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PMID: 9489023 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel.

Plant physiology ·Vol. 116 ·No. 2 ·1998-02-00 ·Pages 785-95

Li J, Lee YR, Assmann SM

Abstract

Increasing evidence suggests that changes in cytosolic Ca2+ levels and phosphorylation play important roles in the regulation of stomatal aperture and as ion transporters of guard cells. However, protein kinases responsible for Ca2+ signaling in guard cells remain to be identified. Using biochemical approaches, we have identified a Ca(2+)-dependent protein kinase with a calmodulin-like domain (CDPK) in guard cell protoplasts of Vicia faba. Both autophosphorylation and catalytic activity of CDPK are Ca2+ dependent. CDPK exhibits a Ca(2+)-induced electrophoretic mobility shift and its Ca(2+)-dependent catalytic activity can be inhibited by the calmodulin antagonists trifluoperazine and N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide. Antibodies to soybean CDPK alpha cross-react with CDPK. Micromolar Ca2+ concentrations stimulate phosphorylation of several proteins from guard cells; cyclosporin A, a specific inhibitor of the Ca(2+)-dependent protein phosphatase calcineurin enhances the Ca(2+)-dependent phosphorylation of several soluble proteins. CDPK from guard cells phosphorylates the K+ channel KAT1 protein in a Ca(2+)-dependent manner. These results suggest that CDPK may be an important component of Ca2+ signaling in guard cells.

MeSH Terms
Calcium/metabolism Catalysis Phosphorylation Plant Cells Plant Proteins/metabolism Plants/enzymology,metabolism Potassium Channels/metabolism Potassium Channels, Inwardly Rectifying Protein Kinases/metabolism
Chemicals
Plant Proteins Potassium Channels Potassium Channels, Inwardly Rectifying Protein Kinases calcium-dependent protein kinase Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Li J
Department of Biology, Pennsylvania State University, University Park 16802, USA.
Lee Y R
Assmann S M
References (50)
50 references, click to expand
  1. Regulation of voltage dependence of the KAT1 channel by intracellular factors.
    J Gen Physiol. 1995 Mar;105(3):309-28 PMID: 7769379
  2. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA.
    Science. 1992 Dec 4;258(5088):1654-8 PMID: 8966547
  3. Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9535-9 PMID: 11607582
  4. Membrane insertion and assembly of ductin: a polytopic channel with dual orientations.
    EMBO J. 1995 Aug 1;14(15):3609-16 PMID: 7641680
  5. Inhibition of T cell signaling by immunophilin-ligand complexes correlates with loss of calcineurin phosphatase activity.
    Biochemistry. 1992 Apr 28;31(16):3896-901 PMID: 1373650
  6. Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase.
    Plant Cell. 1996 Mar;8(3):505-17 PMID: 8721752
  7. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  8. Calcium-Activated K+ Channels and Calcium-Induced Calcium Release by Slow Vacuolar Ion Channels in Guard Cell Vacuoles Implicated in the Control of Stomatal Closure.
    Plant Cell. 1994 May;6(5):669-683 PMID: 12244253
  9. Role of calcium in the modulation of Vicia guard cell potassium channels by abscisic acid: a patch-clamp study.
    J Membr Biol. 1994 Jan;137(2):99-107 PMID: 8006956
  10. A calcium-dependent but calmodulin-independent protein kinase from soybean.
    Plant Physiol. 1987 Apr;83(4):830-7 PMID: 16665348
  11. Cell-free expression of functional Shaker potassium channels.
    Nature. 1992 Nov 12;360(6400):166-9 PMID: 1436093
  12. Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase.
    Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8837-41 PMID: 8090732
  13. Calcium Effects on Stomatal Movement in Commelina communis L. : Use of EGTA to Modulate Stomatal Response to Light, KCl and CO(2).
    Plant Physiol. 1988 Jul;87(3):583-7 PMID: 16666189
  14. Phosphorylation of Raf by ceramide-activated protein kinase.
    Nature. 1995 Nov 16;378(6554):307-10 PMID: 7477354
  15. Signalling in guard cells and regulation of ion channel activity.
    J Exp Bot. 1997 Mar;48 Spec No:515-28 PMID: 21245228
  16. Cellular distribution of calmodulin and calmodulin-binding proteins in Vicia faba L.
    Plant Physiol. 1992;100:970-8 PMID: 11537871
  17. The clathrin coat assembly polypeptide complex. Autophosphorylation and assembly activities.
    J Biol Chem. 1987 Mar 15;262(8):3864-71 PMID: 2880851
  18. Expression of an Arabidopsis potassium channel gene in guard cells.
    Plant Physiol. 1995 Oct;109(2):371-4 PMID: 7480337
  19. Autophosphorylation: a salient feature of protein kinases.
    Mol Cell Biochem. 1993 Nov;127-128:51-70 PMID: 7935362
  20. Resolution and identification of C4 phosphoenolpyruvate-carboxylase protein-kinase polypeptides and their reversible light activation in maize leaves.
    Arch Biochem Biophys. 1993 Dec;307(2):416-9 PMID: 8274031
  21. Central Roles for Potassium and Sucrose in Guard-Cell Osmoregulation.
    Plant Physiol. 1996 Aug;111(4):1051-1057 PMID: 12226347
  22. Methods for increasing the resolution of two-dimensional protein electrophoresis.
    Anal Biochem. 1988 Sep;173(2):424-35 PMID: 3189820
  23. Cytosolic Concentration of Ca2+ Regulates the Plasma Membrane H+-ATPase in Guard Cells of Fava Bean.
    Plant Cell. 1995 Aug;7(8):1333-1342 PMID: 12242406
  24. Characterization of an Arabidopsis calmodulin-like domain protein kinase purified from Escherichia coli using an affinity sandwich technique.
    Biochemistry. 1994 Mar 1;33(8):2033-41 PMID: 8117660
  25. Sensitivity to abscisic acid of guard-cell K+ channels is suppressed by abi1-1, a mutant Arabidopsis gene encoding a putative protein phosphatase.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9520-4 PMID: 7568166
  26. An Abscisic Acid-Activated and Calcium-Independent Protein Kinase from Guard Cells of Fava Bean.
    Plant Cell. 1996 Dec;8(12):2359-2368 PMID: 12239380
  27. Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate.
    Nature. 1990 Aug 23;346(6286):766-9 PMID: 2388696
  28. Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake.
    Annu Rev Biophys Biomol Struct. 1994;23:441-71 PMID: 7919789
  29. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  30. Role of Ca and EGTA on Stomatal Movements in Commelina communis L.
    Plant Physiol. 1985 Dec;79(4):1003-5 PMID: 16664518
  31. Involvement of Calmodulin and Calmodulin-Dependent Myosin Light Chain Kinase in Blue Light-Dependent H Pumping by Guard Cell Protoplasts from Vicia faba L.
    Plant Physiol. 1992 Aug;99(4):1416-21 PMID: 16669053
  32. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane.
    J Cell Biol. 1992 Jul;118(2):481-90 PMID: 1629242
  33. A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel.
    Anal Biochem. 1989 Nov 15;183(1):139-43 PMID: 2559625
  34. Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells.
    EMBO J. 1990 Dec;9(12):3889-92 PMID: 1701140
  35. Signal transduction in guard cells.
    Annu Rev Cell Biol. 1993;9:345-75 PMID: 8280465
  36. Molecular biology of the plasma membrane of higher plants.
    Plant Cell. 1989 Oct;1(10):953-60 PMID: 2562554
  37. A rice membrane calcium-dependent protein kinase is induced by gibberellin.
    Plant Physiol. 1995 Jun;108(2):787-93 PMID: 7610167
  38. A calcium-dependent protein kinase with a regulatory domain similar to calmodulin.
    Science. 1991 May 17;252(5008):951-4 PMID: 1852075
  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. The structure and insertion of integral proteins in membranes.
    Annu Rev Cell Biol. 1990;6:247-96 PMID: 2275815
  41. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  42. Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2202-6 PMID: 7681590
  43. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):3736-40 PMID: 1570292
  44. Phosphorylation by protein kinase A of RCK1 K+ channels expressed in Xenopus oocytes.
    Biochemistry. 1994 Jul 26;33(29):8786-92 PMID: 8038169
  45. Calcium: a program in BASIC for calculating the composition of solutions with specified free concentrations of calcium, magnesium and other divalent cations.
    Comput Biol Med. 1988;18(5):351-66 PMID: 3143515
  46. 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
  47. Functional expression of the plant K+ channel KAT1 in insect cells.
    FEBS Lett. 1996 Feb 19;380(3):229-32 PMID: 8601430
  48. Role of Calcium in Signal Transduction of Commelina Guard Cells.
    Plant Cell. 1991 Apr;3(4):333-344 PMID: 12324599
  49. Ribonuclease S-peptide as a carrier in fusion proteins.
    Protein Sci. 1993 Mar;2(3):348-56 PMID: 8453373
  50. Use of Saccharomyces cerevisiae for patch-clamp analysis of heterologous membrane proteins: characterization of Kat1, an inward-rectifying K+ channel from Arabidopsis thaliana, and comparison with endogeneous yeast channels and carriers.
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2701-5 PMID: 7708709
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
1998-02-00
Pages
785-95
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC35138
Subset
IM
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