Advertisement

Engineering Disease Resistance in Plants Using Phytotoxins as Molecular Stooges

  • P. Balasubramanian
  • R. Samiyappan
  • S. Babu
  • R. Nandakumar
  • V. Shanmugam
  • T. Raguchander
Chapter

Abstract

Onset of plant diseases often results in significant losses in crop yield. A disease is said to be set in when a compatible interaction between a plant pathogen and its host is established. In such a compatible interaction, the plant is rendered susceptible to the invading pathogen. Any relationship between a pathogen and its host plant, in reality, involves interactive molecular processes comprising plant’s genes controlling resistance/susceptibility on the one hand and avirulence/virulence genes of the pathogen on the other (de la Fuente-Martinez and Herrera-Estrella, 1993). Once a compatible interaction is established, the nature of subsequent biological impairments caused by the pathogen largely depend on a variety of biochemical blueprints encompassing production oflytic enzymes and/or toxins by the pathogen (Mitchell, 1984; Panopoulos and Peet, 1985). Enzymes secreted by pathogens cause dissolution of plant cell wall barrier while making the protoplasm vulnerable to attack by toxins which tear apart the naked protoplasm with an eventual loss of electrolytes and ultimate death of the cell (Vidhyasekaran, 1997).

Keywords

Transgenic Plant Glutamine Synthetase Plant Pathol Rhizoctonia Solani Sheath Blight 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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
  2. Bachmann, A.S., Matile, P., and Slusarenko, A.J., 1998, Inhibition of ornithine decarboxylase activity by phaseolotoxin: implications for symptom production in halo blight of French bean, Physiol. Mol. Plant Pathol. 53: 287–299.CrossRefGoogle Scholar
  3. Basnayake, W. V., and Birch, R.G., 1995, A gene from Alcaligenes denitrificans that confers albicidin resistance by reversible antibiotic binding, Microbiology 141: 551–560.PubMedCrossRefGoogle Scholar
  4. Batchvarova, R., Nikolaeva, V., Slavov, S., Bossolova, S., Valkov, V., Atanasova, S., Guelemerov, S., Atanassov, A., and Anzai, H., 1998, Transgenic tobacco cultivars resistant to Pseudomonas syringae pv. tabaci, Theor. Appl. Genet. 97: 986–989.CrossRefGoogle Scholar
  5. Bender, C. L., 1999, Chlorosis-inducing phytotoxins produced by Pseudomonas syringae, Eur. J. Plant Pathol. 105: 1–12.CrossRefGoogle Scholar
  6. Bender, C. L., Alarcon-Chaidez, F., and Gross, D. C., 1999, Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases, Microbiology and Molecular Biology Reviews 63: 266–292.PubMedGoogle Scholar
  7. Birch, R.G., and Patil, S.S., 1987, Evidence that an albicidin-like phytotoxin induces chlorosis in sugarcane leaf scald disease by blocking plastid DNA replication, Physiological and Molecular Plant Pathology 30: 207–214.CrossRefGoogle Scholar
  8. Bohlmann, F., Burckhardt, T., and Zidero, C., 1973, Naturally Occurring Acetylenes, Academic Press, New York.Google Scholar
  9. Braun, A. C., 1955, A study on the mode of action of wild fire toxin, Phytopathology 45: 659–664.Google Scholar
  10. Ciuffetti, L.M., Pope, M.R., Dunkle, L.D., Daly, J.M., and Knoche, H.W., 1983, Isolation and structure of an inactive product derived from the host-specific toxin produced by Helminthosporium carbonum, Biochemistry 22: 3507–3510.CrossRefGoogle Scholar
  11. Coleman, R.H., Shaffer, J., and True, H., 1996, Properties of ß-lactamase from Pseudomonas syringae, Curr. Microbiol. 32: 147–150.PubMedCrossRefGoogle Scholar
  12. Colrat, S., Deswarte, C., Latche, A., Klaebe, A., Bouzayen, M., Fallot, J., and Roustan, J. P., 1999a, Enzymatic detoxification of eutypine, a toxin from Eutypa lata, by Vitis vinifera cells: partial purification of an NADPHdependent aldehyde reductase, Planta 207: 544–550.CrossRefGoogle Scholar
  13. Colrat, S., Latche, A., Guis, M., Pech, J.C., Bouzayen, M., Fallot, J., and Roustan, J. P., 1999b, Purification and characterization of a NADPH-dependent aldehyde reductase from mung bean that detoxifies eutypine, a toxin from Eurypa lata, Plant Physiol. 119: 621–626.PubMedCrossRefGoogle Scholar
  14. Daub, M.E., Li, M., Bilski, P., and Chignell, C.F., 2000, Dihydrocercosporin singlet oxygen production and subcellular localization: a possible defense against cercosporin phototoxicity in Cercospora, Photochem. Photobiol. 71: 135–140.PubMedCrossRefGoogle Scholar
  15. de la Fuente-Martinez, J.M., and Herrera-Estrella, L., 1993, Strategies to design transgenic plants resistant to toxins produced by pathogens, AgBiotech News and Information 5: 595–599.Google Scholar
  16. 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, Biotechnology 10: 905–909.CrossRefGoogle Scholar
  17. deBlock, M., Brouwer, D. D., and Tenning, P., 1989, Transformation of Brassica napus and Brassica oleracea using Agrobaterium tumefaciens and the expression of bar and neo genes in the transgenic plants, Plant Physiol. 91: 694–701.CrossRefGoogle Scholar
  18. Deswarte, C., Canut, H., Klaebe, A., Roustan, J. P., and Fallot, J., 1996, Transport, cytoplasmic accumulation and mechanism of action of the toxin eutypine in Vitis vinifera cells, Arch. Biochem. Biophys. 149: 336–342.Google Scholar
  19. Dewey, R. E., Sledow, J.N., Timothy, D. H., and Levings III, C. S., 1988, A 13-kilodalton maize mitochondria! Protein in E. coli confers sensitivity to Bipolaris maydis toxin, Science 239: 293–295.Google Scholar
  20. Dickman, M. B. and Mitra, A., 1992, Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis, Physiol. Mol. Plant Pathol. 41: 255–263.Google Scholar
  21. Doumbou, C. L., Akimov, V., and Beaulieu, C., 1998, Selection and characterization of microorganisms utilizing Thaxotamin A, a phytotoxin produced by Streptomyces scabies, Appl. Environ. Microbial. 64: 4313–4316.Google Scholar
  22. Dunkle, L.D., Traylor, E.A., and Shore, S.H. 1987, Heat-shock protection of sorghum against effects of the host-specific toxin from Periconia circinata, in, Current Topics in Plant Biochemistry and Physiology: Proceedings of the Plant Biochemistry and Physiology Symposium held at the University of Missouri, Columbia, 1987, pp. 35–45.Google Scholar
  23. 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
  24. Earle, E.D., and Gracen, V.E., 1985, Somaclonal variation in progeny of plants from corn tissue cultures, in: Tissue Culture in Forestry and Agriculture, Randolph R. Henke… et al., eds., Basic Life Sciences 32: 139–152; Paper presented at the “Symposium on Plant Cell and Tissue Culture entitled Propagation of Higher Plants Through Plant Tissue Culture” Sept 9–13, 1984, Knoxville, Tennessee.Google Scholar
  25. Ehrenshaft, M., and Upchurch, R.G., 1993, Host-proteins induce accumulation of the toxin cercosporin and mRNA in a phytopathogenic strains of Cercospora kikuchii, Plant Physiol. 97: 1080–1086.Google Scholar
  26. Feys, B.J.F., Benedetti, C. E., Penfold, C.N., and Turner, J.G., 1994, Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen, Plant Cell 6: 751–759.PubMedGoogle Scholar
  27. Graniti, A., 1991, Phytotoxins and their involvement in plant diseases, Experientia 47: 751–755.CrossRefGoogle Scholar
  28. Haegi, A., and Porta-Puglia, A., 1995, Purification and partial characterization of a toxic compound produced by Pyrenophora graminea, Physiol. Mol. Plant Pathol. 46: 429–444.CrossRefGoogle Scholar
  29. Hatziloukas, E., and Panopoulos, N. J., 1992, Origin, structure, and regulation of argK, encoding the phaseolotoxinresistant ornithine carbamoyltransferase in Pseudomonas syringae pv. phaseolicola, and functional expression of argK in transgenic tobacco, J. Bacteriol. 174: 5895–5909.PubMedGoogle Scholar
  30. 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
  31. Johal, G.S., and Briggs, S. P., 1992, Reductase activity encoded by the Hml disease resistance gene in maize, Science 258: 985–987.PubMedCrossRefGoogle Scholar
  32. Kim, S. D., Knoche, H.W., and Dunkle, L.D., 1987, Essentiality of the ketone function for toxicity of the host- selective toxin produced by Helminthosporium carbonum, Physiol. Mol. Plant Pathol. 30: 433–440.CrossRefGoogle Scholar
  33. Kimura, M., Shingu, Y., Yoneyama, K., and Yamaguchi, I., 1998, Features of Tri101, the trichothecene 3–0acetyltransferase gene, related to the self-defense mechanism in Fusarium graminearum, Biosci. Biotechnol. Biochem. 62: 1033–1036.PubMedCrossRefGoogle Scholar
  34. Kneusel, R. E., Schultz, E., and Matern, U., 1994, Molecular characterization and cloning of an esterase which inactivates the macrolide toxin brefeldin A, J. BioL Chem. 269: 3449–3456.PubMedGoogle Scholar
  35. Meeley, R.B., and Walton, J. D., 1991, Enzymatic detoxification ofHC-toxin, the host-selective cyclic peptide from Cochliobolus carbonum, Plant Physiol 97: 1080–1086.PubMedCrossRefGoogle Scholar
  36. Meeley, R.B., Johan, G.S., Briggs, S. P., and Walton, J. D., 1992, A biochemical phenotype for a disease resistance gene of maize, Plant Cell: 71–77.Google Scholar
  37. Mitchell, R. E., 1976, Isolation and structure of a chlorosis inducing toxin ofPseudomonas syringae, Phytochemistry 15: 1941–1947.CrossRefGoogle Scholar
  38. 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
  39. Mitchell, R. F., and Bieleski, R.L., 1977, Involvement of phaseolotoxin in halo blight of beans. Transport and conversion of functional toxin, Plant Physiol. 60: 723–729.PubMedCrossRefGoogle Scholar
  40. Mosqueda, G., VandenBroek, 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 phaseolotoxin-insensitive ornithine carbamoyltransferase, Mol. Gen. Genet. 222: 461–466.PubMedCrossRefGoogle Scholar
  41. Multani, D.S., Meeley, R.B., Paterson, A.H., Gray, J., Briggs, S. P., and Johal, G.S., 1998, Plant-pathogen microevolution: Molecular basis for the origin of a fungal disease in maize, Proc. Natl. Acad. Sci. USA 95: 1686–1691.PubMedCrossRefGoogle Scholar
  42. Nelson, O.E., and Ullstrup, A.J., 1964, Resistance to leaf spot in maize, J. Heredity. 55: 195–199.Google Scholar
  43. Otani, H., Kohmoto, K., and Kodama, M. 1995, Alternaria toxins and their effects on host plants, Can. J. Bot. 73 (Suppl. 1): S453 - S458.CrossRefGoogle Scholar
  44. Ouchi, S., Toyoda, H., Utsumi, R., Hashimoto, H., and Hadama, T., 1989, A promising strategy for the control of fungal diseases by the use of toxin-degrading microbes, in: Phytotoxins and Plant Pathogenesis, A. Graniti, ed., Springer-Verlag, Berl in Heidelberg.Google Scholar
  45. Panopoulos, N. J., and Peet, R.C., 1985, The molecular genetics of plant pathogenic bacteria and their plasmids, Annu. Rev. Phytopathol. 23: 381–419.CrossRefGoogle Scholar
  46. Panopoulos, N. J., Walton, J. D., Wills, D.K., 1984, Genetic and biochemical basis of virulence in plant pathogens, in: Genes Involved in Microbe-Plant Interactions, D.P.S. Verma and T.J. Hohn, eds., Springer-Verlag, Vienna, Austria.Google Scholar
  47. Patil, S. S., Kolattukody, 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
  48. Ransom, R.F., Wilder, J., and Dunkle, L.D., 1994, Purification and distribution ofpathotoxin enhanced proteins in sorghum, Physiol. Mol. Plant Pathol. 45: 385–395.CrossRefGoogle Scholar
  49. Sanford, J.C., and Johnston, S.A., 1985, The concept of parasite derived resistance-deriving resistance genes from the parasite’s own genome, J. Theor. Biol. 113: 395–405.CrossRefGoogle Scholar
  50. Sawada, H., Takeuchi, T., and Matsuda, I., 1997, Comparative analysis of Pseudomonas syringae pv. actinidiae and pv. phaseolicola based on phaseolotoxin-resistant or ornithine carbamoyltransferase gene (argK) and 16S–23S rRNA intergenic spacer sequences, Appl. Environ. Microbiol. 63: 282–288.PubMedGoogle Scholar
  51. Scheffer, R,P., and Ullstrup, A.J., 1965, A host specific toxic metabolite from Helminthosporium carbonum, Phytopathology 55: 1037–1038.Google Scholar
  52. Scheffer, R.P., Nelson, R.R., and Ullstrup, A.J., 1967, Inheritance of toxin production and pathogenicity in Cochliobolus cautonum and Cochliobolus victoriae, Phytopathology 57: 1288–1291.Google Scholar
  53. Shanmugam, V., Sriram, S., Babu, S., Nandakumar, R., Raguchander, T., Balasubramanian, P., and Samiyappan, R., 2001, Purification and characterization of an extracellular alpha-glucosidase protein from Trichoderma viride which degrades a phytotoxin associated with sheath blight disease in rice, J Appt. Microbiol. 90: (Accepted)Google Scholar
  54. Sinden, S.L., and Durbin, R.D., 1968, Glutamine synthetase inhibition: Possible mode of action of wild fire toxin from Pseudomonas tabaci, Nature 219: 379–380.PubMedCrossRefGoogle Scholar
  55. Song, H.S., Lim, S.M., and Clark, J.M., Jr., 1993, Purification ana partial characterization of a host-specific pathotoxin from culture filtrates of Septoriaglycines, Phytopathology 83: 659–661.CrossRefGoogle Scholar
  56. Sriram, S., 1997, Degradation of Rhizoctonia toxin and its consequences on sheath blight disease and defenserelated proteins in rice, Ph.D thesis, Tamil Nadu Agricultural University, Coimbatore, India.Google Scholar
  57. Sriram, S., Raguchander, T., Babu, S., Nandakumar, R., Shanmugam, V., Balasubramanian, P., Muthukrishnan, S., and Samiyappan, R., 2000, Inactivation of phytotoxin produced by Rhizoctonia solani, the rice sheath blight pathogen, Can. J Microbiol. 46: 520–524.PubMedGoogle Scholar
  58. Stalker, D.M., McBride, K.E., and Malyi, L.D. 1988. Expression in plants of a bromoxynil-specific bacterial nitrilase that confers herbicide resistance, in: Genetic Improvements of Agriculturally Important Crops: Progress and Issues, R. T. Fraley, N.M. Frey, and J. Schell. eds., Current communications in molecular biology, pp. 37–39.Google Scholar
  59. Staskawicz, B.J., Panopoulos, N.J., and Hoogenraad, N.J., 1980, Phytotoxin insensitive ornithine carbamoyl transferase of Pseudomonas syringae pv. phaseoloicola, Basis for immunity to phaseolotoxin, J. Bacteriol. 142: 720–723.PubMedGoogle Scholar
  60. Streber, W.R., and Willmitzer, L. 1989, Transgenic tobacco plants expressing a bacterial detoxifying enzyme are resistant to 2,4-D, Bio/technology 7: 811–816.CrossRefGoogle Scholar
  61. Taylor, P.A., Schnoes, H.K., and Durbin, R.D., 1972, Characterization of chlorosis—inducing toxins from a plant pathogenic Pseudomonas sp, Biochem. Biophys. Acta. 286: 107–117.PubMedCrossRefGoogle Scholar
  62. Tey-Rulh, P., Philippe, I., Renaud, J.M., Tsoupras, G., De Angelis, P., Roustan, J.P., Fallot, J., and Tabacchi, R., 1991, Eutypine, a phytotoxin produced by Eutypa lata, the causal agent of dying-arm disease of grapevine, Phytochemistry 30: 471–473.CrossRefGoogle Scholar
  63. Toyoda, H., Hashimoto, H., Utsumi, R., Kobayashi, H., and Ouchi, S., 1988, Detoxification of fusaric acid by a fusaric acid-resistant mutant of P. solanacearum and its application to biological control of Fusarium wilt of tomato, Phytopathology 78: 1307–1311.CrossRefGoogle Scholar
  64. Toyoda, H., Katsuragi, K., Tamari, T., and Ouchi, S., 1991, DNA sequence of genes for detoxification of fusaric acid a wilt-inducing agent produced by Fusarium spp., J. Phytopathology 133: 265–277.CrossRefGoogle Scholar
  65. Utsumi, R., Hadama, T., Noda, M., Toyoda, H., Hashimoto, H., and Ohuchi, S., 1988, Cloning of fusaric acid-detoxifying gene from Cladosporium werneckii: a new strategy for the prevention of plant diseases, J. Biotechnol 8: 311–316.CrossRefGoogle Scholar
  66. Vidhyasekaran, P., 1993, Principles of Plant Pathology, CBS Publishers, New Delhi, India.Google Scholar
  67. Vidhyasekaran, P., 1997, Fungal Pathogenesis in Plants and Crops: Molecular Biology and Host Defense Mechanisms, Marcel Dekker, Inc, New York.Google Scholar
  68. Vidhyasekaran, P., Borromeo, E.S., and Mew, T.W., 1986, Host-specific toxin production by Helminthosporium oryzae, Phytopathology 76: 261–266.CrossRefGoogle Scholar
  69. Vidhyasekaran, P., Borromeo, E.S., and Mew, T.W., 1992, Helminthosporium oryzae toxin suppresses phenol metabolism in rice plants and aids pathogen colonization, Physiol. Mol. Plant Pathol. 41: 307–315.Google Scholar
  70. Vidhyasekaran, P., RubyPonmalar, T., Samiyappan, R., Velazhahan, R., Vimala, R., Ramanathan, A., Paranidharan, V., and Muthukrishnan, S., 1997, Host-specific toxin production by Rhizoctonia solani, the rice sheath blight pathogen, Phytopathology 87: 1258–1263.PubMedCrossRefGoogle Scholar
  71. Walton, J.D., and Earle, E.D., 1983, The episode in HC-toxin is required for activity against susceptible maize, Physiol. Plant Pathol. 22: 371–376.Google Scholar
  72. Watanabe, T., Sekizawa, Y., Shimura, M., Suzuki, Y., Matsumoto, K., Iwata, M., and Mase, S., 1979, Effects of probenazole (Oryzemate) on rice plants with reference to controlling rice blast, J. Pestic. Sci. 4: 53–59.CrossRefGoogle Scholar
  73. Wenzel, G. 1990, Progeny tests of barley, wheat, and potato regenerated from cell cultures after in vitro selection for disease resistance, Theor. Appl. Genet. 80: 359–365.CrossRefGoogle Scholar
  74. Wise, R.P., Fliss, A.E., Pring, D.R., and Gengenbach, B.G., 1987, Urf 13-T of T cytoplasm maize mitochondria encodes a 13 kDa polypeptide, Plant Mol. Biol. 9: 121–126.CrossRefGoogle Scholar
  75. Woloshuk, C.P., Sisler, H.D., Tokousbalides, M.R., and Dutky, S.R., 1980, Melanin biosynthesis in Pyricularia oryzae: site of tricyclazole inhibition and pathogenicity of melanin-deficient mutants, Pestic. Biochem. Physiol. 14: 256–264.CrossRefGoogle Scholar
  76. Wolpert, T.J., Navarie, D.A., Lorang, I., and Moore, D.L., 1995, Molecular interactions of victorin and oat, Can. J. Bot. 73: 475–482.CrossRefGoogle Scholar
  77. Xie, D.-X., Feys, B.F., James, S., Nieto-Rostro, M., and Turner, J.G., 1998, COIL: an Arabidopsis gene required for jasmonate-regulated defence and fertility, Science 280: 1091–1094.Google Scholar
  78. Yamaguchi, I., Sekido, S., and Misato, T., 1983, Inhibition of appressorial melanization in Pyricularia oryzae by non-fungicidal anti-blast chemicals J. Pestic.Sci. 8: 229–232.CrossRefGoogle Scholar
  79. Yoder, O.C., 1980, Toxin in pathogenesis, Annu. Rev. Phytopathol. 18: 103–129.CrossRefGoogle Scholar
  80. Yoneyama, K., and Anzai, H., 1993, Transgenic plants resistant to diseases by the detoxification of toxins, in: Biotechnology in Plant Disease Control, 1. Chet, ed., Wiley-Liss Inc., New York.Google Scholar
  81. Zhang, L., Xu, J., and Birch, R.G., 1998, High affinity binding of albicidin phytotoxins by the AlbA protein from Klebsiella oxytoca, Microbiology 144: 555–559.PubMedCrossRefGoogle Scholar
  82. Zhang, L., Xu, J., and Birch, R.G., 1999, Engineered detoxification confers resistance against a pathogenic bacterium, Nature Biotechnology 17: 1021–1024.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • P. Balasubramanian
    • 1
  • R. Samiyappan
    • 1
  • S. Babu
    • 1
  • R. Nandakumar
    • 1
  • V. Shanmugam
    • 1
  • T. Raguchander
    • 1
  1. 1.Department of Plant PathologyTamil Nadu Agricultural UniversityCoimbatoreIndia

Personalised recommendations