Activation of the Potato PR-10a Gene Requires the Phosphorylation of the Nuclear Factor PBF-1.
    Plant Cell. 1995 May;7(5):589-598 PMID: 12242377
  6. A calcium-dependent but calmodulin-independent protein kinase from soybean.
    Plant Physiol. 1987 Apr;83(4):830-7 PMID: 16665348
  7. Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses.
    EMBO J. 1997 Feb 17;16(4):726-38 PMID: 9049302
  8. Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells.
    Plant Cell. 1997 Feb;9(2):249-59 PMID: 9061955
  9. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel.
    Plant Physiol. 1998 Feb;116(2):785-95 PMID: 9489023
  10. PLANT DISEASE RESISTANCE GENES.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:575-607 PMID: 15012275
  11. Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses.
    Plant Cell. 1999 Feb;11(2):273-87 PMID: 9927644
  12. Characterization and partial purification of an oligopeptide elicitor receptor from parsley (Petroselinum crispum).
    FEBS Lett. 1998 Jul 24;431(3):405-10 PMID: 9714552
  13. Two genes that encode Ca(2+)-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana.
    Mol Gen Genet. 1994 Aug 15;244(4):331-40 PMID: 8078458
  14. Early signalling events implicated in leukotriene B4-induced activation of the NADPH oxidase in eosinophils: role of Ca2+, protein kinase C and phospholipases C and D.
    Biochem J. 1995 Sep 15;310 ( Pt 3):795-806 PMID: 7575412
  15. Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat.
    Biochemistry. 1992 Feb 18;31(6):1721-7 PMID: 1737026
  16. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9
    Plant Cell. 1998 Aug;10(8):1251-66 PMID: 9707527
  17. An increase in cytosolic calcium ion concentration precedes hypoosmotic shock-induced activation of protein kinases in tobacco suspension culture cells.
    FEBS Lett. 1997 Jan 20;401(2-3):202-6 PMID: 9013887
  18. Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8145-50 PMID: 8755618
  19. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis.
    Plant J. 1992 May;2(3):359-66 PMID: 1303800
  20. Cloning, expression and N-terminal myristoylation of CpCPK1, a calcium-dependent protein kinase from zucchini (Cucurbita pepo L.).
    Plant Mol Biol. 1999 Jan;39(2):199-208 PMID: 10080688
  21. Activation of Plant Plasma Membrane Ca2+-Permeable Channels by Race-Specific Fungal Elicitors.
    Plant Physiol. 1997 Jan;113(1):269-279 PMID: 12223606
  22. Molecular genetics of plant disease resistance.
    Science. 1995 May 5;268(5211):661-7 PMID: 7732374
  23. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles.
    Plant Cell. 2000 Jun;12(6):963-77 PMID: 10852940
  24. Unusual membrane-associated protein kinases in higher plants.
    J Membr Biol. 1998 Aug 1;164(3):205-13 PMID: 9691114
  25. Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean.
    Biochemistry. 1998 May 12;37(19):6801-9 PMID: 9578565
  26. Activation of a Ca(2+)-dependent protein kinase involves intramolecular binding of a calmodulin-like regulatory domain.
    Biochemistry. 1996 Oct 8;35(40):13222-30 PMID: 8855961
  27. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging.
    Science. 1994 Nov 4;266(5186):789-93 PMID: 7973631
  28. Measurement of Ca2+ fluxes during elicitation of the oxidative burst in aequorin-transformed tobacco cells.
    J Biol Chem. 1997 Nov 7;272(45):28274-80 PMID: 9353281
  29. Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants.
    Plant Cell. 1999 Feb;11(2):263-72 PMID: 9927643
  30. Fusicoccin, 14-3-3 proteins, and defense responses in tomato plants.
    Plant Physiol. 1999 Apr;119(4):1243-50 PMID: 10198082
  31. Characterization of a calcium-dependent protein kinase of tobacco leaves that is associated with the plasma membrane and is inducible by sucrose.
    Plant Cell Physiol. 1998 Nov;39(11):1176-83 PMID: 9891416
  32. Receptor-mediated activation of a MAP kinase in pathogen defense of plants.
    Science. 1997 Jun 27;276(5321):2054-7 PMID: 9197271
  33. Map-based cloning of a protein kinase gene conferring disease resistance in tomato.
    Science. 1993 Nov 26;262(5138):1432-6 PMID: 7902614
  34. Resistance response physiology and signal transduction.
    Curr Opin Plant Biol. 1998 Aug;1(4):305-10 PMID: 10066609
  35. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275 PMID: 15012264
  36. A functional homolog of mammalian protein kinase C participates in the elicitor-induced defense response in potato.
    Plant Cell. 1997 Apr;9(4):653-64 PMID: 9144967
  37. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs.
    Plant Cell. 1998 Feb;10(2):255-66 PMID: 9490748
  38. The structure and function of a soybean beta-glucan-elicitor-binding protein.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1029-34 PMID: 9023377
  39. Characterization of eight new members of the calmodulin-like domain protein kinase gene family from Arabidopsis thaliana.
    Plant Mol Biol. 1996 May;31(2):405-12 PMID: 8756605
  40. Ca2+-dependent protein kinases and stress signal transduction in plants.
    Science. 1996 Dec 13;274(5294):1900-2 PMID: 8943201
  41. Fungal elicitors induce a transient release of active oxygen species from cultured spruce cells that is dependent on Ca(2+) and protein-kinase activity.
    Planta. 1992 Apr;187(1):136-41 PMID: 24177978
  42. The 14-3-3 proteins: cellular regulators of plant metabolism.
    Trends Plant Sci. 1999 Sep;4(9):367-371 PMID: 10462770
  43. Functional analysis of plant disease resistance genes and their downstream effectors.
    Curr Opin Plant Biol. 1999 Aug;2(4):273-9 PMID: 10458999
  44. The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium.
    Planta. 1997 Dec;203(4):442-7 PMID: 9421928
  45. Role of active oxygen species and NO in plant defence responses.
    Curr Opin Plant Biol. 1999 Aug;2(4):287-94 PMID: 10459001
  46. Expression of three members of the calcium-dependent protein kinase gene family in Arabidopsis thaliana.
    Plant Mol Biol. 1996 Mar;30(6):1259-75 PMID: 8704134
  47. PEST sequences and regulation by proteolysis.
    Trends Biochem Sci. 1996 Jul;21(7):267-71 PMID: 8755249
  48. Protein kinase C isotypes and signal-transduction in human neutrophils: selective substrate specificity of calcium-dependent beta-PKC and novel calcium-independent nPKC.
    Biochim Biophys Acta. 1993 Apr 16;1176(3):276-86 PMID: 8471629
  49. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21.
    Science. 1995 Dec 15;270(5243):1804-6 PMID: 8525370
  50. Signal perception and transduction in plant defense responses.
    Genes Dev. 1997 Jul 1;11(13):1621-39 PMID: 9224713
  51. Intramolecular binding contributes to the activation of CDPK, a protein kinase with a calmodulin-like domain.
    Biochemistry. 1996 Sep 17;35(37):12029-37 PMID: 8810907
  52. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses.
    Cell. 1994 Aug 12;78(3):449-60 PMID: 8062387
  53. Regulation of Plant Defense Response to Fungal Pathogens: Two Types of Protein Kinases in the Reversible Phosphorylation of the Host Plasma Membrane H+-ATPase.
    Plant Cell. 1996 Mar;8(3):555-564 PMID: 12239392
  54. 14-3-3 proteins activate a plant calcium-dependent protein kinase (CDPK).
    FEBS Lett. 1998 Jul 3;430(3):381-4 PMID: 9688575
  55. A novel chloride channel in Vicia faba guard cell vacuoles activated by the serine/threonine kinase, CDPK.
    EMBO J. 1996 Dec 2;15(23):6564-74 PMID: 8978683
  56. Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2751-5 PMID: 11038609
  57. Dead cells do tell tales.
    Curr Opin Plant Biol. 1998 Dec;1(6):480-5 PMID: 10066637
  58. K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction.
    Plant J. 1999 Aug;19(4):453-62 PMID: 10504567
  59. Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp.
    Plant Cell. 1998 Mar;10(3):435-50 PMID: 9501116
  60. Isolation of a French bean (Phaseolus vulgaris L.) homolog to the beta-glucan elicitor-binding protein of soybean (Glycine max L.).
    Biochim Biophys Acta. 1999 Apr 14;1418(1):127-32 PMID: 10209217
  61. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox).
    Plant J. 1998 May;14(3):365-70 PMID: 9628030
  62. Structure and function of proteins controlling strain-specific pathogen resistance in plants.
    Curr Opin Plant Biol. 1998 Aug;1(4):288-93 PMID: 10066601
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2000-05-00
Pages
803-16
Language
English
Region
England
NLM ID
9208688
PMCID
PMC139928
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com