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Current Ideas on the Genetics and Regulation of the Synthesis of Phaseolotoxin in Pseudomonas Syringae PV. Phaseolicola

  • Ariel Alvarez-Morales
  • Karina López-López
  • José Luis Hernández-Flores
Chapter

Abstract

The bacterium Pseudomonas syringae pv. phaseolicola is the causal agent of the “halo blight” disease of beans (Phaseolus vulgaris L.). This bacterium shares wide evolutionary relatedness with Pseudomonas savastonoi, and it was proposed that its taxonomic status be changed to P. savastanoi pv. phaseolicola; however, this proposal has been rejected and the organism has been maintained within the P. syringae group66. The disease attacks both foliage and pods, and is a major problem in temperate areas of the world. Leaf symptoms appear several days after infection as small water-soaked spots on the lower surface. At 7-10 days after infection, the lesions appear as greasy water-soaked points of infections. Pods can also be infected and lesions appear as brown or red water-soaked spots.Seeds may also become infected and the disease may be transmitted through the infected seed. At temperatures between 18°C and 23°C and high humidity, a zone of yellow-green tissue may develop around the initial site of infection after 3–8 days, giving rise to what is known as the chlorotic halo. In cases of severe infection, the chlorosis may become systemic. In fact, halo blight is considered to be a low-temperature disease and epidemic potential is greatest at temperatures ranging between 18°C and 22°C.

Keywords

Pathogenicity Island Homo Arginine Transition State Analogue Arginine Biosynthesis Ornithine Carbamoyltransferase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Aguilar, P.S., Hernandez-Arriaga, A.M., Cybulski, L.E., Erazo, A.C., and de Mendoza, D., 2001, Molecular basis of thermosensing: A two-component signal transduction thermometer in Bacillus subtilis. EMBO J., 20: 1681–1691.CrossRefGoogle Scholar
  2. 2.
    Alarcón-Chaidez, F.J., Keith, L., Zhao, Y., and Bender, C.L., 2003, RpoN (σ54 ) is required for plasmid-encoded coronatine biosynthesis in Pseudomonas syringae. Plasmid, 49: 106–117.CrossRefGoogle Scholar
  3. 3.
    Alfano, J.R., Charkowski, A.O., Deng, W.-L., Badel, J.L., Petnicki-Ocwieja, T., van Dijk, K., and Collmer, A., 2000, The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. USA, 97: 4856–4861.Google Scholar
  4. 4.
    Anzai, H., Yoneyama, K., and Yamaguchi, I., 1989, Transgenic tobacco resistant to a bacterial disease by the detoxification of a pathogenic toxin. Mol. Gen. Genet., 219: 492–494.CrossRefGoogle Scholar
  5. 5.
    Badel, J.L., Charkowski, A.O., Deng, W-L., and Collmer, A., 2002, A gene in the Pseudomonas syringae pv. tomato Hrp pathogenicity island conserved effector locus, hopPtoA1, contributes to efficient formation of bacterial colonies in planta and is duplicated elsewhere in the genome. Mol. Plant-Microbe Interact., 15: 1014–1024.PubMedCrossRefGoogle Scholar
  6. 6.
    Bender, C.L., Alarcón-Chaidez, E, and Gross, D.C., 1999, Pseudomonas syringae phytotoxins: Mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev., 63: 266–292.PubMedGoogle Scholar
  7. 7.
    Blanc-Potard, A.-B., Solomon, E, Kayser, J., and Groisman, E.A., 1999, The SPI-3 Pathogenicity island of Salmonella enterica. J. Bacteriol. 181: 998–1004.PubMedGoogle Scholar
  8. 8.
    Borchert, S., Patil, S.S., and Marahiel, M.A., 1992, Identification of putative multifunctional peptide synthetase genes using highly conserved oligonucleotide sequences derived from known synthetases. FEMS Microbiol. Lett., 92: 175–180.CrossRefGoogle Scholar
  9. 9.
    Bustos, S.A. and Schleif, R.F, 1993, Functional domains of the AraC protein. Proc. Natl. Acad. Sci. USA, 90: 5638–5642.PubMedCrossRefGoogle Scholar
  10. 10.
    Clarke, P.H. and Laverack, P.D., 1983, Expression of the argF gene of Pseudomonas aeruginosa in Pseudomonas aeruginosa, Pseudomonas putida and Escherichia coli. J. Bacteriol. 154: 508–512.PubMedGoogle Scholar
  11. 11.
    Cunin, R., Glansdorff, N., Piérard, A., and Stalon, V., 1986, Biosynthesis and metabolism of Arginine in bacteria. Microbiol. Rev., 50: 314–352.PubMedGoogle Scholar
  12. 12.
    De Ita, M.E., Marsch-Moreno, R., Guzmán, P., and Alvarez-Morales, A., 1998, Physical map of the chromosome of the phytopathogenic bacterium Pseudomonas syringae pv. Phaseolicola. Microbiology, 144: 493–501.CrossRefGoogle Scholar
  13. 13.
    de la Fuente-Martinez, J.M., Mosqueda-Cano, G., Alvarez-Morales, A., and Herrera-Estrella, L., 1992, Expression of a bacterial phaseolotoxin-resistant ornithyl transcarbamylase in transgenic tobacco confers resistance to Pseudomonas syringae pv. Phaseolicola. Bio/technology, 10: 905–909.PubMedCrossRefGoogle Scholar
  14. 14.
    Doekel, S. and Marahiel, M.A., 2001, Biosynthesis of natural products on modular peptide synthetases. Metab. Eng., 3: 64–77.PubMedCrossRefGoogle Scholar
  15. 15.
    Durbin, R.D., 1991, Bacterial phytotoxins: Mechanism of action. Experientia, 47: 776–783.CrossRefGoogle Scholar
  16. 16.
    Durbin, R.D. and Langston-Unkefer, P.J., 1988, The mechanisms for self-protection against bacterial phytotoxins. Annu. Rev. Phytopathol., 26: 313–329.CrossRefGoogle Scholar
  17. 17.
    Ferguson, A.R. and Johnston, J.S., 1980, Phaseolotoxin: Chlorosis, ornithine accumulation and inhibition of ornithine carbamoyltransferase in different plants. Physiol. Plant Pathol., 16: 269–275.CrossRefGoogle Scholar
  18. 18.
    Ferguson, A.R., Johnston, J.S., and Mitchell, R.E., 1980, Resistance of Pseudomonas syringae pv. phaseolicola to its own toxin, phaseolotoxin. FEMS Microbiol. Lett., 7: 123–125.CrossRefGoogle Scholar
  19. 19.
    Finlay, B.B. and Falkow, S., 1997, Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev., 61: 136–169.PubMedGoogle Scholar
  20. 20.
    Fritsche, E., Bergner, A., Humm, A., Piepersberg, W., and Huber, R., 1998, Crystal structure of L-arginine: inosamine-phosphate amidinotransferase StrB 1 from Streptomyces griseus: An enzyme involved in streptomycin biosynthesis. Biochemistry, 37: 17664–17672.PubMedCrossRefGoogle Scholar
  21. 21.
    Gallegos, M.T., Michan, C., and Ramos, J.L., 1993, The XylS/AraC family of regulators. Nucl. Acids Res., 21: 807–810.PubMedCrossRefGoogle Scholar
  22. 22.
    Glansdorff, N., 1996, Biosynthesis of arginine and polyamines. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 408–433. American Society for Microbiology Press, Washington, DC.Google Scholar
  23. 23.
    Goss, R.W., 1970, The relation of temperature to common and halo blight of beans. Phytopatholology, 30: 258–264.Google Scholar
  24. 24.
    Guerzoni, M.E., Lanciotti, R., and Cocconcelli, P.S., 2001, Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology, 147: 2255–2264.PubMedGoogle Scholar
  25. 25.
    Hatziloukas, E. and Panopoulos, N.J., 1992, Origin, structure and regulation of argK, encoding the phaseolotoxin-resistant carbamoyltransferase in Pseudomonas syringae pv. Phaseolicola, and functional expression of argK in transgenic tobacco. J. Bacteriol., 174: 5895–5909.PubMedGoogle Scholar
  26. 26.
    Hatziloukas, E., Panopoulos, N.J., Delis, S., Prosen, D.E., and Schaad, N.W., 1995, An open reading frame in the approximately 28-kb tox-argK gene cluster encodes a polypeptide with homology to fatty acid desaturases. Gene, 166: 83–87.PubMedCrossRefGoogle Scholar
  27. 27.
    Hendrickson, E.K., Guevera, P., Peñaloza-Vázquez, A., Shao, J., Bender, C., and Ausubel, F.M., 2000, Virulence of the phytopathogen Pseudomonas syringae pv. maculicola is rpoN dependent. J. Bacteriol., 182: 3498–3507.PubMedCrossRefGoogle Scholar
  28. 28.
    Hernández-Flores, J.L., López-López, K., Garcidueñas-Piña, R., Jofre-Garfias, A., and Alvarez-Morales, A., 2003, The global arginine regulator ArgR controls expression of argF in Pseudomonas syringae pv. phaseolicola but is not required for the synthesis of phaseolotoxin or for the regulated expression of argK. J. Bacteriol., in press.Google Scholar
  29. 29.
    Hernández-Guzmán, G. and Alvarez-Morales, A., 2001, Isolation and characterization of the gene coding for the amidinotransferase involved in the biosynthesis of phaseolotoxin in Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact., 14: 545–554.PubMedCrossRefGoogle Scholar
  30. 30.
    Humm, A., Fritsche, E., and Steinbacher, S., 1997, Structure and reaction mechanism of L-arginine: glycine amidinotransferase. Biol. Chem., 378: 193–197.PubMedGoogle Scholar
  31. 31.
    Humm, A., Huber, R., and Mann, K., 1994, The amino acid sequences of human and pig L-arginine: glycine amidinotransferase. FEBS Lett., 339: 101–107.PubMedCrossRefGoogle Scholar
  32. 32.
    Jackson, R.W., Athanassopoulos, E., Tsiamis, G., Mansfield, J.W., Sesma, A., Arnold, D.L., Gibbon, M.J., Murillo, J., Taylor, J.D., and Vivian, A., 1999, Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc. Natl. Acad. Sci. USA, 96: 10875–10880.PubMedCrossRefGoogle Scholar
  33. 33.
    Jahn, O., Sauerstein, J., Laplace, E., and Reuter, G., 1989, Detection of an insensitive ornithine-carbamoyltransferase in strains of Pseudomonas syringae pv. phaseolicola with different phytotoxin-generating capacities. J. Basic Microbiol., 29: 299–303.PubMedCrossRefGoogle Scholar
  34. 34.
    Jahn, O., Sauerstein, J., and Reuter, G., 1987, Characterization of two ornithine carbamoyltransferases from Pseudomonas syringae pv. phaseolicola, the producer of phaseolotoxin. Arch. Microbiol., 147: 174–178.PubMedCrossRefGoogle Scholar
  35. 35.
    Jahn, O., Sauerstein, J., and Reuter, G., 1985, Detection of two ornithine carbamoyltransferases in a phaseolotoxin-producin strain of Pseudomonas syringae pv. phaseolicola. J. Basic Microbiol., 25: 543–546.PubMedCrossRefGoogle Scholar
  36. 36.
    Kim, J.-G., Park, B.K., Yoo, C.-H., Jeon, E., Oh, J., and Hwang, I., 2003, Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J. Bacteriol., 185: 3155–3166.PubMedCrossRefGoogle Scholar
  37. 37.
    Langley, D.B., Templeton, M.D., Fields, B.A., Mitchell, R.E., and Collyer, C.A., 2000, Mechanism of inactivation of ornithine transcarbamoylase by N δ-(N’-Sulfodiaminophosphinyl)-L-omithine, a true transition state analogue? J. Biol. Chem., 275: 20012–20019.PubMedCrossRefGoogle Scholar
  38. 38.
    López-López, K., Hernández-Flores, J.L., Cruz-Aguilar, M., and Alvarez-Morales, A., 2003, In Pseudomonas syringae pv. phaseolicola, expression of the argK gene, encoding the phaseolotoxinresistant ornithine carbamoyltransferase, is regulated indirectly by temperature and directly by a precursor resembling carbamoylphosphate. J. Bacteriol. 186: 146–153.CrossRefGoogle Scholar
  39. 39.
    Lu, C.-D. and Abdelal, A.T., 2001, The gdhB gene of Pseudomonas aeruginosa encodes an arginine-inducible NAD+-dependent glutamate dehydrogenase which is subject to allosteric regulation. J. Bacteriol., 183: 490–499.PubMedCrossRefGoogle Scholar
  40. 40.
    Markisch, U. and Reuter, G., 1990, Biosynthesis of homoarginine and ornithine as precursors of the phytoeffector phaseolotoxin by the amidinotransfer from arginine to lysine catalyzed by an amidinotransferase in Pseudomonas syringae pv. phaseolicola. J. Basic. Microbiol., 30: 425–433.CrossRefGoogle Scholar
  41. 41.
    Merriman, T.R., Merriman, M.E., and Lamont, L.L., 1995, Nucleotide sequence of pvdD, a pyoverdine biosynthetic gene from Pseudomonas aeruginosa: pvdD has similarity to peptide synthetases. J. Bacteriol., 177: 252–258.PubMedGoogle Scholar
  42. 42.
    Mitchell, R.E., 1983, Atypical toxin production by Pseudomonas syringae pv. Phaseolicola. Physiol. Plant Pathol. 22: 123–128.Google Scholar
  43. 43.
    Mitchell, R.E., 1978, Halo blight of beans: Toxin production by several Pseudomonas phaseolicola isolates. Physiol. Plant Pathol., 13: 37–49.CrossRefGoogle Scholar
  44. 44.
    Mitchell, R.E., 1976, Isolation and structure of a chlorosis-inducing toxin of Pseudomonas phaseolicola. Phytochemistry, 15: 1941–1947.CrossRefGoogle Scholar
  45. 45.
    Mitchell, R.E., 1984, The relevance of non-host-specific toxins in the expression of virulence by pathogens. Annu. Rev. Phytopathol., 22: 215–245.CrossRefGoogle Scholar
  46. 46.
    Mitchell, R.E. and Bieleski, R.L., 1977, Involvement of phaseolotoxin in halo blight of beans. Transport and conversion to functional toxin. Plant Physiol., 60: 723–729.PubMedCrossRefGoogle Scholar
  47. 47.
    Mitchell, R.E., Johnston, J.S., and Ferguson, A.R., 1981, Phaseolotoxin and other phosphosulphanyl compounds: Biological effects. Physiol. Plant Pathol., 19: 227–235.Google Scholar
  48. 48.
    Mosqueda, G., Van den Broeck, G., Saucedo, O., Bailey, A.-M., Alvarez-Morales, A., and Herrera-Estrella, L., 1990, Isolation and characterization of the gene from Pseudomonas syringae pv. phaseolicola encoding the phascolotoxin-insensitive ornithine carbamoyltransferase. Mol. Gen. Genet., 222: 461–466.PubMedCrossRefGoogle Scholar
  49. 49.
    Nishijyo, T., Haas, D., and Itoh, Y., 2001, The CbrA-CbrB two-component regulatory system controls the utilization of multiple carbon and nitrogen sources in Pseudomonas aeruginosa. Mol. Microbiol., 40: 917–931.PubMedCrossRefGoogle Scholar
  50. 50.
    Nishijyo, T., Park, S.-M., Lu, C.-D., Itoh, Y., and Abdelal, A.T., 1998, Molecular characterization of an operon encoding a system for transport of arginine and ornithine and the ArgR regulatory protein in Pseudomonas aeruginosa. J. Bacteriol., 180: 5559–5566.PubMedGoogle Scholar
  51. 51.
    Noël, L., Thieme, E., Nennstiel, D., and Bonas, O., 2002, Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J. Bacteriol., 184: 1340–1348.PubMedCrossRefGoogle Scholar
  52. 52.
    Nüske, J. and Fritsche, W., 1989, Phaseolotoxin production by Pseudomonas syringae pv. phaseolicola: The influence of temperature. J. Basic Microbiol., 29: 441–447.PubMedCrossRefGoogle Scholar
  53. 53.
    Park, S.-M., Lu, C.-D., and Abdelal, A.T., 1997, Cloning and characterization of argR, a gene that participates in regulation of arginine biosynthesis and catabolism in Pseudomonas aeruginosa PAO1. J. Bacteriol., 179: 5300–5308.PubMedGoogle Scholar
  54. 54.
    Park, S.-M., Lu, C.-D., and Abdelal, A.T., 1997, Purification and characterization of an arginine regulatory protein, ArgR, from Pseudomonas aeruginosa and its interactions with the control regions for the car, argF and aru operons. J. Bacteriol., 179: 5309–5317.PubMedGoogle Scholar
  55. 55.
    Patil, S.S., Kolattukudy, P.E., and Dimond, A.E., 1970, Inhibition of ornithine carbamoyl transferase from bean plants by the toxin of Pseudomonas phaseolicola. Plant Physiol., 46: 752–753.PubMedCrossRefGoogle Scholar
  56. 56.
    Peet, R.C., Lindgren, P.B., Willis, D.K., and Panopoulos, N.J., 1986, Identification and cloning of genes involved in phaseolotoxin production by Pseudomonas syringae pv. “phaseolicola”. J. Bacteriol., 166: 1096.PubMedGoogle Scholar
  57. 57.
    Peet, R.C. and Panopoulos, N.J., 1987, Ornithine carbamoyltransferase genes and phaseolotoxin immunity in Pseudomonas syringae pv. phaseolicola. EMBO J., 6: 3585–3591.PubMedGoogle Scholar
  58. 58.
    Peñaloza-Vázquez, A. and Bender, C.L., 1998, Characterization of corR, a transcriptional activator which is required for biosynthesis of the phytotoxin coronatine. J. Bacteriol., 180: 6252–6259.PubMedGoogle Scholar
  59. 59.
    Reuter, G., 1989, Enzymatic regulation of microbial phytoeffector biosynthesis. In M.E. Bushell and U. Grafe (eds), Bioactive Metabolites from Microorganisms. Elsevier, Amsterdam.Google Scholar
  60. 60.
    Rohde, B.H., Pohlack, B., and Ullrich, M.S., 1998, Occurrence of thermoregulation of genes involved in coronatine biosynthesis among various Pseudomonas syringae strains. J. Basic Microbiol., 38: 41–50.PubMedCrossRefGoogle Scholar
  61. 61.
    Rowley, K.B., Clements, D.E., Mandel, M., Humphreys, T., and Patil, S.S., 1993, Multiple copies of a DNA sequence from Pseudomonas syringae pathovar phaseolicola abolish thermoregulation of phaseolotoxin production. Mol. Microbiol., 8: 625–635.PubMedCrossRefGoogle Scholar
  62. 62.
    Rowley, K.B., Xu, R., and Patil, S.S., 2000, Molecular analysis of thermoregulation of phaseolotoxin-resistant ornithine carbamoyltransferase (argK) from Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact., 13: 1071–1080.PubMedCrossRefGoogle Scholar
  63. 63.
    Sawada, H., Kanaya, S., Tsuda, M., Suzuki, F., Azegami, K., and Saitou, N., 2002, A phylogenomic study of the OCTase genes in Pseudomonas syringae pathovars: The horizontal transfer of the argK-tox cluster and the evolutionary history of OCTase genes on their genomes. J. Mol. Evol., 54: 437–457.PubMedCrossRefGoogle Scholar
  64. 64.
    Sawada, H., Suzuki, F., Matsuda, I., and Saitou, N., 1999, Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster. J. Mol. Evol., 49: 627–644.PubMedCrossRefGoogle Scholar
  65. 65.
    Sawada, H., Takeuchi, T., and Matzuda, I., 1997, Comparative analysis of Pseudomonas syringae pv. actinidiae and pv. phaseolicola based on phaseolotoxin-resistant ornithine carbamoyltransferase gene (argK) and 16S-23S rRNA intergenic spacer sequences. Appl. Environ. Microbiol., 63: 282–288.PubMedGoogle Scholar
  66. 66.
    Schaad, N.W., Vidaver, A.K., Lacy, G.H., Rudolph, K., and Jones, J.B., 2000, Evaluation of proposed amended names of several pseudomonads and xanthomonads and recommendations. Phytopathology, 90: 208–213.PubMedCrossRefGoogle Scholar
  67. 67.
    Scholz-Schroeder, B.K., Soule, J.D., Lu, S.-E., Grgurina, I., and Gross, D.C., 2001, A physical map of the syringomycin and syringopeptin gene clusters localized to an approximately 145-kb DNA region of Pseudomonas syringae pv. syringae strain B301D. Mol. Plant-Microbe Interact., 14: 1426–1435.PubMedCrossRefGoogle Scholar
  68. 68.
    Shurtleff, M.C. and Averre III, C.W., 1997, Glossary of Plant-Pathological Terms, 1st edn. APS Press, St. Paul Minnesota.Google Scholar
  69. 69.
    Stachelhaus, T. and Marahiel, M.A., 1995, Modular structure of peptide synthetases revealed by dissection of the multyfunctional enzyme GrsA. J. Biol. Chem., 270: 6163–6169.PubMedCrossRefGoogle Scholar
  70. 70.
    Staskawicz, B.J. and Panopoulos, N.J., 1980, Phaseolotoxin transport in Escherichia coli and Salmonella typhimurium via the oligopeptidase permease. J. Bacteriol., 142: 474–479.PubMedGoogle Scholar
  71. 71.
    Staskawicz, B.J. and Panopoulos, N.J., 1979, A rapid and sensitive assay for phaseolotoxin. Phytopathology, 69: 663–666.CrossRefGoogle Scholar
  72. 72.
    Staskawicz, B.J., Panopoulos, N.J., and Hoogenraad, N.J., 1980, Phaseolotoxin insensitive ornithine carbamoyltransferase of Pseudomonas syringae pv. phaseolicola: Basis for immunity to phaseolotoxin. J. Bacteriol., 142: 720–723.PubMedGoogle Scholar
  73. 73.
    Tamura, K., Imamura, M., Yoneyama, K., Kohno, Y., Takikawa, Y., Yamaguchi, I., and Takahashi, H., 2002, Role of phaseolotoxin production by Pseudomonas syringae pv. actinidiae in the formation of halo lesions of kiwifruit canker disease. Physiol. Mol. Plant Pathol., 60: 207–214.CrossRefGoogle Scholar
  74. 74.
    Templeton, M.D., Mitchell, R.E., Sullivan, P.A., and Shepherd, M.G., 1985, The inactivation of ornithine transcarbamoylase by Nδ-(N’-sulphodiaminophosphinyl)-L-ornithine. Biochem. J., 228: 347–352.PubMedGoogle Scholar
  75. 75.
    Templeton, M.D., Sullivan, P.A., and Shepherd, M.G., 1986, Phaseolotoxin-insensitive L-ornithine transcarbamoylase from Pseudomonas syringae pv. phaseolicola. Physiol. Mol. Plant Pathol., 29: 393–403.CrossRefGoogle Scholar
  76. 76.
    Turgay, K. and Marahiel, M.A., 1994, A general approach for identifying and cloning peptide synthetase genes. Peptide Res., 7: 238–241.Google Scholar
  77. 77.
    Walker, J.B., 1973, Amidinotransferases. In P. D. Boyer (ed.), The Enzymes, 3rd edn., vol. IX. Academic Press, NY, London.Google Scholar
  78. 78.
    Wong, K.-K., McClelland, M., Stillwell, L.C., Sisk, E.C., Thurston, S.J., and Saffer, J.D., 1998, Identification and sequence analysis of a 27-kilobase chromosomal fragment containing a Salmonella pathogenicity island located at 92 minutes on the chromosome map of Salmonella enterica serovar typhimurium LT2. Infect. Immun., 66: 3365–3371.Google Scholar
  79. 79.
    Zhang, Y., Rowley, K.B., and Patil, S.S., 1993, Genetic organization of a cluster of genes involved in the production of phaseolotoxin, a toxin produced by Pseudomonas syringae pv. phaseolicola. J. Bacteriol., 175: 6451–6458.PubMedGoogle Scholar
  80. 80.
    Zhang, Y.X. and Patil, S.S., 1997, The phtE locus in the phaseolotoxin gene cluster has ORFs with homology to genes encoding amino acid transferases, the AraC family of transcriptional factors, and fatty acid desaturases. Mol. Plant-Microbe Interact., 10: 947–960.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2004

Authors and Affiliations

  • Ariel Alvarez-Morales
    • 1
  • Karina López-López
    • 1
  • José Luis Hernández-Flores
    • 1
  1. 1.Cinvestav IPN—Irapuato UnitDepartment of Genetic EngineeringIrapuatoMexico

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