Modulation of Plasma Membrane H+-ATPase Activity Differentially Activates Wound and Pathogen Defense Responses in Tomato Plants

Systemin is an important mediator of wound-induced defense gene activation in tomato plants, and it elicits a rapid alkalinization of the growth medium of cultured Lycopersicon peruvianum cells. A possible mechanistic link between proton fluxes across the plasma membrane and the induction of defense genes was investigated by modulating plasma membrane H+-ATPase activity. Inhibitors of H+-ATPase (erythrosin B, diethyl stilbestrol, and vanadate) were found to alkalinize the growth medium of L. peruvianum cell cultures and to induce wound response genes in whole tomato plants. Conversely, an activator of the H+-ATPase (fusicoccin) acidified the growth medium of L. peruvianum cell cultures and suppressed systemin-induced medium alkalinization. Likewise, in fusicoccin-treated tomato plants, the wound- and systemin-triggered accumulation of wound-responsive mRNAs was found to be suppressed. However, fusicoccin treatment of tomato plants led to the accumulation of salicylic acid and the expression of pathogenesis-related genes. Apparently, the wound and pathogen defense signaling pathways are differentially regulated by changes in the proton electrochemical gradient across the plasma membrane. In addition, alkalinization of the L. peruvianum cell culture medium was found to depend on the influx of Ca2+ and the activity of a protein kinase. Reversible protein phosphorylation was also shown to be involved in the induction of wound response genes. The plasma membrane H+-ATPase as a possible target of a Ca2+-activated protein kinase and its role in defense signaling are discussed.

[1]  T. Boller,et al.  The Plant Wound Hormone Systemin Binds with the N-Terminal Part to Its Receptor but Needs the C-Terminal Part to Activate It , 1998, Plant Cell.

[2]  L. E. González de la Vara,et al.  The plasma-membrane H+-ATPase from beet root is inhibited by a calcium-dependent phosphorylation , 1998, Planta.

[3]  A. Schaller Action of proteolysis-resistant systemin analogues in wound signalling. , 1998, Phytochemistry.

[4]  E. Titarenko,et al.  Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[5]  M. Palmgren,et al.  The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H(+)-ATPase. , 1997, The Plant cell.

[6]  E. Titarenko,et al.  Jasmonic Acid-Dependent and -Independent Signaling Pathways Control Wound-Induced Gene Activation in Arabidopsis thaliana , 1997, Plant physiology.

[7]  J. Stratmann,et al.  Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Piotrowski,et al.  Topology and target interaction of the fusicoccin‐binding 14‐3‐3 homologs of Commelina communis , 1997 .

[9]  Eric Davies,et al.  Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato , 1997, Planta.

[10]  Jörg Durner,et al.  Salicylic acid and disease resistance in plants , 1997 .

[11]  T. Jabs,et al.  Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Hedrich,et al.  Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[13]  H. Leyser,et al.  Ethylene as a Signal Mediating the Wound Response of Tomato Plants , 1996, Science.

[14]  G. Howe,et al.  Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  B. Stanković,et al.  Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato , 1996, FEBS letters.

[16]  P. Vera,et al.  Primary structure and expression of a pathogen-induced protease (PR-P69) in tomato plants: Similarity of functional domains to subtilisin-like endoproteases. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Malone,et al.  Rapid, Long-distance Signal Transmission in Higher Plants , 1996 .

[18]  E. Johannes,et al.  Systemin transiently depolarizes the tomato mesophyll cell membrane and antagonizes fusicoccin‐induced extracellular acidification of mesophyll tissue , 1996 .

[19]  E. Blumwald,et al.  Regulation of Plant Defense Response to Fungal Pathogens: Two Types of Protein Kinases in the Reversible Phosphorylation of the Host Plasma Membrane H+-ATPase. , 1996, The Plant cell.

[20]  C. Ryan,et al.  Systemin – a polypeptide defense signal in plants , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[21]  H. Sano,et al.  Tobacco MAP Kinase: A Possible Mediator in Wound Signal Transduction Pathways , 1995, Science.

[22]  C. Ryan,et al.  Induction of wound response genes in tomato leaves by bestatin, an inhibitor of aminopeptidases. , 1995, The Plant cell.

[23]  Y. Ito,et al.  Cutting activates a 46-kilodalton protein kinase in plants. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[24]  E. Weiler,et al.  Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid , 1995, Plant Physiology.

[25]  T. Kinoshita,et al.  Cytosolic Concentration of Ca2+ Regulates the Plasma Membrane H+-ATPase in Guard Cells of Fava Bean. , 1995, The Plant cell.

[26]  J. Fisahn,et al.  Proteinase Inhibitor II Gene Expression Induced by Electrical Stimulation and Control of Photosynthetic Activity in Tomato Plants , 1995 .

[27]  J. Ryals,et al.  Signal transduction in systemic acquired resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. Parniske,et al.  Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Boutry,et al.  The Plasma Membrane H+-ATPase (A Highly Regulated Enzyme with Multiple Physiological Functions) , 1995, Plant physiology.

[30]  T. Boller,et al.  Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells , 1995 .

[31]  J. Thain,et al.  Depolarization of tomato leaf cells by oligogalacturonide elicitors , 1995 .

[32]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[33]  T. Jabs,et al.  High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses , 1994, Cell.

[34]  E. Blumwald,et al.  Plant Defense Response to Fungal Pathogens (Activation of Host-Plasma Membrane H+-ATPase by Elicitor-Induced Enzyme Dephosphorylation) , 1994, Plant physiology.

[35]  G. Pearce,et al.  Structure-activity of deleted and substituted systemin, an 18-amino acid polypeptide inducer of plant defensive genes. , 1993, The Journal of biological chemistry.

[36]  P. Minchin,et al.  Electrical signalling and systemic proteinase inhibitor induction in the wounded plant , 1992, Nature.

[37]  D. Klessig,et al.  Temperature-Dependent Induction of Salicylic Acid and Its Conjugates during the Resistance Response to Tobacco Mosaic Virus Infection. , 1992, The Plant cell.

[38]  M. Sussman,et al.  Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat. , 1992, Biochemistry.

[39]  E. Farmer,et al.  Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. , 1992, The Plant cell.

[40]  M. Palmgren Regulation of plant plasma membrane H+‐ATPase activity , 1991 .

[41]  G. Pearce,et al.  A Polypeptide from Tomato Leaves Induces Wound-Inducible Proteinase Inhibitor Proteins , 1991, Science.

[42]  D. Bowles,et al.  The role of pH and ion transport in oligosaccharide-induced proteinase inhibitor accumulation in tomato plants. , 1990 .

[43]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[44]  L. Willmitzer,et al.  Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[45]  I. Raskin,et al.  Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Serrano Plasma Membrane ATPase , 1989 .

[47]  D. Bowles,et al.  The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids , 1988 .

[48]  M. Cocucci Inhibition of plasma membrane and tonoplast ATPases by erythrosin B , 1986 .

[49]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[50]  L. Hadwiger,et al.  Chitosans and pectic polysaccharides both induce the accumulation of the antifungal phytoalexin pisatin in pea pods and antinutrient proteinase inhibitors in tomato leaves. , 1983, Biochemical and biophysical research communications.

[51]  Michael D Greenfield,et al.  Wound-Induced Proteinase Inhibitor in Plant Leaves: A Possible Defense Mechanism against Insects , 1972, Science.

[52]  S. K. Boey,et al.  Plasma Membrane , 2005 .