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PMID: 12237354 Published · ppublish English Journal Article

Early Events Induced by the Elicitor Cryptogein in Tobacco Cells: Involvement of a Plasma Membrane NADPH Oxidase and Activation of Glycolysis and the Pentose Phosphate Pathway.

The Plant cell ·Vol. 9 ·No. 11 ·1997-11-00 ·Pages 2077-2091

Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, Douce R, Guern J

Abstract

Application of the elicitor cryptogein to tobacco (cv Xanthi) is known to evoke external medium alkalinization, active oxygen species production, and phytoalexin synthesis. These are all dependent on an influx of calcium. We show here that cryptogein also induces calcium-dependent plasma membrane depolarization, chloride efflux, cytoplasm acidification, and NADPH oxidation without changes in NAD+ and ATP levels, indicating that the elicitor-activated redox system, responsible for active oxygen species production, uses NADPH in vivo. NADPH oxidation activates the functioning of the pentose phosphate pathway, leading to a decrease in glucose 6-phosphate and to the accumulation of glyceraldehyde 3-phosphate, 3- and 2-phosphoglyceric acid, and phosphoenolpyruvate. By inhibiting the pentose phosphate pathway, we demonstrate that the activation of the plasma membrane NADPH oxidase is responsible for active oxygen species production, external alkalinization, and acidification of the cytoplasm. A model is proposed for the organization of the cryptogein responses measured to date.

Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Pugin A.
Unite Associee, Institut National de la Recherche Agronomique/Universite de Bourgogne, INRA BV 1540, 21034 Dijon Cedex, France.
Frachisse J. M.
Tavernier E.
Bligny R.
Gout E.
Douce R.
Guern J.
References (52)
52 references, click to expand
  1. Rapid Stimulation of an Oxidative Burst during Elicitation of Cultured Plant Cells : Role in Defense and Signal Transduction.
    Plant Physiol. 1989 May;90(1):109-16 PMID: 16666719
  2. High affinity binding of a glycopeptide elicitor to tomato cells and microsomal membranes and displacement by specific glycan suppressors.
    J Biol Chem. 1993 Jul 15;268(20):14724-31 PMID: 8325850
  3. Induction of protein phosphorylation, protein synthesis, immediate-early-gene expression and cellular proliferation by intracellular pH modulation. Implications for the role of hydrogen ions in signal transduction.
    Eur J Biochem. 1993 Apr 1;213(1):349-57 PMID: 8477706
  4. Involvement of Free Calcium in Action of Cryptogein, a Proteinaceous Elicitor of Hypersensitive Reaction in Tobacco Cells.
    Plant Physiol. 1995 Nov;109(3):1025-1031 PMID: 12228650
  5. Elicitors and suppressors of the defense response in tomato cells. Purification and characterization of glycopeptide elicitors and glycan suppressors generated by enzymatic cleavage of yeast invertase.
    J Biol Chem. 1992 May 25;267(15):10258-65 PMID: 1587815
  6. Are Redox Reactions Involved in Regulation of K+ Channels in the Plasma Membrane of Limnobium stoloniferum Root Hairs?
    Plant Physiol. 1994 Jul;105(3):927-935 PMID: 12232255
  7. Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure.
    Nature. 1990 Aug 23;346(6286):769-71 PMID: 2388697
  8. Regulation of intracellular pH values in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies.
    J Biol Chem. 1992 Jul 15;267(20):13903-9 PMID: 1629190
  9. 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
  10. The O2- -forming NADPH oxidase of the phagocytes: nature, mechanisms of activation and function.
    Biochim Biophys Acta. 1986 Nov 4;853(1):65-89 PMID: 3021215
  11. Tobacco cells contain a protein, immunologically related to the neutrophil small G protein Rac2 and involved in elicitor-induced oxidative burst.
    FEBS Lett. 1997 Feb 17;403(2):149-53 PMID: 9042956
  12. Involvement of the oxidative burst in phytoalexin accumulation and the hypersensitive reaction.
    Plant Physiol. 1992 Nov;100(3):1189-95 PMID: 16653104
  13. Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell.
    EMBO J. 1994 Jul 1;13(13):2970-5 PMID: 8039493
  14. Methyl phosphonate as a 31P-NMR probe for intracellular pH measurements in Dictyostelium amoebae.
    Biochimie. 1989 Aug;71(8):941-8 PMID: 2508763
  15. Regulation of Vacuolar pH of Plant Cells: II. A P NMR Study of the Modifications of Vacuolar pH in Isolated Vacuoles Induced by Proton Pumping and Cation/H Exchanges.
    Plant Physiol. 1989 Jan;89(1):27-36 PMID: 16666525
  16. Anion channels as central mechanisms for signal transduction in guard cells and putative functions in roots for plant-soil interactions.
    Plant Mol Biol. 1995 Jun;28(3):353-61 PMID: 7543302
  17. Purification and properties of d-glucose-6-phosphate dehydrogenase.
    J Biol Chem. 1955 Sep;216(1):67-79 PMID: 13252007
  18. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response.
    Cell. 1992 Jul 10;70(1):21-30 PMID: 1623521
  19. Biochemical changes during sucrose deprivation in higher plant cells. Phosphorus-31 nuclear magnetic resonance studies.
    J Biol Chem. 1987 Apr 15;262(11):5000-7 PMID: 3031035
  20. The plant extracellular matrix: news from the cell's frontier.
    Plant Cell. 1996 Sep;8(9):1451-63 PMID: 8837501
  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. Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants.
    Plant Cell. 1995 Jul;7(7):833-844 PMID: 12242389
  23. Cloning of two plant cDNAs encoding a beta-type proteasome subunit and a transformer-2-like SR-related protein: early induction of the corresponding genes in tobacco cells treated with cryptogein.
    Plant Mol Biol. 1997 Oct;35(3):261-9 PMID: 9349250
  24. The respiratory burst oxidase.
    J Biol Chem. 1994 Oct 7;269(40):24519-22 PMID: 7929117
  25. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions.
    Cell. 1994 May 20;77(4):551-63 PMID: 8187175
  26. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.
    Science. 1993 Dec 17;262(5141):1883-6 PMID: 8266079
  27. Cooperation and Competition between Adenylate Kinase, Nucleoside Diphosphokinase, Electron Transport, and ATP Synthase in Plant Mitochondria Studied by 31P-Nuclear Magnetic Resonance.
    Plant Physiol. 1997 Jan;113(1):191-199 PMID: 12223600
  28. Protein Phosphorylation Is Induced in Tobacco Cells by the Elicitor Cryptogein.
    Plant Physiol. 1994 Apr;104(4):1245-1249 PMID: 12232163
  29. Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells.
    Trends Biochem Sci. 1989 May;14(5):187-92 PMID: 2475930
  30. The relationship between ATP and an electrogenic pump in the plasma membrane of Neurospora crassa.
    J Membr Biol. 1973;14(4):305-38 PMID: 4360924
  31. The biochemical basis of the NADPH oxidase of phagocytes.
    Trends Biochem Sci. 1993 Feb;18(2):43-7 PMID: 8488557
  32. Active Oxygen Species in Plant Defense against Pathogens.
    Plant Physiol. 1994 Jun;105(2):467-472 PMID: 12232215
  33. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
    Cell. 1994 Nov 18;79(4):583-93 PMID: 7954825
  34. Monitoring of cellular metabolism by NMR.
    Biochim Biophys Acta. 1981 Nov 9;639(1):53-76 PMID: 7030398
  35. The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH.
    Nature. 1981 Apr 2;290(5805):406-9 PMID: 7219526
  36. P NMR Study of Elicitor Treated Phaseolus vulgaris Cell Suspension Cultures.
    Plant Physiol. 1987 Nov;85(3):716-9 PMID: 16665766
  37. Plasmalemma redox activity and h extrusion: I. Activation of the h-pump by ferricyanide-induced potential depolarization and cytoplasm acidification.
    Plant Physiol. 1988 May;87(1):25-9 PMID: 16666112
  38. Plant and human neutrophil oxidative burst complexes contain immunologically related proteins.
    Biochim Biophys Acta. 1996 Mar 15;1289(2):231-7 PMID: 8600979
  39. Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco.
    Eur J Biochem. 1989 Aug 15;183(3):555-63 PMID: 2776750
  40. Specific inhibitors of vacuolar type H(+)-ATPases induce apoptotic cell death.
    Biochem Biophys Res Commun. 1995 Jul 6;212(1):255-62 PMID: 7612014
  41. Function of Oxidative Cross-Linking of Cell Wall Structural Proteins in Plant Disease Resistance.
    Plant Cell. 1994 Dec;6(12):1703-1712 PMID: 12244231
  42. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase.
    Biochem J. 1986 Jul 1;237(1):111-6 PMID: 3800872
  43. The respiratory burst oxidase.
    Adv Enzymol Relat Areas Mol Biol. 1992;65:49-95 PMID: 1570769
  44. Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells.
    Plant Physiol. 1995 Apr;107(4):1241-1247 PMID: 12228430
  45. pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate.
    Proc Natl Acad Sci U S A. 1981 Oct;78(10 ):6271-5 PMID: 7031646
  46. 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
  47. Relationship of Transplasmalemma Redox Activity to Proton and Solute Transport by Roots of Zea mays.
    Plant Physiol. 1986 Apr;80(4):805-11 PMID: 16664722
  48. Stress responses in alfalfa (Medicago sativa L.) XIX. Transcriptional activation of oxidative pentose phosphate pathway genes at the onset of the isoflavonoid phytoalexin response.
    Plant Mol Biol. 1995 Aug;28(5):885-900 PMID: 7640360
  49. 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
  50. Function of the oxidative burst in hypersensitive disease resistance.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4158-63 PMID: 11607542
  51. Responses of Cultured Tobacco Cells to Cryptogein, a Proteinaceous Elicitor from Phytophthora cryptogea: Possible Plasmalemma Involvement.
    Plant Physiol. 1991 Feb;95(2):486-91 PMID: 16668010
  52. Oxidative stress and apoptosis in HIV infection: a role for plant-derived metabolites with synergistic antioxidant activity.
    Immunol Today. 1994 May;15(5):209-13 PMID: 8024680
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
1997-11-00
Pages
2077-2091
Language
English
Region
England
NLM ID
9208688
PMCID
PMC157059
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