Skip to main content

Lipopeptide Secondary Metabolites from the Phytopathogenic Bacterium Pseudomonas Syringae

  • Chapter
Advances in Microbial Toxin Research and Its Biotechnological Exploitation

Abstract

Over the past 20 years or so, significant advances have been made in the study of the secondary metabolism of the widespread phytopathogenic Gram-negative bacterium Pseudomonas syringae. Interdisciplinary approach, which required the expertise of plant pathologists, chemists, biochemists and molecular biologists, led to the discovery of a new family of bioactive peptide secondary metabolites. The determination of their structures was pivotal for the investigations on the biosynthetic pathways, their relevance in the development of plant disease, and for the understanding of the molecular bases of their biological activities in plant, microbial and animal cells. In particular, the antibiotic activities of some of these compounds appear very interesting in the perspective of their utilization both in medicine and in agriculture. The goal of this chapter is to summarize the present knowledge in various areas of research on P. syringae peptide metabolites.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adetuyi, F.C., Isogai, A., Di Giorgio, D., Ballio, A., and Takemoto, J.Y., 1995, Saprophytic Pseudomonas syringae strani M1 of wheat produces cyclic lipodepsipeptides, FEMS Microbiol. Lett. 131: 63–67.

    Article  PubMed  CAS  Google Scholar 

  • Agner, G., Kaulin, Y.A., Gurney, P.A., Szabo, Z., Schagina, L.V., Takemoto, J.Y., and Blasko, K., 2000a, Membrane-permeabilizing activities of cyclic lipodepsipeptides, syringopeptin 22A and syringomycin E from Pseudomonas syringae pv. syringae in human red blood cells and in bilayer lipid membranes, Bioel ectrochem. 52: 161–167.

    CAS  Google Scholar 

  • Agner, G., Kaulin, Y.A., Schagina, L.V., Takemoto, J.Y., and Blasko, K., 2000b, Effect of temperature on the formation and inactivation of syringomycin E pores in human red blood cells and bimolecular lipid membranes, Biochim. Biophys. Acta 1466: 79–86.

    Article  CAS  Google Scholar 

  • Backman, P.A., and DeVay, J.E., 1971, Studies on the mode of action and biogenesis of the phytotoxin syringomycin, Physiol. Pathol. 1: 215–233.

    Article  CAS  Google Scholar 

  • Ballio, A., Barra, D., Bossa, F., Collina, A., Grgurina, I., Marino, G., Paci, M., Pucci, P., Segre, A., and Simmaco, M., 1991, Syringopeptins, new phytotoxic lipodepsipeptides of Pseudomonas syringae pv. syringae, FEBS Lett. 291: 109–112.

    Article  PubMed  CAS  Google Scholar 

  • Ballio, A., Barra, D., Bossa, F., DeVay, J.E., Grgurina, I., Iacobellis, N.S., Marino, G., Pucci, P., Simmaco, M., and Surico, G., 1988, Multiple forms of syringomycin, Physiol. Mol. Plant Pathol. 33: 493–496.

    Article  CAS  Google Scholar 

  • Ballio, A., Bossa, F., Camoni, L., Di Giorgio, D., Flamand, M.C., Maraite, H., Nitti, G., Pucci, P., and Scaloni, A., 1996, Structure of fuscopeptins, phytotoxic metabolites of Pseudomonas fuscovaginae, FEBS letters 381: 213–216.

    Article  PubMed  CAS  Google Scholar 

  • Ballio, A., Bossa, F., Collina, A., Gallo, M., Iacobellis, N.S., Paci, M., Pucci, P., Scaloni, A., Segre, A., and Simmaco, M., 1990, Structure of syringotoxin, a bioactive metabolite of Pseudomonas syringae pv. syringae, FEBS Lett. 269: 377–380.

    Article  PubMed  CAS  Google Scholar 

  • Ballio, A., Bossa, F., Di Giorgio, D., Di Nola, A., Manetti, C., Paci, M., Scaloni, A., and Segre, A., 1995, Solution conformation of the Pseudomonas syringae pv. syringae phytotoxic lipodepsipeptide syringopeptin 25 A. Two-dimensional NMR, distance geometry and molecular dynamics, Eur, J. Biochem. 234: 747–758.

    CAS  Google Scholar 

  • Ballio, A., Bossa, F., Di Giorgio, D., Ferranti, P., Paci, M., Pucci, P., Scaloni, A., Segre, A., and Strobel, G.A., 1994a, Novel bioactive lipodepsipeptides from Pseudomonas syringae: the pseudomycins, FEBS Lett. 355: 96–100.

    Article  PubMed  CAS  Google Scholar 

  • Ballio, A., Collina, A., Di Nola, A., Maneti, C., Paci, M., and Segre, A., 1994b, Determination of structure and conformation in solution of syringotoxin, a lipodepsipeptide from Pseudomonas syringae pv. syringae by 2D-NMR and molecular dynamics, Struct. Chem. 5: 43–50.

    Article  CAS  Google Scholar 

  • Bard, M. 1972, Biochemical and genetic aspects of nystation resistance in Saccharomyces cerevisiae, J. Bacteriol. 111: 649–657.

    PubMed  CAS  Google Scholar 

  • Barè, S., Coiro, V.M., Scaloni, A., Di Nola, A., Paci, M., Segre, A.L., and Ballio, A., 1999, Conformations in solution of the fuscopeptins. Phytotoxic metabolites of Pseudomonas fuscovaginae, Eur. J. Biochem. 266: 1–10.

    Article  Google Scholar 

  • Batoko, H., de Kerchove d’Exaerde, A., Kinet, J-M., Bouharmont, J., Gage, R.A., Maraite, H., and Boutry, M., 1998, Modulation of plant plasma membrane H’-ATPase by phytotoxic lipodepsipeptide produced by the plant pathogen Pseudomonas fuscovaginae, Biochim. Biophys. Acta 1372: 216–226.

    Google Scholar 

  • Bender, C.L., Alarcón-Chaidez, F., and Gross, D.C., 1999, Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases, Microbiol. Mol. Biol. 63: 266–292.

    CAS  Google Scholar 

  • Bidwai, A.P., and Takemoto, J.Y., 1987, Bacterial phytotoxin, syringomycin, induces a protein kinase-mediated phosphorylation of red beet plasma membrane polypeptides, Proc. Natl. Acad. Sci. 84: 6755–6759.

    Article  PubMed  CAS  Google Scholar 

  • Bidwai, A.P., Zhang, L., Bachmann, R.C., and Takemoto J.Y., 1987, Mechanism of action of Pseudomonas syringae phytotoxin, syringomycin, Plant. Physiol. 83: 39–43.

    Article  PubMed  CAS  Google Scholar 

  • Blasko, K., Schagina, L.V., Agner, G., Kaulin, Y.A., and Takemoto, J.Y., 1998, Membrane sterol composition modulates the pore forming activity of syringomycin E in human red blood cells, Biochim. Biophys. Acta 1373: 163–169.

    Article  CAS  Google Scholar 

  • Brodey, C.L., Rainey, B.P., Tester, M., and Johnstone, K., 1991, Bacterial blotch disease of the cultivated mushroom is caused by an ion channel forming lipodepsipeptide toxin, Mol. Plant-Microbe Interact. 4: 407–411.

    Article  CAS  Google Scholar 

  • Bradbury, J.F., 1986, Guide to Plant Pathogenic Bacteria, Kew CAB International Mycological Institute, London.

    Google Scholar 

  • Bull, C.T., Stack, J.P., and Smilanick, J.L., 1997, Pseudomonas syringae strain ESC-10 and ESC-11 survive in wounds on citrus and control green and blue molds of citrus, Biol. Control 8: 81–88.

    Google Scholar 

  • Bull, C.T., Wadsworth, M.L., Sorensen, K.M., Takemoto, J.Y., Austin, R.K., and Smilanick, J.L., 1998, Syringomycin E produced by biological control agens controls green mold on lemons, Biol. Control 12: 89–95.

    Article  Google Scholar 

  • Bultreys, A., and Gheysen, I., 1999, Biological and molecular detection of toxic lipodepsipeptide-producing Pseudomonas syringae strains and PCR identification in plants, Appl. Environ. Microbiol. 65: 1904–1909.

    PubMed  CAS  Google Scholar 

  • Camoni, L., Di Giorgio, D., Marra, M., Aducci, P., and Ballio, A., 1995, Pseudomonas syringae pv. Syringae phytotoxins reversibly inhibit the plasma membrane H+-ATPase and disrupt unilamellar liposomes, Biochem. Biophys.Res.Com. 214: 118–124.

    CAS  Google Scholar 

  • Che, F.S., Kasamo, K., Fuchuchi, N., Isogai, A., and Suzuki, A., 1992, Bacterial phytotoxins, syringomycin, syringostatin and syringotoxin, exert their effect on the plasma membrane hydrogen ion-ATPase partly by a detergent-like action and partly by inhibition of the enzyme, Physiol. Plant. 86: 518–524.

    Article  CAS  Google Scholar 

  • Chen, S.H., Sun, X., Boyer, R., Paschal, J., Zeckner, D., Current, W., Zweifel, M., and Rodriguez, M., 2000, Syntheses and biological evaluation of novel pseudomycin side-chain analogues, Part 2, Bioorg. Med. Chem. Letters 10: 2107–2110.

    Article  CAS  Google Scholar 

  • Cliften, P., Wang, Y., Mochizuchi, D., Miyakawa, T., Wangspa, R., Hughes, J., and Takemoto, J. Y., 1996, Syr2, a gene necessary for syringomycin growth inhibition of Saccharomyces cerevisiae, Microbiol. 142: 477–484.

    CAS  Google Scholar 

  • Coiro, V.M., Segre, A.L., Di Nola, A., Paci, M., Grottesi, A., Veglia, G., and Ballio, A., 1998, Solution conformation of the Pseudomonas syringae MSU 16H phytotoxic lipodepsipeptide pseudomycin A determined by computer simulations using distance geometry and molecular dynamics from NMR data, Eur. J. Biochem. 257: 449–456.

    Article  PubMed  CAS  Google Scholar 

  • Conti, E., Stachelhaus, T., Marahiel, MA, and Brick, P., 1997, Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S, EMBO J. 16: 4171–4183.

    Article  Google Scholar 

  • Dalla Serra, M., Fagiuoli, G., Nordera, P., Bernhart, I., Della Volpe, C., Di Giorgio, D., Ballio, A., and Menestrina, G., 1999a, The interaction of lipodepsipeptide toxins from Pseudomonas syringae pv. syringae with biological membranes: a comparison of syringotoxin, syringomycin and two syringopeptins, Mol. Plant-Microbe Interact. 12: 391–400.

    Article  PubMed  Google Scholar 

  • Dalla Serra, M., Bernhart, I., Nordera, P., Di Giorgio, D., Ballio, A., and Menestrina, G., 1999b, Conductive properties and gating of channels formed by syringopeptin 25 A, a bioactive lipodepsipeptide from Pseudomonas syringae pv. syringae, in planar lipid membranes, Mol. Plant-Microbe Interact. 12: 401–409.

    Article  PubMed  Google Scholar 

  • De Lucca, A.J., Jacks, T.J., Takemoto, J.Y., Vinyard, B., Peter, J., Navarro, E., and Walsh, T.J., 1999, Fungal lethality, binding and cytotoxicity of syringomycin E., Antimicrob. Agents and Chemother. 43: 371–373.

    Google Scholar 

  • De Lucca, A.J., and Walsh, T.J., 1999, Antifungal peptides: novel therapeutic compounds against emerging pathogens, Antimicrob. Agents and Chemother. 1: 1–11.

    Google Scholar 

  • DeVay, J.E., Lukezic, F.L., Sinden, S.L., English, H., and Coplin, D.L., 1968, A biocide produced by pathogenic isolates of Pseudomonas syringae and its possible role in the bacterial canker of peach trees, Phytopathol. 58: 95–101.

    Google Scholar 

  • Di Giorgio, D., Camoni, L., and Ballio, A., 1994, Toxins of Pseudomonas syringae pv. syringae affect proton transport across the plasma membrane of maize, Physiol. Plant. 91: 741–746.

    Article  Google Scholar 

  • Di Giorgio, D., Camoni, L., Marchiafava, C., and Ballio, A., 1997, Biological activities of pseudomycin A, a lipodepsinonapeptide from Pseudomonas syringae MSU 16H, Phytochem. 45: 1385–1391.

    Article  Google Scholar 

  • Di Giorgio, D., Camoni, L., Mott, K.A., Takemoto, J.Y., and Ballio, A., 1996a, Syringopeptins, Pseudomonas syringae pv. syringae pytotoxins, resemble syringomycin in closing stomata, Plant Pathol. 45: 564–571.

    Article  Google Scholar 

  • Di Giorgio, D., Lavermicocca, P., Marchiafava, C., Camoni, L., Surico, G., and Ballio, A., 1996b, Effect of syringomycin E and syringopeptins on isolated plant mitochondria, Physiol. Mol. Plant Pathol. 48: 325–334.

    Article  Google Scholar 

  • Emanuele, M.C., Scaloni, A., Lavermicocca, P., Iacobellis, N.S., Camoni, L., Di Giorgio, D., Pucci, P., Paci, M., Segre, A., and Ballio, A., 1998, Corpeptins, new bioactive lipodepsipeptides from cultures of Pseudomonas corrugata, FEBS Lett. 433: 317–320.

    Article  PubMed  CAS  Google Scholar 

  • Feigin, A.M., Schagina, L.V., Takemoto, J.Y., Teeter, J.H., and Brand, J.G., 1997, The effect of sterol on the sensitivity of membranes to the channel-forming antifungal antibiotic, syringomycin E., Biochim. Biophys. Acta 1324: 102–110.

    Article  PubMed  CAS  Google Scholar 

  • Feigin, A.M., Takemoto, J.Y., Wangspa, R., Teeter, J.H., and Brand, J.G., 1996, Properties of voltage-gated ion channels formed by syringomycin E in planar lipid bilayers, J. Membr. Biol. 149: 41–47.

    Article  PubMed  CAS  Google Scholar 

  • Flamand, M.C., Pelsser, S., Ewbank, E., and Maraite, H., 1996, Production of syringotoxin and other bioactive peptides by Pseudomonas fuscovaginae, Physiol. Mol. Plant Pathol. 48: 217–231.

    Article  CAS  Google Scholar 

  • Fogliano, V., Gallo, M., Vinale, F., Ritieni, A., Randazzo, G., Greco, M.L., Lops, R., and Graniti, A., 1999, Immunological detection of syringopeptins produced by Pseudomonas syringae pv. lachrymans, Physiol. Mol. Plant Pathol. 55: 255–261.

    Article  CAS  Google Scholar 

  • Fukuchi, N., Isogai, A., Nakayama, J., and Suzuki, A., 1990a, Structure of syringotoxin B, a phytotoxin produced by citrus isolates of Pseudomonas syringae pv. syringae, Agric. Biol. Chem. 54: 3377–3379.

    Article  PubMed  CAS  Google Scholar 

  • Fukuchi, N., Isogai, A., Nakayama, J., Takayama, S., Yamashita, S., Suyama, K., and Suzuki, A., 1992a, Isolation and structural elucidation of syringostatins, phytotoxins produced by Pseudomonas syringae pv. syringae lilac isolate, J. Chem. Soc. Perkin Trans 1: 875–880.

    Article  Google Scholar 

  • Fukuchi, N., Isogai, A., Nakayama, J., Takayama, S., Yamashita, S., Suyama, K, Takemoto, J.Y., and Suzuki, A., 1992 b, Structure and stereochemistry of three phytoxins, syringomycin, syringotoxin and syringostatin, produced by Pseudomonas syringae pv. syringae, J. Chem. Soc. Perkin Trans. 1: 1149–1157.

    Google Scholar 

  • Fukuchi, N., Isogai, A., and Suzuki, A., 1991, Stereochemistry of syringostatin, syringomycin and syringotoxin, phytotoxins of Pseudomonas syringae pv. syringae, Agric. Biol. Chem. 55: 625–627.

    Article  CAS  Google Scholar 

  • Fukuchi, N., Isogai, A., Yamashita, S., Suyama, K., Takemoto, J.Y., and Suzuki, A., 1990b, Structure of phytotoxin syringomycin produced by sugar cane isolate of Pseudomonas syringae pv. syringae, Tet. Lett. 31: 1589–1592.

    Article  CAS  Google Scholar 

  • Gallo, M., Fogliano, V., Ritieni, A., Peluso, L., Greco, M.L., Lops, R., and Graniti, A., 2000, Immunoassessment of Pseudomonas syringae lipodepsipeptides (syringomycins and syringopeptins), Phytopathol. mediterr. 39: 410–416.

    CAS  Google Scholar 

  • Gardan, L., Shafif, H.,and Grimont, P.A.D., 1997, DNA relatedness among pathovars of P. syringae and rekated bacteria, in: Pseudomonas syringae Pathovars and Related Pathogens, K. Rudolph, T. J. Burr, J. W. Mansfield, D. Stead, A. Vivian and J. von Kietzell, eds., Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 445–448.

    Chapter  Google Scholar 

  • Gevers, W., Kleinkauf, H., and Lipmann, F., 1968, The activation of amino acids for biosynthesis of gramicidin S., Proc. Nat. Acad Sci. 60: 269–276.

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez, C.F., DeVay, J.E., and Wakeman, R.J., 1981, Syringotoxin: a phytotoxin unique to citrus isolates of Pseudomonas syringae, Physiol. Plant Pathol. 18, 41–50.

    CAS  Google Scholar 

  • Grgurina, I., Barca, A., Cervigni, S., Gallo, M., Scaloni, A., and Pucci, P., 1994, Relevance of chlorine-substituent for the antifugal activity of syringomycin and syringotoxin, metabolites of the phytopathogenic bacterium Pseudomonas syringae pv. syringae, Experientia 50: 130–133.

    Article  PubMed  CAS  Google Scholar 

  • Grgurina, I., and Benincasa, M., 1994, Evidence of the non ribosomal biosynthetic mechanism in the formation of syringomycin and syringopeptin, bioactive lipodepsipeptides of the phytopathogenic bacterium Pseudomonas syringae pv. syringae, It. Biochem. Soc. Trans. 5: 143.

    Google Scholar 

  • Grgurina, I., Gross, D.C., Iacobellis, N.S., Lavermicocca, P., Takemoto, J.Y., and Benincasa, M., 1996, Phytotoxin production by Pseudomonas syringae pv. syringae: syringopeptin production by syr mutants defective in biosynthesis or secretion of syringomycin, FEMS Microbiol. Lett. 138: 35–39.

    Article  CAS  Google Scholar 

  • Grgurina, I., Iacobellis, N.S., Ippolito, C., and Curci, R., 1997b, Detection of Syringomycin in plant tissues infected with Pseudomonas syringae pv. syringae, in: Pseudomonas syringae Pathovars and Related Pathogens, K. Rudolph, T. J. Burr, J. W. Mansfield, D. Stead, A. Vivian and J. von Kietzell, eds., Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 188–191.

    Chapter  Google Scholar 

  • Grgurina, I., and Mariotti, F., 1999, Biosynthetic origin of syringomycin and syringopeptin 22, toxic secondary metabolites of the phytopathogenic bacterium Pseudomonas syringae pv. syringae, FEBS Lett. 462: 151–154.

    Article  PubMed  CAS  Google Scholar 

  • Grgurina, I., Scaloni, A., and Iacobellis, N.S., 1997a, A novel syringopeptin produced by a bean strain of Pseudomonas syringae pv. syringae, It. Biochem. Soc. Trans. 9: 397.

    Google Scholar 

  • Grigoriev, P., Schlegel, R., Domberger, K., and Grafe, U., 1995, Formation of membrane pores by aurantimycins A and B, new lipopeptide antibiotics from Streptomyces aurantiacus, Bioelectrochem. and Bioen. 36: 57–59.

    Article  CAS  Google Scholar 

  • Grilley, M.M., Stock, S.D., Dickson, R.C., Lester, R.L., and Takemoto, J.Y., 1998, Syringomycin action gene SYR2 is essential for sphingolipid 4-hydroxylation in Saccharomyces cerevisiae, J. Biol. Chem. 273: 11062–11068.

    Article  PubMed  CAS  Google Scholar 

  • Gross, D.C., Cody, S., Proebsting, E.L. Jr, Radamaker, G.K., and Spotts, R.A., 1984, Ecotypes and pathogenicity of ice-nucleation-active Pseudomonas syringae isolated from deciduous tree orchards, Phytopathology 74: 241–348.

    Article  Google Scholar 

  • Gross, D.C., and DeVay, J.E., 1977, Production and purification of syringomycin, a phytotoxin produced by Pseudomanas syringae, Physiol. Plant Pathol. 11: 13–28.

    CAS  Google Scholar 

  • Gross, D.C., DeVay, J.E., and Stadtman, F.H., 1977b, Chemical properties of syringomycin and syringotoxin: toxigenic peptides produced by Pseudomonas syringae, J. Appl. Bacteriol. 43: 453–464.

    Article  CAS  Google Scholar 

  • Guenzi, E., Galli, G., Grgurina, I., Gross, D.C., and Grandi, G., I998a, Characterization of the syringomycin synthetase gene cluster, J. Biol. Chem. 273: 32857–32863.

    Google Scholar 

  • Guenzi, E., Galli, G., Grgurina, I., Pace, E., Ferranti, P., and Grandi, G., 1998b, Coordinate transcription and physical linkage of domains in surfactin synthetase are not essential for proper assembly and activity of the multienzyme complex, J. Biol. Chem. 273: 14403–14410.

    Article  PubMed  CAS  Google Scholar 

  • Hama, H., Young, D.A., Radding, J.A., Ma, D., Tang, J., Stock, S.D., and Takemoto, J.Y., 2000, Requirement of sphingolipid alpha-hydroxylation for fungicidal action of syringomycin E., FEBS Lett. 478: 26–28.

    Article  PubMed  CAS  Google Scholar 

  • Harrison, L., Teplow, D. B., Rinaldi, M., and Strobel, G. A., 1991, Pseudomycins, a family of novel peptides from Pseudomonas syringae possessing broad-spectrum antifungal activity, J. Gen. Microbiol. 137: 2857–2865.

    Article  PubMed  CAS  Google Scholar 

  • Hemmi, K., Julmanop, C., Hirata, D., Tsuchiya, E., Takemoto, J.Y., and Miyakawa, T., 1995, The physiological roles of membrane ergosterol as revealed by the phenotypes of syrllerg3 null mutant of Saccharomyces cerevisiae, Biosci. Biotech. Biochem. 59: 482–486.

    Article  CAS  Google Scholar 

  • Hiramoto,M., Okada,K., and Nagai, 5.,1970, The revised structure of viscosin, a peptide antibiotic, Tet. Lett. 13: 1087–1090.

    Google Scholar 

  • Hirano, S.S., and Upper, C.D., 1990, Population biology and epidemiology of Pseudomonas syringae, Annual Review of Phytopathology 28: 155–177.

    Article  Google Scholar 

  • Hutchison, M.L., and Gross, D.C., 1997, Lipopeptide phytotoxin produced by Pseudomonas syringae pv. syringae: comparison of the biosurfactant and ion channel-forming activities of syringopeptin and syringomycin, Mol. Plant Microbe Interact. 10: 347–354.

    Article  PubMed  CAS  Google Scholar 

  • Hutchison, M.L, and Johnstone, K., 1993, Evidence of the involvement of the surface active properties on the extracellular toxin tolaasin in the manifestation of brown blotch disease symptoms by Pseudomonas tolaasii on Agarus bisporus, Physiol. Mol. Plant Pathol. 42: 373–384.

    Article  CAS  Google Scholar 

  • Hutchison, M.L., Tester, M.A., and Gross, D.C., 1995, Role of biosurfactant and ion channel-forming activities of syringomycin in transmembrane ion flux: a model for the mechanism of action in the plant-pathogen interaction, Mol. Plant Microbe Interact. 8: 1–10.

    Article  Google Scholar 

  • lacobellis, N.S., and Lavermicocca, P., 1990, Evidence for the presence of syringomycin-like substance in tissues infected with Pseudomonas syringae pv. syringae, in: 8rn Congress of Mediterranean Phytopathological Union, Agadir, Morocco, pp. 187–188.

    Google Scholar 

  • Iacobellis, N.S., Lavermicocca, P., Grgurina, I., Simmaco, M., and Ballio, A., 1992, Phytotoxic properties of Pseudomonas syringae pv. syringae toxins, Physiol. Mol. Plant Pathol. 40: 107–116.

    Article  CAS  Google Scholar 

  • Isogai, A., Iguchi, H., Nakayama, J., Kusai, J., Takemoto, J.Y., and Suzuki, A., 1995, Structural analysis of new syringopeptins by tandem mass spectrometry, Biosci. Biotech. Biochem. 59: 1374–1376.

    Article  CAS  Google Scholar 

  • Jamison, J., Levy, S., Sun, X., Zeckner, D., Current, W., Zweifel, M., Rodriguez, M., Turner, W., and Chen, S.H., 2000, Syntheses and antifungal activity of pseudomycin side-chain analogues, Part 1, Bioorg. Med. Chem. Letters 10: 2101–2105.

    Article  CAS  Google Scholar 

  • Janisiewicz, W.J., and Bors, B., 1995, Development of a microbial community of bacterial and yeast antagonists to control wound-invading postharvest pathogens of fruits, App. Environ. Microbiol. 9: 3261–3267.

    Google Scholar 

  • Janisiewicz, W.J., and Jeffers, S.N., 1997, Efficacy of commercial formulation of two biofungicides for control of blue mold and gray mold of apples in cold storage, Crop Protection 16: 629–633.

    Article  CAS  Google Scholar 

  • Janisiewicz, W.J., and Marchi, A., 1992, Control of storage rots on various pear cultivars with saprophytic strain of Pseudomonas syringae, Plant Disease 76: 555–560.

    Article  Google Scholar 

  • Julmanop, C., Takano, Y., Takemoto, J.Y., and Miyakawa, T., 1993, Protection by sterols against the cytotoxicity of syringomycin in the yeast Saccharomyces cerevisiae, J. Gen. Microbiol. 139: 2323–2327.

    Article  PubMed  CAS  Google Scholar 

  • Kaulin, Y.A., Schagina, L.V., Bezrukov, S.M., Maley, V.V., Feigin, A.M., Takemoto, J.Y., Teeter, J.H., and Brand, J.G., 1998, Cluster organization of ion channel formed by the antibiotic syringomycin E in bilayer lipid membranes, Biophys. J. 74: 2918–2925.

    CAS  Google Scholar 

  • Kauss, H., 1987, Some aspects of calcium-dependent regulation in plant metabolism, Annu. Rev. Plant Physiol. 38: 47–72.

    Article  CAS  Google Scholar 

  • Kauss, H., 1990, Role of the plasma membrane in host-pathogen interactions; pages 320–350 in: The Plant Plasma Membrane-Structure, Function and Molecular Biology. Larson, C. amd Moller, I. M. (eds) Springer-Verlag, Berlin.

    Google Scholar 

  • Kauss, H., Waldmann, T., Jeblick, W., and Takemoto, J.Y., 1991, The phytotoxin syringomycin elicits Cat+-dependent callose synthesis in suspension-cultured cells of Catharanthus roseus, Physiol. Plant. 81: 134–138.

    Article  CAS  Google Scholar 

  • Kenwick, S.,and Jacobsen, B.J., 1988, Biological control of Fusarium dry rot on potato with antagonistic bacteria I commercial formulation, Phytopathology 88: 47.

    Google Scholar 

  • Kleinkauf H., and von Döhren, H., 1987, Biosynthesis of peptide antibiotics, Ann. Rev. Microbiol. 41: 259–289. Kleinkauf, H., and von Döhren, H., 1996, A nonribosomal system of peptide biosynthesis, Eur. J. Biochem. 236: 335–351.

    Article  Google Scholar 

  • Klement, Z., Rudolph, K., and Sands, D.C., 1990, Methods in Phytobaceriolgy, Akademiai Kiado, Budapest.

    Google Scholar 

  • Layock, M.V., Hildebrand, P.D., Thibault, P., Walter, J.A., and Wright, J.L.C., 1991, Viscosin, a potent petidolipid biosurfactant and phytopathogenic mediator produced by a pectolytic strain of Pseudomonas fluorescens, J. Agric. Food Chem. 39: 438–489.

    Google Scholar 

  • Lam, B. S., Strobel, G. A., Harrison, L. A., and Lam, S T, 1987, Transposon mutagenesis and tagging of fluorescent Pseudomonas: antimycotic production is necessary for control of Dutch elm disease, Proc. Natl. Acad. Sci. 84: 6447–6451.

    Article  PubMed  CAS  Google Scholar 

  • Latoud, C., Peypoux, F., Michel, G., Genet, R., and Morgat, J.L., 1986, Interactions of antibiotics of the iturin group with human erythrocytes, Biochim. Biophys. Acta 856: 526–535.

    Article  PubMed  CAS  Google Scholar 

  • Latoud, C., Peypoux, F., and Michel,G.,1990, Interaction of iturin A, a lipopeptide antibiotic,with Saccharomyces cerevisiae cells: influence of the sterol membrane composition, Can J. Microbiol. 36: 384–389.

    Google Scholar 

  • Lavermicocca, P., Iacobellis, N.S., Simmaco, M., and Graniti, A., 1997, Biological properties and spectrum of activity of Pseudomonas syringae pv. syringae toxins, Physiol. Mol. Plant Pathol. 50: 129–140.

    Article  CAS  Google Scholar 

  • Little, O.K., Bostock, R.M., and Kirkpatrick, B.C., 1998, Genetic characterization of Pseudomonas syringae pv. syringae strains from stone fruits in California, App. Environ. Microbiol. 10: 3818–3823.

    Google Scholar 

  • Maget-Dana, R., Harnois, I., and Ptak, M., 1989, Interactions of the lipopeptide antifungal iturin A with lipids in mixed monolayers, Biochim. Biophys. Acta. 981: 309–314.

    Article  PubMed  CAS  Google Scholar 

  • Maget-Dana, R., Ptak, M. L., Peypoux, F., and Michel, G., 1985, Pore-forming properties of iturin A, a lipopeptide antibiotic, Biochim. Biophys. Acta 815: 405–409.

    Article  PubMed  CAS  Google Scholar 

  • Maget-Dana, R., and Ptak, M., 1995, Interactions of surfactins with membrane models, Biophys. J. 68: 1937–1943.

    Article  PubMed  CAS  Google Scholar 

  • Maget-Dana, R., Thimon, L., Peypoux, F., and Ptak, M., 1992, Surfactin/iturin interactions may explain the synergistic effect of surfactin on the biological properties of iturin A, Biochimie 74: 1047–1051.

    Article  PubMed  CAS  Google Scholar 

  • Marahiel, M.A., Stachelhaus, T., and Moots, H.D., 1997, Modular peptide synthetases involved in nonribosomal peptide synthesis, Chem. Rev. 97: 2651–2675.

    Article  PubMed  CAS  Google Scholar 

  • Marshall, E., 1994, The emerging fungal threat, Science 266: 1632–1633.

    Article  Google Scholar 

  • Metzger, J. W., Sawyer, W. H., Wille, B., Biesert, L., Bessler, W. G., and Jung, G., 1993, Interaction of immunologically-active lipopeptides with membranes, Biochim. Biophys. Acta. 1149: 29–39.

    Article  PubMed  CAS  Google Scholar 

  • Mo, Y.Y., Geibel, M., Bonsall, R.F., and Gross, D.C., 1995, Analysis of sweet cherry (Prunus avium L.) leaves for plant signal molecules that activate the syrB gene required for the synthesis of the phytotoxin, syringomycin, by Pseudomonas syringae pv. syringae, Plant Physiol. 107: 603–612.

    PubMed  CAS  Google Scholar 

  • Mo, Y. Y., and Gross, D. C., 1991a, Expression in vitro and during plant pathogenesis of the syrB gene required for syringomycin production by Pseudomonas syringae pv. syringae, Mol. Plant Microbe Interact. 4: 28–36.

    Article  CAS  Google Scholar 

  • Mo, Y.Y., and Gross, D.C., 1991b, Plant signal molecules activate the syrB gene, wich is required for syringomycin production by Pseudomonas syringae pv. syringae, J. Bacteriol. 18: 5784–5792.

    Google Scholar 

  • Morgan, K.M., and Chatterjee, A.K., 1985, Isolation and characterization of Tn5 insertion mutants of Pseudomonas syringae pv. syringae altered in the production of the peptide phytotoxin syringotoxin, J. Bacteriol. 14–18.

    Google Scholar 

  • Morgan, K.M., and Chatterjee, A.K., 1988, Genetic organization and regulation of proteins associated with production of syringotoxin by Pseudomonas syringae pv. syringae, J Bacteriol. 170: 5689–5697.

    PubMed  CAS  Google Scholar 

  • Mortshire-Smith, R.J., Nutkins, J.C., Packuran, L.C., Brodey, C.L., Rainey, P.B., Johnstone, K., and Williams, D.H., 1991, Determination of the structure of an extracellular peptide produced by the mushroom saprotroph Pseudomonas reactans, Tetrahedron 47: 3645–3654.

    Article  Google Scholar 

  • Mott, K.A., and Takemoto, J.Y., 1989, Syringomycin, a bacterial phytotoxin, closes stomata, Plant Physiol. 90: 1435–1439.

    Article  PubMed  CAS  Google Scholar 

  • Neu, T.R., Hartner,T., and Poralla, K., 1990, Surface active properties of viscosin, a peptidolipid antibiotic, Appl. Microbiol. Biotechnol. 32: 518–520.

    CAS  Google Scholar 

  • Nutkins, J.C., Mortshire-Smith, R.J., Packmamn, L.C., Brodey, C.L., Rainey, P.B., Johnstone, K., and Williams, D.H., 1991, Structure determination of tolaasin, an extracellular lipodepsipeptide produced by mushroom pathogen Pseudomonas tolaasii Paine, J. Am. Chem. Soc. 113: 2621–2627.

    Article  CAS  Google Scholar 

  • Paine, S.G., 1919, Studies on bacteriosis II. A brown blotch disease of cultivated mushrooms, Annals of Applied Biology 5: 206–219.

    Article  Google Scholar 

  • Paynter, V.A., and Alconero, R., 1979, A specific fluorescent antibody for detection of syringomycin in infected peach tree tissues, The Am. Physiopathol. Soc. 69: 493–496.

    CAS  Google Scholar 

  • Penner, D., DeVay, J.E., and Backman, P., 1969, The influence of syringomycin on ribonucleic acid synthesis, Plant Physiol. 44: 806–808.

    Article  PubMed  CAS  Google Scholar 

  • Potera, C., 1994, From bacteria: a new weapon against fungal infection, Science 265: 605.

    Article  PubMed  CAS  Google Scholar 

  • Quentin, M.J., Besson, F., Peypoux, F., and Michel, G., 1982, Action of peptidolipidic antibiotics of the iturin group on erythrocytes. Effect of some lipids on heamolysis, Biochim. Biophys. Acta 684: 207–211.

    Article  PubMed  CAS  Google Scholar 

  • Quigley, B.N., and Gross, D.C., 1994, Syringomycin production among strains of Pseudomonas syringae pv. syringae: conservation of the syrB and syrD genes,and activation of phytotoxin production by plant signal molecules, Mol. Plant-Microbe Interact. 7: 78–99.

    Article  PubMed  CAS  Google Scholar 

  • Quigley, B.N., Mo, Y.Y., and Gross, D.C., 1993, SyrD is required for syringomycin production by Pseudomonas syringae pathovar syringae and is related to a family of ATP-bindig secretion proteins, Mol. Microbiol. 9: 787–801.

    CAS  Google Scholar 

  • Reidl, H.H., Grover, T.A., and Takemoto, J.Y., 1989, Phosphorus-31 NMR evidence for cytoplasmic acidification and phosphate extrusion in syringomycin-treated cells of Rhodotorula pilimanae, Biochim. Biophys. Acta 1010: 325–329.

    Article  PubMed  CAS  Google Scholar 

  • Reidl, H.H., and Takemoto, J.Y., 1987, Mechanism of action of bacterial phytotoxin, syringomycin. Simultaneous measurement of early responses in yeast and maize, Biochim. Biophys. Acta 898: 59–69.

    Article  CAS  Google Scholar 

  • Rainey, P.B., Brodey, C.L., and Johnstone, K., 1991, Biological properties and spectrum of activity of tolaasin, a lipodepsipeptide toxin produced by the mushroom pathogen Pseudomonas tolaasii, Physiol. Mol. Plant Pathol. 39: 57–70.

    Article  CAS  Google Scholar 

  • Risse, D., Beiderbeck, H., Taraz, K., Budzikiewicz, H., and Gustine, D., 1995, Corrugatin, a lipopeptide siderophore from Pseudomonas corrugata, Z. Naturforsch 53: 295–304.

    Google Scholar 

  • Rodriguez, M.J., Belvo, M., Morris, R., Zeckner, D., Current, W.L., Sachs, R.K., and Zweifel, M.J., 2001, The synthesis of pseudomycin C via a novel acid promoted side-chain deacylation of pseudomycin A, Bioorg. Med. Chem. Lett. 11: 161–164.

    Article  PubMed  CAS  Google Scholar 

  • Scaloni, A., Bachmann, R.C., Takemoto, J.Y., Barra, D., Simmaco, M., and Ballio, A., 1994, Stereochemical structure of syringomycin, a phytotoxic metabolite of Pseudomonas syringae pv. syringae, Nat. Prod. Letters 4: 159–164.

    Article  CAS  Google Scholar 

  • Scaloni, A., Camoni, L., Di Giorgio, D., Scortichini, M., Cozzolino, R., and Ballio, A., 1997, A new syringopeptin produced by Pseudomonas syringae pv. syringae strain isolated from diseased twigs of laurel, Physiol. Mol. Plant Pathol. 51: 259–264.

    Article  CAS  Google Scholar 

  • Scholz-Schroeder, B.K., Hutchinson, M.L., Grgurina, I., and Gross, D.C., 2001, The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B 301 D on the basis of sypA and syrB 1 biosynthesis mutant analysis, Mol. Plant Microbe Interact. 14: 336–348.

    Google Scholar 

  • Scheffer, R.J., 1983, Biological control of Dutch elm disease by Pseudomonas species, Annals Appl. Biol. 103: 21–30.

    Article  Google Scholar 

  • Segre, A., Bachman, R.C., Ballio, A., Bossa, F., Grgurina, I., Iacobellis, N.S., Marino, G., Pucci, P., Simmaco, M., and Takemoto, J.Y., 1989, The structure of syringomycin A1, E and G., FEBS Lett. 255: 27–31.

    Article  CAS  Google Scholar 

  • Sinden, S.L., De Vay, J.E., and Backman, P.A., 1971, Properties of syringomycin, a wide spectrum antibiotic and phytotoxin produced by Pseudomonas syringae, and its role in the bacterial canker disease of peach trees, Physiol. Plant Pathol. 1: 199–210.

    Article  CAS  Google Scholar 

  • Singh, V.K., and Takemoto, J.Y., 1996, Suppression of mitogen-induced lymphocyte proliferation by syringomycin E., FEMS Immunol. Medical Microbiol. 15: 177–179.

    Article  CAS  Google Scholar 

  • Sorensen, K.N., Kim, K-H, and Takemoto, J.Y., 1996, In vitro antifungal and fungicidal activities and erythrocyte toxicities of cyclic lipodepsinonapeptides produced by Pseudomonas syringae pv. syringae, Antimicrob. Agents and Chemother. 40: 2710–2713.

    CAS  Google Scholar 

  • Sorensen, K.N., Kim, K-H, and Takemoto, J.Y., 1998a, PCR detection of cyclic lipodepsinonpeptide-producing Pseudomonas syringae pv. syringae and similarity of strains, Appl. Environ. Microbiol. 64: 226–230.

    PubMed  CAS  Google Scholar 

  • Sorensen, K.N., Wangstrom, A.A., Allen, S.D., and Takemoto, J.Y., 1998b, Efficacy of syringomycin E in a murine model of vaginal candidiasis, J. Antibiotics 51: 743–749.

    Article  CAS  Google Scholar 

  • Stachelhaus, T., Mootz, H.D., and Marahiel, M.A., 1999, The specificity-conferring code of adenylation domains in non ribosomal peptide synthetase, Chem. Biol. 6: 493–505.

    Article  PubMed  CAS  Google Scholar 

  • Stapp, C., 1958, Pseudomonas syringae van Hall, in: Pflanzenpathogene Bakterien,Paul Parey in Berlin and Hamburg, pp. 198–204.

    Google Scholar 

  • Surico, G., and DeVay, J.E., 1982, Effect of syringomycin and syringotoxin produced by Pseudomonas syringae pv. syringae on structure and function of mitochondria isolated from locus spot resistant and susceptible maize lines, Physiol. Plant Pathol. 21: 39–53.

    Article  CAS  Google Scholar 

  • Stock, S.D., Hama, H., Radding, J.A., Young, D.A., and Takemoto, J.Y., 2000, Syringomycin E inhibition of Saccharomyces cerevisiae: requirement for biosynthesis of sphingolipids with very-long-chain fatty acids and mannose-and phosphoinositol-containing head groups, Antimicrob. Agents and Chemother. 44: 1174–1180.

    Article  CAS  Google Scholar 

  • Taguchi, N., Takano, Y., Julmanop, C., Wang, Y., Stock, S., Takemoto, J., and Miyakawa, T., 1994, Identification and analysis of the Saccharomyces cerevisiae SYR1 gene reveals that ergosterol is involved in the action of syringomycin, Microbiology 140: 353–359.

    Article  PubMed  CAS  Google Scholar 

  • Takemoto, J.Y., Yu, Y., Stock, S.D., and Miyakawa, T., 1993, Yeast genes involved in growth inhibition by Pseudomonas syringae pv syringae syringomycin family lipodepsipeptides, FEMS Microbiof. Lett. 114: 339–342.

    Article  CAS  Google Scholar 

  • Takemoto, J.Y., Zhang, L., Taguchi, N., Tachikawa, T., and Miyakawa, T., 1991, Mechanism of action of the phytotoxin syringomycin: a resistant mutant of Saccharomyces cerevisiae reveals an involvement of Cat’ transport, J. Gen. Microbiol. 137: 653–659.

    Article  CAS  Google Scholar 

  • Thimon, L., Peypoux, F., Maget-Dana, R., Roux, B., and Michel, G., 1992, Interactions of bioactive lipopeptides, iturin A and surfactin from Bacillus subtilis, Biotecnol. Appl. Biochem. 16: 144–151.

    CAS  Google Scholar 

  • Tolaas, A.G., 1915, A bacterial disease of cultivated mushrooms, Phytopathology 5: 51–54.

    Google Scholar 

  • van Hall, C.J.J., 1902, De seringenziegte, veroorzaakt door Pseudomonas syringae nov. sp. Bijdragen tot Kennis der bakterieele Plantenziekten, Amsterdam, 409 p.

    Google Scholar 

  • Vassilev, V., Lavermicocca, P., Di Giorgio, D., and Iacobellis, N.S., 1996, Production of syringomycins and syringopeptins by Pseudomonas syringae pv. atrofaciens, Plant Pathology 45: 316–322.

    Article  CAS  Google Scholar 

  • von Döhren, H., Keller, V., Vater, J., and Zocher, R., 1997, Multifunctional peptide synthetases, Chem. Rev. 97: 2675–2705.

    Article  Google Scholar 

  • von Kietzel, J., and Rudolph, K., 1997, Wheat diseases caused by Pseudomonas syringae pathovars, in: The Bacterial Diseases of Wheat: Concepts and Methods of Disease Management, E. Duvellier, L. Fucikovsky and K. Rudolph, eds., Mexico, CIMMYT, pp. 49–57.

    Google Scholar 

  • Williamson, S.M., Guzman, M., Anas,O., Martin, D.H., Jin, X., and Sutton,T.B., 1999, Evaluation of potential biocontrol agents for crown rot of banana, Phytopathology 89: S85.

    Google Scholar 

  • Xu, G.W., and Gross D.C., 1988a, Evaluation of the role of syringomycin in plant pathogenesis by using Tn5 mutants of Pseudomonas syringae pv. syringae defective in syringomycin production, Appl. Environ. Microbiol. 54: 1345–1353.

    PubMed  CAS  Google Scholar 

  • Xu, G.W., and Gross, D.C., 1988b, Physical and functional analyses of the syrA and syrB genes involved in syringomycin production by Pseudomonas syringae pv. syringae, J. Bacteriol. 170: 5680–5688.

    PubMed  CAS  Google Scholar 

  • Zhang, Y., Boyer, R., Sun, X., Paschal, J., and Chen, S.H., 2000, Serendipitous synthesis of novel dehydro-and dechloro-pseudomycin B derivatives, Bioorg. Med. Chem. Lett., 10: 775–778.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, J.H., Quigley, N.B., and Gross, D.C., 1995, Analysis of the syrB and syrC gene of Pseudomonas syringae pv. syringae indicates that syringomycin is synthesized by a thiotemplate mechanism, J. Bacteriol. 177: 4009–4020.

    PubMed  CAS  Google Scholar 

  • Zhang, J.H., Quigley, N.B., and Gross, D.C., 1997, Analysis of the syrP gene, which regulates syringomycin synthesis by Pseudomonas syringae pv. syringae, Appl. Environ. Microbiol. 63: 2771–2778.

    PubMed  CAS  Google Scholar 

  • Zhang, L., and Takemoto, J.Y., 1986, Mechanism of action of Pseudomonas syringae phytotoxin, syringomycin. Interaction with the plasma membrane of wild-type and respiratory-deficient strains of Saccharomyces cerevisiae, Biochim. Biophys. Acta 861: 201–204.

    PubMed  CAS  Google Scholar 

  • Zhang, L., and Takemoto, J.Y., 1987, Effects of Pseudomonas syringae pv. syringae phytotoxin, syringomycin, on plasma membrane functions of Rhodotorula pilimanae, Phytopathol. 77: 297–303.

    Article  CAS  Google Scholar 

  • Zhang, L., and Takemoto, J.Y., 1989, Syringomycin stimulation of potassium efflux by yeast cells, Biochim. Biophys. Acta 987: 171–175.

    Article  CAS  Google Scholar 

  • Zhang, Y.Z., Sun, X., Zeckner, D.J., Sachs, R.K., Current, W.L., and Chen, S-H., 2001a, 8-amido-bearing pseudomycin B (PSB) analogue: novel antifungal agents, Bioorg. Med. Chem. Letters 11: 123–126.

    Google Scholar 

  • Zhang, Y.Z., Sun, X., Zeckner, D.J., Sachs, R.K., Current, W.L., Gidda, J., Rodriguez, M., and Chen, S-H., 200lb, Syntheses and antifungal activities of novel 3-amido bearing pseudomycin analogues, Bioorg. Med. Chem. Letters 11: 903–907.

    Google Scholar 

  • Zimmerman, S., Ehrhardt, T., Plesch, G., and Müller-Röber, 1999, Ion channels in plant signaling, Cell. and Mol. Life Sci. 55: 183–203.

    Article  Google Scholar 

  • Ziegler, W., and Pavlovkin, J., 1985, Syringotoxin, ein phytotoxin von Pseudomonas syringae pv. syringae, erzeugt ionenkanäle in bimolekularen lipid membranen, Acta Phytopathologica Academiae Scientarum Hungaricae 20: 35–45.

    CAS  Google Scholar 

  • Ziegler, W., Pavlovkin, J., Remis, D., and Pokorny, J., 1986, The anionic/cationic selectivity of the syringotoxin channel, Biologia (Bratislava) 41: 1091–1096.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Grgurina, I. (2002). Lipopeptide Secondary Metabolites from the Phytopathogenic Bacterium Pseudomonas Syringae . In: Upadhyay, R.K. (eds) Advances in Microbial Toxin Research and Its Biotechnological Exploitation. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-4439-2_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-4439-2_9

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4419-3384-3

  • Online ISBN: 978-1-4757-4439-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics