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Genetics of toxin production and resistance in phytopathogenic bacteria

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Abstract

Genes for phytotoxin production have been identified and cloned from several phytopathogenic pseudomonads. These genes comprise physically linked clusters that have been located both on the chromosome and on endogenous plasmids. Contained within these genetic regions are resistance genes specific to those toxins that have a bactericidal component to their activity. DNA sequences required for toxin production are often conserved among bacteria with divergent host specificities, suggesting the ability of toxin genes to be transferred between bacteria. Toxins are usually modulators of plant pathogenicity, their production causing a significant increase in disease severity. In one case, however, toxin production appears to be a major contributor to the basic pathogenicity of a plant pathogenic bacterium.

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References

  1. Anzai, H., Yoneyama, K., and Yamaguchi, I., Transgenic tobacco resistant to a bacterial disease by the detoxification of a pathogenic toxin. Molec. gen. Genet.219 (1989) 492–494.

    Article  CAS  Google Scholar 

  2. Bender, C. L., and Malvick, D. K., Coronatine-producing strains ofPseudomonas syringae pathovarstomato, glycinea, andatropurpurea share related plasmid DNA sequences. Phytopathology78 (1988) 1527.

    Google Scholar 

  3. Bender, C. L., Malvick, D. K., and Mitchell, R. E., Plasmid-mediated production of the phytotoxin coronatine inPseudomonas syringae pv.tomato. J. Bact.171 (1989) 807–812.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bender, C. L., Stone, H. E., Sims, J. J., and Cooksey, D. A., Reduced pathogen fitness ofPseudomonas syringae pv.tomato Tn5 mutants defective in coronatine production. Physiol. molec. Plant Path.30 (1987) 273–283.

    Article  CAS  Google Scholar 

  5. Bidwai, A. P., and Takemoto, J. Y., Bacterial phytotoxin, syringomycin, induces a protein kinase-mediated phosphorylation of red beet plasma membrane polypeptides. Proc. natl. Acad. Sci. USA84 (1987) 6755–6759.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bidwai, A. P., Zhang, L., Bachmann, R. C., and Takemoto, J. Y., Mechanism of action ofPseudomonas syringae phytotoxin, syringomycin. Stimulation of red beet plasma membrane ATPase activity. Plant Physiol.83 (1987) 39–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Braun, A. C., A comparative study ofBacterium tabacum Wolf and Foster andBacterium angulatum Fromme and Murray. Phytopathology27 (1937) 283–304.

    Google Scholar 

  8. Carlson, P. S., Methionine sulfoximine-resistant mutants of tobacco. Science180 (1973) 1366–1368.

    Article  CAS  PubMed  Google Scholar 

  9. Chatterjee, A. K., Somylai, G., and Nordeen, R. O., Molecular cloning and expression of syringotoxin (syt) genes ofPseudomonas syringae pv.syringae, in: Pseudomonas: Biotransformations, Pathogenesis, and Evolving Biotechnology, pp. 58–63. Eds S. Silver, A. N. Chakrabarty, B. Inglewski and S. Kaplan. American Society for Microbiology, Washington. DC 1990.

    Google Scholar 

  10. Clayton, E. E., Toxin produced byBacterium tabacum and its relation to host range. J. agric. Res.48 (1934) 411–426.

    CAS  Google Scholar 

  11. Durbin, R. D., Uchytil, T. F., Steele, J. A., and Ribeiro, L. D., Tabtoxinine-β-lactam fromPseudomonas tabaci. Phytochemistry17 (1978) 147–148.

    Article  CAS  Google Scholar 

  12. Elliott, C., Halo blight of oats. J. agric. Res.19 (1920) 139–172.

    Google Scholar 

  13. Ferguson, A. R., Johnson, J. S., and Mitchell, R. E., Resistance ofPseudomonas syringae pv.phaseolicola to its own toxin, phaseolotoxin. Fedn Eur. Microbiol. Soc. Lett.7 (1980) 123–125.

    Article  CAS  Google Scholar 

  14. Ferguson, A. R., and Johnston, J. S., Phaseolotoxin: chlorosis, ornithine accumulation and inhibition of ornithine carbamoyltransferase in different plants. Physiol. Plant Path.16 (1980) 269–275.

    Article  CAS  Google Scholar 

  15. Gasson, M. J., Indicator technique for antimetabolic toxin production by phytopathogenic species ofPseudomonas. Appl. envir. Microbiol.39 (1980) 25–29.

    Article  CAS  Google Scholar 

  16. Gnanamanickam, S. S., Starratt, A. N., and Ward, E. W. B., Coronatine production in vitro and in vivo and its relation to symptom development in bacterial blight of soybean. Can. J. Bot.60 (1982) 645–650.

    Article  CAS  Google Scholar 

  17. Gonzalez, C. F., DeVay, J. E., and Wakeman, R. J., Syringotoxin: a phototoxin unique to citrus isolates ofPseudomonas syringae. Physiol. Plant Path.18 (1981) 41–50.

    Article  CAS  Google Scholar 

  18. Goss, R. W., The relationship of temperature to common and halo blight of beans. Phytopathology30 (1940) 258–264.

    Google Scholar 

  19. Gross, D. C., and Cody, Y. S., Mechanisms of plant pathogenesis byPseudomonas species. Can. J. Microbiol.31 (1985) 403–410.

    Article  CAS  Google Scholar 

  20. Gross, D. C., and DeVay, J. E., Population dynamics and pathogenesis ofPseudomonas syringae in maize and cowpea in relation to the in vitro production of syringomycin. Phytopathology67 (1977) 475–483.

    Article  Google Scholar 

  21. Gross, D. C., and DeVay, J. E., Production and purification of syringomycin, a phytotoxin produced byPseudomonas syringae. Physiol. Plant Path.11 (1977) 13–28.

    Article  CAS  Google Scholar 

  22. Hrabak, E. M., Rich, J. J., Kennedy, C. J., and Willis, D. K., A locus required for lesion formation byPseudomonas syringae pv.syringae on bean affects syringomycin production in vitro. Phytopathology79 (1989) 1178 (abstract).

    Google Scholar 

  23. Ichihara, A., Shiraishi, K., Sato, H., Sakamura, S., Nishiyama, K., sakai, R., Furasaki, A., and Matsumota, T., The structure of coronatine. J. Am. chem. Soc.99 (1977) 636–637.

    Article  CAS  Google Scholar 

  24. Johnson, J., and Murwin, H. F., Experiments on the control of wildfire of tobacco, in: Research Bulletin62, Agricultural Experiment Station of the University of Wisconsin, Madison 1925.

    Google Scholar 

  25. Kinscherf, T. G., Coleman, R. H., Barta, T. M., and Willis, D. K., isolation and characterization of a chromosomal region involved in tabtoxin production in the bean pathogenPseudomonas syringae BR2. J. Bact., in press.

  26. Knight, T. J., Durbin, R. D., and Langston-Unkefer, P. J., Role of glutamine synthetase adenylylation in the self-protection ofPseudomonas syringae subsp. ‘tabaci’ from its toxin, tabtoxinine-β-lactam. J. Bact.166 (1986) 224–229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Knight, T. J., Durbin, R. D., and Langston-Unkefer, P. J., Self-protection ofPseudomonas syringae pv. ‘tabaci’ from its toxin, tabtoxinine-β-lactam. J. Bact.169 (1987) 1954–1959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Koster, W. H., Cimarusti, C. M., and Sykes, R. B., Monobactams, in: Chemistry and biology of β-lactam antibiotics, pp. 339–375. Eds R. B. Morin and M. Gorman. Academic Press, New York 1982.

    Chapter  Google Scholar 

  29. Langston-Unkefer, P. J., Macy, P. A., and Durbin, R. D., Inactivation of glutamine synthetase by tabtoxin-β-lactam. Effects of substrates and pH. Plant Physiol.76 (1984) 71–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Levi, C., and Durbin, R. D., The isolation and properties of a tabtoxin-hydrolysing aminopeptidase from the periplasm ofPseudomonas syringae pv.syringae. Physiol. molec. Plant path.28 (1986) 345–352.

    Article  CAS  Google Scholar 

  31. Manning, J. M., Moore, S., Rowe, W. B., and Meister, A., Identification ofl-methionineS-sulfoximine as the diastereoisomer ofl-methionineSR-sulfoximine that inhibits glutamine synthetase. Biochemistry8 (1969) 2681–2685.

    Article  CAS  PubMed  Google Scholar 

  32. Marek, E. T., and Dickson, R. C., Cloning and characterization ofSaccharomyces cerevisiae genes that conferl-methionine sulfoximine and tabtoxin resistance. J. Bact.169 (1987) 2440–2448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Martin, J. F., and Liras, P., Organization and expression of genes involved in the biosynthesis of antibiotics and other secondary metabolites. A. Rev. Microbiol.43 (1989) 173–206.

    Article  CAS  Google Scholar 

  34. Mitchell, R. E., Isolation and structure of a chlorosis inducing toxin ofPseudomonas phaseolicola. Phytochemistry15 (1976) 1941–1947.

    Article  CAS  Google Scholar 

  35. Mitchell, R. E., Coronatine production by some phytopathogenic pseudomonads. Physiol. Plant Path.20 (1982) 83–89.

    Article  CAS  Google Scholar 

  36. Mitchell, R. E., Coronatine biosynthesis: incorporation ofl-[U-14C]isoleucine andl-[U14C]threonine into the 1-amido-1-carboxy-2-ethylcyclopropyl moiety. Phytochemistry24 (1985) 247–249.

    Article  CAS  Google Scholar 

  37. Mitchell, R. E., and Bielski, R. L., Involvement of phaseolotoxin in halo blight of beans: transport and conversion to functional toxin. Plant Physiol.60 (1977) 723–729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mitchell, R. E., Hale, C. N., and Shanks, J. C., Production of different pathogenic symptoms and different toxins by strains ofPseudomonas syringae pv.tomato not distinguishable by gel-immunodiffusion assay. Physiol. Plant Path.23 (1983) 315–322.

    Article  CAS  Google Scholar 

  39. Mitchell, R. E., and Young, H., Identification of a chlorosis-inducing toxin ofPseudomonas glycinea as coronatine. Phytochemistry17 (1978) 2028–2029.

    Article  CAS  Google Scholar 

  40. Moore, R. A., Starratt, A. N., Ma, S.-W., Morris, V. L., and Cuppels, D. A., Identification of a chromosomal region required for biosynthesis of the phytotoxin coronatine byPseudomonas syringae pv.tomato. Can. J. Microbiol.35 (1989) 910–917.

    Article  CAS  Google Scholar 

  41. Moore, R. E., Niemczura, W. P., Kwok, O. C. H., and Patil, S. S., Inhibitors of ornithine carbamoyltransferase fromP. syringae pv.phaseolicola. Revised structure of phaseolotoxin. Tetrahedron Lett.25 (1984) 3931–3934.

    Article  CAS  Google Scholar 

  42. Morgan, M. K., and Chatterjee, A. K., Isolation and characterization of Tn5 insertion mutants ofPseudomonas syringae pv.syringae altered in the production of the peptide syringotoxin. J. Bact.164 (1985) 14–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Morgan, M. K., and Chatterjee, A. K., Genetic organization and regulation of proteins associated with the production of syringotoxin byPseudomonas syringae pv.syringae. J. Bact.170 (1988) 5689–5697.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Morris, R. M., Genes specifying auxin and cytokinin biosynthesis in phytopathogens. A. Rev. Plan Physiol.37 (1986) 509–538.

    Article  CAS  Google Scholar 

  45. Nishiyama, K., Sakai, R., Ezuka, A., Ichihara, A., Shiraishi, K., Ogasawara, M., Sato, H., and Sakamura, S., Phytotoxic effect of coronatine produced byPseudomonas coronafaciens var.atropurpurea on leaves of Italian ryegrass. Ann. Phytopath. Soc. Japan42 (1976) 613–614.

    Article  Google Scholar 

  46. Parry, R. J., and Mafoti, R., Biosynthesis of coronatine, a novel polyketide. J. Am. chem. Soc.108 (1986) 4681–4682.

    Article  CAS  Google Scholar 

  47. Patil, S. S., Emmons, B., and Hayward, C., An ultraviolet-induced nontoxigenic mutant ofPseudomonas phaseolicola of altered pathogenicity. Phytopathology64 (1974) 590–595.

    Article  Google Scholar 

  48. Patil, S. S., Kolatukudy, P. E., and Dimond, A. E., Inhibition of ornithine carbamoyltransferase from bean plants by the oxin ofPseudomonas phaseolicola. Plant Physiol.46 (1970) 752–753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Patil, S. S., Tam, L. Q., and Sakai, W. S., Mode of action of the toxin fromPseudomonas phaseolicola. I. Toxin specificity, chlorosis, and ornithine accumulation. Plant Physiol.49 (1972) 803–807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Patil, S. S., Youngblood, P., Christiansen, P., and Moore, R. E., Phaseotoxin A: an antimetabolite fromPseudomonas phaseolicola. Biochem. biophys. Res. Commun.69 (1976) 1019–1027.

    Article  CAS  PubMed  Google Scholar 

  51. Peet, R. C., Lindgren, P. B., Willis, D. K., and Panopoulos, N. J., Identification and cloning of genes involved in phaseolotoxin production byPseudomonas syringae pv. ‘phaseolicola’. J. Bact.166 (1986) 1096–1105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Peet, R. C., and Panopoulos, N. J., Ornithine carbamoyltransferase genes and phaseolotoxin immunity inPseudomonas syringae pv.syringae. EMBO J.6 (1987) 3585–3591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Quigley, N. B., Mo, Y.-Y., and Gross, D. C., Genetic and DNA sequence analysis of the interval between two divergently transcribed phytotoxin biosynthesis genes fromPseudomonas syringae pv.syringae. Phytopathology79 (1989) 1178–1179.

    Google Scholar 

  54. Ream, W.,Agrobacterium tumefaciens and interkingdom genetic exchange. A. Rev. Phytopath.27 (1989) 583–618.

    Article  CAS  Google Scholar 

  55. Ribeiro, R. de L. D., Hagedorn, D. J., Durbin, R. D., and Uchtil, T. F., Characterization of the bacterium inciting bean wildfire in Brazil. Phytopathology69 (1979) 208–212.

    Article  Google Scholar 

  56. Sakai, R., Nishiyama, K., Ichihara, A., Shiraishi, K., and Sakamura, S., The relation between bacterial toxic action and plant growth regulation, in: Recognition and Specificity in Plant Host-Parasite Interactions, pp. 165–179. Eds J. M. Daly and I. Uritani. University Press, Baltimore, MD 1979.

    Google Scholar 

  57. Sato, M., A plasmid involved in coronatine production byPseudomonas syringae pv.atropurpurea. Proc. Fifth International Congress of Plant Pathology, Kyoto, Japan 1988, p. 12.

  58. Sato, M., Nishiyama, K., and Shirata, A., Involvement of plasmid DNA in the productivity of coronatine byPseudomonas syringae pv.atropurpurea. Ann. Phytopath. Soc. Japan49 (1983) 522–528.

    Article  CAS  Google Scholar 

  59. Schaad, N. W., and Cunfer, B. M., Synonymy ofPseudomonas coronafaciens, Pseudomonas coronafaciens pathovarzeae, Pseudomonas coronafaciens subsp.atropurpurea, andPseudomonas striafaciens. Int. J. syst. Bact.29 (1979) 213–221.

    Article  Google Scholar 

  60. Sinden, S. L., and Durbin, R. D., Glutamine synthetase inhibition: possible mode of action of wildfire toxin fromPseudomonas tabaci. Nature229 (1968) 379–380.

    Article  Google Scholar 

  61. Staskawicz, B. J., and Panopoulos, N. J., A rapid and sensitive microbiological assay for phaseolotoxin. Phytopathology69 (1979) 663–666.

    Article  CAS  Google Scholar 

  62. Staskawicz, B. J., and Panopoulos, N. J., Phaseolotoxin transport inEscherichia coli andSalmonella typhimurium via the oligopeptide permease. J. Bact.142 (1980) 474–479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Staskawicz, B. J., Panopoulos, N. J., and Hoogenraad, N. J., Phaseolotoxin-insensitive ornithine carbamoyltransferase ofPseudomonas syringae pv.syringae: basis for immunity to phaseolotoxin. J. Bact.142 (1980) 720–723.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Stewart, W. W., Isolation and proof of structure of wildfire toxin (Pseudomonas tabaci). Nature229 (1971) 174–178.

    Article  CAS  PubMed  Google Scholar 

  65. Surico, G., and DeVay, J. E., Effect of syringomycin and syringotoxin produced byPseudomonas syringae pv.syringae on structure and function of mitochondria isolated from holcus spot resistant and susceptible maize lines. Physiol. Plant Path.21 (1982) 39–53.

    Article  CAS  Google Scholar 

  66. Taylor, P. A., Schnoes, H. K., and Durbin, R. D., Characterization of chlorosis-inducing toxins from a plant pathogenicPseudomonas sp. Biochim. biophys. Acta286 (1972) 107–117.

    Article  CAS  PubMed  Google Scholar 

  67. Templeton, M. D., Sullivan, P. A., and Shepherd, M. G., Phaseolotoxin-insensitivel-ornithine transcarbamoylase fromPseudomonas syringae pv.phaseolicola. Physiol. molec. Plant Path.29 (1986) 393–403.

    Article  CAS  Google Scholar 

  68. Tessi, J. L., Estudio comparativo de dos bacterios patogenos en avena y determinacion de una toxina que origina sus diferencias. Rev. Invest. Agr.7 (1953) 131–145.

    Google Scholar 

  69. Thomas, M. D., and Durbin, R. D., Glutamine synthetase fromPseudomonas syringae pv.tabaci: properties and inhibition by tabtoxinine-β-lactam. J. gen. Microbiol.131 (1985) 1061–1067.

    CAS  Google Scholar 

  70. Thomas, M. D., Langston-Unkefer, P. J., Uchytil, T. F., and Durbin, R. D., Inhibition of glutamine synthetase from pea by tabtoxinine-β-lactam. Plant Physiol.71 (1983) 912–915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Turner, J. G., Tabtoxin, Produced byPseudomonas tabaci, decreasesNicotiana tabacum glutamine synthetase in vivo and causes accumulation of ammonia. Physiol. Plant Path.19 (1981) 57–67.

    Article  CAS  Google Scholar 

  72. Uchytil, T. F., and Durbin, R. D., Hydrolysis of tabtoxins by plant and bacterial enzymes. Experientia36 (1980) 301–302.

    Article  CAS  Google Scholar 

  73. Willis, D. K., Kinscherf, T. G., Coleman, R. H., and Barta, T. M., Identification and isolation of a DNA region required for tabtoxin production: apparent deletion inPseudomonas syringae pv.tabaci variantangula and Tox mutants, in: Phytotoxins and Plant Pathogenesis, pp. 61–70. Eds A. Graniti, R. D. Durbin and A. Ballio. Springer-Verlag, Berlin 1989.

    Chapter  Google Scholar 

  74. Xu, G.-W., and Gross, D. C., Evaluation of the role of syringomycin in plant pathogenesis by using Tn5 mutants ofPseudomonas syringae pv.syringae defective in syringomycin production. Appl. envir. Microbiol.54 (1988) 1345–1353.

    Article  CAS  Google Scholar 

  75. Xu, G.-W., and Gross, D. C., Physical and functional analyses of thesyrA andsyrB genes involved in syringomycin production byPseudomonas syringae pv.syringae. J. Bact.170 (1988) 5680–5688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Zhang, L., and Takemoto, J. Y., Effects ofPseudomonas syringae phytotoxin, syringomycin, on plasma membrane functions ofRhodotorula pilimanae. Phytopathology77 (1987) 297–303.

    Article  CAS  Google Scholar 

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Willis, D.K., Barta, T.M. & Kinscherf, T.G. Genetics of toxin production and resistance in phytopathogenic bacteria. Experientia 47, 765–771 (1991). https://doi.org/10.1007/BF01922455

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