Structure and Expression of Plant Genes Encoding Pathogenesis-Related Proteins

  • John F. Bol
Part of the Plant Gene Research book series (GENE)


In the early seventies Van Loon and Van Kammen (1970) and Gianinazzi et al (1970) independently reported the de novo synthesis of four proteins in tobacco plants reacting hypersensitively to infection with tobacco mosaic virus (TMV). Later on, six additional components specific to TMVinfected tobacco were identified (Pierpoint et al, 1981; Van Loon, 1982). Initially, these proteins were called “new components” or “b-proteins”. The name “pathogenesis-related” proteins, or PRs, was proposed by Antoniw et al (1980) to permit the grouping of similar proteins from different tobacco cultivars. The ten PR proteins induced by TMV-infection of the Nicotiana tabacum cultivars Samsun NN and Xanthi nc have been characterized in most detail. These are designated 1 a (IV, b 1), lb (III, b2), 1c (II, b3), 2 (I, b4), N (b5), O (b6), P (b7), Q (b8), R (b9) and S in order of decreasing mobility in alkaline, non-denaturing gels (the notation given between parentheses is no longer commonly used). Proteins similar to one or more of these PRs have been detected in other Nicotiana species such as N. debneyi, N. glutinosa, N. rustica, N. sylvestris and N. tomentosiformis (Ahl and Gianinazzi, 1982; Ahl et al., 1982).


Salicylic Acid Tobacco Mosaic Virus Plant Pathol Polyacrylic Acid Tobacco Mosaic Virus Infection 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahl, P., Benjama, A., Samson, R., Gianninazzi, S., 1981: Induction chez le tabac par Pseudomonas syringae de nouvelles protéines (protéines b) associées au développement d’une résistance non spécifique à une deuxième infection. Phyto-path. Z. 102, 201–212.Google Scholar
  2. Ahl, P., Gianninazzi, S., 1982: b-Protein as a constitutive component in highly (TMV) resistant interspecific hybrids of Nicotiana glutinosa × Nicotiana debneyi. Plant Sci. Lett. 26, 173–181.CrossRefGoogle Scholar
  3. Ahl, P., Cornu, A., Gianninazzi, S., 1982: Soluble proteins as genetic markers in studies of resistance and phylogeny in Nicotiana. Phytopathology 72, 80–85.CrossRefGoogle Scholar
  4. Antoniw, J. F., Pierpoint, W. S., 1978: The purification and properties of one of the “b” proteins from virus-infected tobacco plants. J. Gen. Virol. 39, 343–350.CrossRefGoogle Scholar
  5. Antoniw, J. F., White, R. F., 1980: The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopathol. Z. 98, 331–341.CrossRefGoogle Scholar
  6. Antoniw, J. F., Ritter, C. E., Pierpoint, W. S., Van Loon, L. C., 1980: Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. J. Gen. Virol. 47, 79–87.CrossRefGoogle Scholar
  7. Antoniw, J. F., White, R. F., 1983: Biochemical properties of the pathogenesis-related proteins from tobacco. Neth. J. Plant Pathol. 89, 255–264.CrossRefGoogle Scholar
  8. Antoniw, J. F., White, R. F., Barbara, D. J., Jones, P., Longley, A., 1985: The detection of PR (b) protein and TMV by ELISA in systemic and localized virus infections of tobacco. Plant Mol. Biol. 4, 55–60.CrossRefGoogle Scholar
  9. Antoniw, J. F., White, R. F., 1986: Changes with time in the distribution of virus and PR protein around single local lesions of TMV infected tobacco. Plant Mol. Biol. 6, 145–149.CrossRefGoogle Scholar
  10. Asselin, A., Grenier, J., Cote, F., 1985: Light-influenced extra cellular accumulation of b (pathogenesis-related) proteins in Nicotiana green tissue induced by various chemicals or prolonged floating on water. Can. J. Bot. 63, 1276–1283.CrossRefGoogle Scholar
  11. Bol, J. F., Hooft van Huijsduijnen, R. A. M., Cornelissen, B. J. C., Van Kan, J. A. L., 1987: Characterization of pathogenesis-related (PR) proteins and genes. In: Plant resistance to viruses. Evered, D., Harnett, S., Eds. J. Wiley and Sons Ltd., Chichester, p. 72–80.Google Scholar
  12. Boller, T., Gehri, A., Mauch, F., Vogeli, U., 1983: Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157, 22–31.CrossRefGoogle Scholar
  13. Broglie, K. E., Gaynor, J. J., Broglie, R. M., 1986: Ethylene-regulated gene expression: molecular cloning of the genes encoding an endochitinase from Phaseolus vulgaris. Proc. Natl. Acad. Sci. U.S.A. 83, 6820–6824.PubMedCrossRefGoogle Scholar
  14. Camacho Henriquez, A., Sanger, H. L., 1984: Purification and partial characterization of the major “pathogenesis-related” tomato leaf protein pl4 from potato spindle tuber viroid (PSTV)-infected tomato leaves. Arch. Virol. 81, 263–284.PubMedCrossRefGoogle Scholar
  15. Carr, J. P., Antoniw, J. F., White, R. F., Wilson, T. M. A., 1982: Latent messenger RNA in tobacco (Nicotiana tabacum). Biochem. Soc. Trans. 10, 353–354.Google Scholar
  16. Carr, J. P., Dixon, D. C., Klessig, D. F., 1985: Synthesis of pathogenesis-related proteins in tobacco is regulated at the level of mRNA accumulation and occurs on membrane-bound polysomes. Proc. Natl. Acad. Sci. U. S.A. 82, 7999–8003.PubMedCrossRefGoogle Scholar
  17. Carr, J. P., Dixon, D. C., Nikolau, B. J., Voelkerding, K. V., Klessig, D. F., 1987: Synthesis and localization of pathogenesis-related proteins in tobacco. Mol. Cell. Biol. 7, 1580–1583.PubMedGoogle Scholar
  18. Cornelissen, B. J. C., Hooft van Huijsduijnen, R. A. M., Van Loon, L. C., Bol, J. F., 1986 a: Molecular characterization of the messenger RNAs for “pathogenesis-related” proteins 1a, 1b and 1c, induced by TMV infection of tobacco. EMBO J. 5, 37–40.PubMedGoogle Scholar
  19. Cornelissen, B. J. C., Hooft van Huijsduijnen, R. A. M., Bol, J. F., 1986 b: A tobacco mosaic virus-induced tobacco protein is homologous to the sweet-tasting protein thaumatin. Nature 321, 531–532.PubMedCrossRefGoogle Scholar
  20. Cornelissen, B. J. C., Horowitz, J., Van Kan, J. A. L., Goldberg, R. B., Bol, J. F., 1987: Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucleic Acids Res. 15, 6799–6811.PubMedCrossRefGoogle Scholar
  21. De Wit, P. J. G. M., Buurlage, M. B., 1986: The occurrence of host-, pathogen-and interaction-specific proteins in the apoplast of Cladosporium fulvum (syn.fulvia Fulva) infected tomato leaves. Physiol. Mol. Plant Pathol. 29, 159–172.CrossRefGoogle Scholar
  22. Dumas, E., Gianninazzi, S., Cornu, A., 1987: Genetic aspects of polyacrylic acid induced resistance to tobacco mosaic virus and tobacco necrosis virus in Nicotiana plants. Plant Pathol., in press.Google Scholar
  23. Fincher, G. B., Lock, P. A., Morgan, M. M., Lingelbach, K., Wettenhall, R. E. H., Mercer, J. F. B., Brandt, A., Thomsen, K. K., 1986: Primary structure of the (1,3–1,4)-β-D-glucan 4-glucohydrolase from barley aleurone. Proc. Natl. Acad. Sci. U.S.A. 83, 2081–2085.PubMedCrossRefGoogle Scholar
  24. Fortin, M. G., Parent, J. G., Asselin, A., 1985: Comparative study of two groups of b proteins (pathogenesis-related) from the intercellular fluid of Nicotiana leaf tissue infected by tobacco mosaic virus. Can. J. Bot. 63, 932–937.Google Scholar
  25. Fraser, R. S. S., 1981: Evidence for the occurrence of the “pathogenesis-related” proteins in leaves of healthy tobacco plants during flowering. Physiol. Plant Pathol. 19, 69–76.Google Scholar
  26. Fraser, R. S. S., 1982: Are “pathogenesis-related” proteins involved in acquired systemic resistance of tobacco mosaic virus? J. Gen. Virol. 58, 305–313.CrossRefGoogle Scholar
  27. Fraser, R. S. S., Clay, C. M., 1983: Pathogenesis-related proteins and acquired systemic resistance: causal relationship or separate effects? Neth. J. Plant. Pathol. 89, 283–292.CrossRefGoogle Scholar
  28. Gianinazzi, S., Martin, C., Vallee, J. C., 1970: FrHypersensibilite aux virus, temperatures et proteines solubles chez le Nicotiana Xanthinc. Apparition de nouvelles macromolecules lors de la repression de la synthese virale. C. R. Acad. Sci. Paris D. 270, 2383–2386.Google Scholar
  29. Gianinazzi, S., Kassanis, B., 1974: Virus resistance induced in plants by polyacrylic acid. J. Gen. Virol. 23, 1–9.CrossRefGoogle Scholar
  30. Gianinazzi, S., Prat, H. M., Shewry, P. R., Miflin, B. J., 1977: Partial purification and preliminary characterization of soluble proteins specific to virus infected tobacco plants. J. Gen. Virol. 34, 345–351.CrossRefGoogle Scholar
  31. Gianinazzi, S., Ahl., P., Cornu, A., Scalla, R., Cassini, R., 1980: First report of host b-protein appearance in response to a fungal infection in tobacco. Physiol. Plant Pathol. 16, 337–342.Google Scholar
  32. Gianinazzi, S., 1983: Genetic and molecular aspects of resistance induced by infections or chemicals. In: Plant-Microbe Interactions Molecular and Genetic Perspectives. Nester, E. W., Kosuge, T. Eds., Macmillan Publ. Co., New York, vol. 1, 321–342.Google Scholar
  33. Gianinazzi, S., Ahl., P., 1983: The genetic and molecular basis of b-proteins in the genus Nicotiana. Neth. J. Plant Pathol. 89, 275–281.CrossRefGoogle Scholar
  34. Hooft van Huijsduijnen, R. A. M., Cornelissen, B. J. C., Van Loon, L. C., Van Boom, J. H., Tromp, M., Bol, J. F., 1985: Virus-induced synthesis of pathogenesis-related proteins in tobacco. EMBO J. 4, 2167–2171.PubMedGoogle Scholar
  35. Hooft van Huijsduijnen, R. A. M., Van Loon, L. C., Bol, J. F., 1986 b: cDNA cloning of six mRNAs induced by TMV infection of tobacco and a characterization of their translation products. EMBO J. 5, 2057–2061.PubMedGoogle Scholar
  36. Hooft van Huijsduijnen, R. A. M., Alblas, S. W., De Rijk, R. H., Bol, J. F., 1986 b: Induction by salicylic acid of pathogenesis-related proteins and resistance to alfalfa mosaic virus infection in various plant species. J. Gen. Virol. 67, 2135–2143.CrossRefGoogle Scholar
  37. Hooft van Huijsduijnen, R. A. M., Kauffmann, S., Brederode, F. Th., Cornelissen, B. J. C., Legrand, M., Fritig, B., Bol, J. F., 1987: Homology between chitinases that are induced by TMV infection of tobacco. Plant Mol. Biol. 9, 411–420.CrossRefGoogle Scholar
  38. Jamet, E., 1985: Modification de la synthèse protéique chez des plantes hypersensibles à une infection virale: étude plus particulière des protéines PR (“pathogenesis-related”) du tabac. Ph. D. Thesis, University Louis Pasteur, Strasbourg.Google Scholar
  39. Jamet, E., Fritig, B., 1986: Purification and characterization of 8 of the pathogenesis-related proteins in tobacco leaves reacting hypersensitively to tobacco mosaic virus. Plant Mol. Biol. 6, 69–80.CrossRefGoogle Scholar
  40. Kassanis, B., Gianinazzi, S., White, R. F., 1974: A possible explanation for the resistance of virus-infected tobacco plants to second infection. J. Gen. Virol. 23, 11–16.CrossRefGoogle Scholar
  41. Leach, J. E., Sherwood, J., Fulton, R. W., Sequira, L., 1983: Comparison of soluble proteins associated with disease resistance induced by bacterial lipopolysac-charide and by viral necrosis. Physiol. Plant Pathol. 23, 377–385.CrossRefGoogle Scholar
  42. Legrand, M., Kauffmann, S., Geoffroy, P., Fritig, B., 1987: Biological function of “pathogenesis-related” proteins: four tobacco PR-proteins are chitinases. Proc. Natl. Acad. Sci. U.S.A. 84, 6750–6754.PubMedCrossRefGoogle Scholar
  43. Lucas, J., Camacho Henriquez, A., Lottspeich, F., Henschen, A., Sanger, H. L., 1985: Amino acid sequence of the “pathogenesis-related” leaf protein p14 from viroid-infected tomato reveals a new type of structurally unfamiliar proteins. EMBO J. 4, 2745–2749.PubMedGoogle Scholar
  44. Maiss, E., Poehling, H. M., 1983: Resistance against plant viruses induced by culture filtrates of the fungus Stachybotrys chartarum. Neth. J. Plant Pathol. 89, p. 323.CrossRefGoogle Scholar
  45. Matsuoka, M., Ohashi, Y., 1984: Biochemical and serological studies of pathogenesis-related proteins of Nicotiana species. J. Gen. Virol. 65, 2209–2215.CrossRefGoogle Scholar
  46. Moore, A. E., Stone, B. A., 1972: Effect of infection with TMV and other viruses on the level of a β-1, 3-glucan hydrolase in leaves of Nicotiana glutinosa. Virology 50, 791–798.PubMedCrossRefGoogle Scholar
  47. Nassuth, A., Sanger, H. L., 1986: Immunological relationship between “pathogenesis-related” leaf proteins from tomato, tobacco and cowpea. Virus Research 4, 229–242.CrossRefGoogle Scholar
  48. Parent, J. G., Asselin, A., 1984: Detection of pathogenesis-related proteins (PR or b) and of other proteins in the intercellular fluid of hypersensitive plants infected with tobacco mosaic virus. Can. J. Bot. 62, 564–569.CrossRefGoogle Scholar
  49. Pfitzner, U. M., Goodman, H. M., 1987: Isolation and characterization of cDNA clones encoding pathogenesis-related proteins from tobacco mosaic virus infected tobacco plants. Nucleic Acids Res. 15, 4449–4465.PubMedCrossRefGoogle Scholar
  50. Pierpoint, W. S., Robinson, N. P., Leason, M. B., 1981: The pathogenesis-related proteins of tobacco: their induction by viruses in intact plants and their induction by chemicals in detached leaves. Physiol. Plant Pathol. 19, 85–97.Google Scholar
  51. Pierpoint, W. S., 1986: The pathogenesis-related proteins of tobacco leaves. Phyto-chemistry 25, 1595–1601.Google Scholar
  52. Pierpoint, W. S., Tatham, A. S., Pappin, D. J. C., 1987: Identification of the virus-induced protein of tobacco leaves that resembles the sweet-protein thaumatin. Physiol. Mol. Plant Pathol., in press.Google Scholar
  53. Redolfi, P., 1983: Occurrence of pathogenesis-related (b) and similar proteins in different plant species. Neth. J. Plant Pathol. 89, 245–254.CrossRefGoogle Scholar
  54. Richardson, M., Valdes-Rodriguez, S., Blanci-Labra, A., 1987: A possible function for thaumatin and a TMV-induced protein suggested by homology to a maize inhibitor. Nature 327, 432–434.CrossRefGoogle Scholar
  55. Riggleman, R. C., Fristensky, B., Hadwiger, L. A., 1985: The disease resistance response in pea is associated with increased levels of specific mRNAs. Plant Mol. Biol. 4, 81–86.CrossRefGoogle Scholar
  56. Ross, A. F., 1961: Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340–358.PubMedCrossRefGoogle Scholar
  57. Ross, A. F., 1966: Systemic effects of local lesion formation. In: Viruses of Plants, Beemster, A. B. R., Dijkstra, J. Eds., North Holland Publ. Co., Amsterdam, pp. 127–150.Google Scholar
  58. Schlumbaum, A., Mauch, F., Vogli, U., Boiler, T., 1986: Plant chitinases are potent inhibitors of fungal growth. Nature 324, 365–367.CrossRefGoogle Scholar
  59. Sherwood, J. L., 1985: The association of (pathogenesis-related) proteins with viral-induced necrosis in Nicotiana sylvestris. Phytopathol. Z. 112, 48–55.CrossRefGoogle Scholar
  60. Shinshi, H., Mohnen, D., Meins, F., 1987: Regulation of a plant pathogenesis-related enzyme: inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc. Natl. Acad. Sci. U.S.A. 84, 89–93.PubMedCrossRefGoogle Scholar
  61. Somsich, I. E., Schmelzer, E., Bollman, J., Hahlbrock, K., 1986: Rapid activation by fungal elicitor of genes encoding “pathogenesis-related” proteins in cultured parsley cells. Proc. Natl. Acad. Sci. U.S.A. 83, 2427–2430.CrossRefGoogle Scholar
  62. Van Loon, L. C., Van Kammen, A., 1970: Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var “Samsun” and “Samsun NN”. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 40, 199–211.CrossRefGoogle Scholar
  63. Van Loon, L. C., 1975: Similarity of qualitative changes of specific proteins after infection with different viruses and their relationship to acquired resistance. Virology 67, 566–575.CrossRefGoogle Scholar
  64. Van Loon, L. C., 1976: Specific soluble leaf proteins in virus-infected tobacco plants are not normal constituents. J. Gen. Virol. 30, 375–379.CrossRefGoogle Scholar
  65. Van Loon, L. C., 1977: Induction by 2-chloroethylphosphonic acid of viral-like lesions, associated proteins, and systemic resistance in tobacco. Virology 80, 417–420.PubMedCrossRefGoogle Scholar
  66. Van Loon, L. C., 1982: Regulation of changes in proteins and enzymes associated with active defence against virus infection. In: Wood, R. K. S., Ed., Active defense mechanisms in plants. Plenum Press, New York, pp. 247–273.Google Scholar
  67. Van Loon, L. C., Antoniw, J. F., 1982: Comparison of the effects of salicylic acid and ethephon with virus-induced hypersensitivity and acquired resistance in tobacco. Neth. J. Plant Pathol. 88, 237–256.CrossRefGoogle Scholar
  68. Van Loon, L. C., 1983: The induction of pathogenesis-related proteins by pathogens and specific chemicals. Neth. J. Plant Pathol. 89, 265–273.CrossRefGoogle Scholar
  69. Van Loon, L. C., 1985: Pathogenesis-related proteins. Plant Mol. Biol. 4, 111–116.CrossRefGoogle Scholar
  70. Varner, J. E., Cassab, G. I., 1986: A new protein in petunia. Nature 323, p. 110.CrossRefGoogle Scholar
  71. Wagih, E. E., Coutts, R. H. A., 1982: Comparison of virus-elicited and other stresses on the soluble protein fraction of cucumber cotyledons. Phytopathol. Z. 104, 364–374.CrossRefGoogle Scholar
  72. White, R. F., 1979: Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99, 410–412.PubMedCrossRefGoogle Scholar
  73. White, R. F., 1983: Serological detection of pathogenesis-related proteins. Neth. J. Plant Pathol. 89, p. 311.CrossRefGoogle Scholar
  74. White, R. F., Antoniw, J. F., Carr, J. P., Woods, R. D., 1983: The effects of aspirin and polyacrylic acid on the multiplication and spread of TMV in different cultivars of tobacco with and without the N-gene. Phytopath. Z. 107, 224–232.CrossRefGoogle Scholar
  75. White, R. F., Dumas, E., Shaw, P., Antoniw, J. F., 1986: The chemical induction of PR (b) proteins and resistance to TMV infection in tobacco. Antiviral Research 6, 177–185.PubMedCrossRefGoogle Scholar
  76. White, R. F., Rybicki, E. P., Von Wechmar, M. B., Dekker, J. L., Antoniw, J F., 1987: Detection of PR1 type proteins in Amaranthaceae, Chenopodiaceae, Gram-ineae and Solanaceaeby immunoelectroblotting. J. Gen. Virol. 68, 2043–2048.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag/Wien 1988

Authors and Affiliations

  • John F. Bol
    • 1
  1. 1.Department of BiochemistryLeiden UniversityAL LeidenThe Netherlands

Personalised recommendations