Skip to main content
Log in

Host recognition by toxigenic plant pathogens

  • Multi-author Review
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

Certain fungal pathogens release host-selective (or host-specific) toxins (HST) as a host recognition factor during spore germination at the infection site on plants. Prior to penetration of the pathogen into its host, the released toxin specifically binds to a putative receptor on the host cells and initiates signaling mechanisms leading to pleiotropic effects on cells. Of these, the crucial one negates the general and inducible defense reactions of the cells. This is accomplished by a signal from the HSt, which is transduced through a path way at or near the step of plasma membrane modulation, which is directly or indirectly triggered by the HST. This mechanism operates even though the toxin may affect mitochondria or chloroplasts as the primary target organelle. The fungal spore is able to penetrate the so-called ‘narcotized cell’ and completes the initial colonization of the host. The host recognition process may take place without necessitating host cell death, even in the case of perthophytic parasites. At the molecular level, HST-mediated recognition of the host by a pathogen requires strict stereochemical precision like a lock and key.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Akimitsu, K., Kohmoto, K., Otani, H., and Nishimura, S., Hostspecific effects of toxin from the rough lemon pathotype ofAlternaria alternata on mitochondria. Plant Physiol.89 (1989) 925–931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Braun C. J., Siedow, J. N., and Levings III, C. S., The T-urf t3 gene is responsible for toxin sensitivity in maize andE. coli, in: The Molecular Basis of Plant Development, New Series, vol. 92, pp. 79–85. Ed. R. Goldberg, Alan R. Liss, New York 1989.

    Google Scholar 

  3. Braun, C. J., Siedow, J. N., and Levings III, C. S., Fungal toxins bind to the URF13 protein in maize mitochondria andEscherichia coli. Plant Cell2 (1990) 153–161.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Braun, C. J., Siedow, J. N., Williams, M. E., and Levings III, C. S., Mutations in the maize mitochondrial T-urft3 gene eliminate sensitivity to a fungal pathotoxin. Proc. natl. Acad. Sci. USA86 (1989) 4435–4439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Crombie, L., and Jarrett, S. R. M., Synthesis of the host-selective plant toxins AF IIa, AF IIc and AK II employing sharpless chiral epoxidation under kinetic control. Tetrahedron Lett.30 (1989) 4303–4306.

    Article  CAS  Google Scholar 

  6. Crombie, L., Horsham, M. A., and Jarrett, S. R. M., Synthesis of the (2E,4Z,6E)-and (2E,4E,6Z)-tetraenol stems of the host-selective AK and AF toxins by hydrometallation. Tetrahedron Lett.30 (1989) 4299–4302.

    Article  CAS  Google Scholar 

  7. Daly, J. M., Mechanisms of action, in: Toxins in Plant Disease, pp. 331–394. Ed. R. D. Durbin. Academic Press, New York 1981.

    Chapter  Google Scholar 

  8. Daly, J. M., The role of recognition in plant disease. A. Rev. Phytopath.22, (1984), 273–307.

    Article  CAS  Google Scholar 

  9. Danko, S. J., Kono, Y., Daly, J. M., Suzuki, Y., Takeuchi, S., and McCrey, D. A., Structure and biological activity of a host-specific toxin produced by the fungal corn pathogenPhyllosticta maydis. Biochemistry23 (1984) 759–766.

    Article  CAS  Google Scholar 

  10. Dewey, R. E., Siedow, J. N., Timothy, C. S., and Levings III, C. S., A 13-kilodalton maize mitochondrial protein inE. coli confers sensitivity toBipolaris maydis toxin. Science239 (1988) 293–295.

    Article  CAS  PubMed  Google Scholar 

  11. Frantzen, K. A., Daly, J. M., and Knoche, H. W., The binding of host-selective toxin analogs to mitochondria from normal and ‘Texas’ male sterile cytoplasm maize. Plant Physiol.83 (1987) 863–868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gardner, J. M., Kono, Y., Tatum, J. H., Suzuki, Y., and Takeuchi, S., Structure of the major component of ACRL-toxins, host-specific pathotoxic compounds produced byAlternaria citri. Agric. Biol. Chem.49 (1985) 1235–1238.

    CAS  Google Scholar 

  13. Gilchrist, D. G., Molecular mode of action, in: Toxins and Plant Pathogenesis, pp. 81–136. Eds J. M. Daly and B. J. Deverall. Academic Press, Sydney, Australia 1983.

    Google Scholar 

  14. Graniti, A., Durbin, R. D., and Ballio, A. (Eds) Phytotoxins and Plant Pathogenesis. Springer-Verlag, Berlin 1989.

    Google Scholar 

  15. Hayami, C., Otani, H., Nishimura, S., and Kohmoto, K., Induced resistance in pear leaves by spore germination fluids of nonpathogens toAlternaria alternata, Japanese pear pathotype and suppression of the induction by AK-toxin. J. Fac. Agric. Tottori Univ.17 (1982) 9–18.

    Google Scholar 

  16. Heath, M. C., A generalized concept of host-parasite specificity. Phytopathology71 (1981) 1121–1123.

    Article  Google Scholar 

  17. Holden, M. J., and Sze, H., Dissipation of the membrane potential in susceptible corn mitochondria by the toxin ofHelminthosporium maydis, race T, and toxin analogs. Plant Physiol.84 (1987) 670–676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Holden, M. J., and Sze, H., Effects ofHelminthosporium maydis race T toxin on electron transport in susceptible corn mitochondria and prevention of toxin actions by dicyclohexylcarbodiimide. Plant Physiol.91 (1989) 1296–1302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Huang, J., Lee, S.-H., Lin, C., Medici, R., Hack, E., and Myers, A. M., Expression in yeast of the T-URF13 protein from Texas malesterile maize mitochondria confers sensitivity to methomyl and to Texas-cytoplasm-specific fungal toxins. EMBO J.9 (1990) 339–347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Irie, H., Igarashi, J., Matsumoto, K., Yanagawa, Y., Nakashima, T., Ueno, T., and Fukami, H., An approach to a synthesis of the hostspecific toxins AK-toxin I and II, starting from vitamin C as a chiral. Chem. pharm. Bull.33 (1985) 1313–1315.

    Article  CAS  Google Scholar 

  21. Itoh, Y., Kohmoto, K., Otani, H., Kodama, M., Nishimura, S., Nakatsuka, S., and Goto, T., Isolation and biological activities of host-specific toxins, ACT-toxins produced by the tangerine pathotype ofAlternaria alternata. Ann. phytopath. Soc. Japan.55 (1989) 482.

    Google Scholar 

  22. Kato, T., Yamada, M., and Ueno, T., Synthesis of enantio AM-toxin I. Agric. Biol. Chem.51 (1987) 1707–1709.

    Google Scholar 

  23. Kohmoto, K., Recent advances in studies of host-specific toxins —with special reference toAlternaria toxins. Korean J. Plant Path.3 (1987) 43–53.

    Google Scholar 

  24. Kohmoto, K., and Durbin, R. D. (Eds), Host-Specific Toxins: Recognition and Specificity Factors in Plant Disease. Tottori Univ. Press, Tottori 1989.

    Google Scholar 

  25. Kohmoto, K., Otani, H., and Nishimura, S., Primary action sites for host-specific toxins produced byAlternaria species, in: Molecular Determinants of Plant Diseases, pp. 127–143. Eds S. Nishimura, C. P. Vance and N. Doke. Japan Sci. Soc. Press/Springer-Verlag, Tokyo 1987.

    Google Scholar 

  26. Kohmoto, K., Otani, H., Kodama, M., and Nishimura, S., Host recognition: Can accessibility to fungal invasion be induced by host-specific toxins without necessitating necrotic cell death? in: Phytotoxins and Plant Pathogenesis, pp. 249–265. Eds A. Graniti, R. D. Durbin and A. Ballio. Springer-Verlag, Heidelberg 1989.

    Chapter  Google Scholar 

  27. Kohmoto, K., Kondoh, Y., Kohguchi, T., Otani, H., Nishimura, S., and Scheffer, R. P., Ultrastructural changes in host leaf cells caused by host-selective toxin ofAlternaria alternata from rough lemon. Canad. J. Bot.62 (1984) 2485–2492.

    Article  CAS  Google Scholar 

  28. Kono, Y., Structural studies on host-specific pathotoxins in corn blight and citrus brown spot diseases, in: Phytotoxins and Plant Pathogenesis, pp. 7–21. Eds A. Graniti, R. D. Durbin and A. Ballio. Springer-Verlag, Heidelberg 1989.

    Chapter  Google Scholar 

  29. Kono, Y., Gardner, J. M., Suzuki, Y., and Takeuchi, S., Studies on host-selective toxins produced by a pathotype ofAlternaria citri causing brown spot disease of mandarins. Agric. Biol. Chem.50 (1986) 1597–1606.

    CAS  Google Scholar 

  30. Livingston, R. S., and Scheffer, R. P., Toxic and protective effects of analogues ofHelminthosporium sacchari toxin on sugarcane tissues. Physiol. Plant Path.24 (1984) 133–142.

    Article  CAS  Google Scholar 

  31. Maekawa, N., Yamamoto, M., Nishimura, S., Kohmoto, K., Kuwata, M., and Watanabe, Y., Studies on host-specific AF-toxins produced byAlternaria alternata strawberry pathotype causing Alternaria black spot of strawberry. 1. Production of host-specific toxins and their biological activities. Ann. Phytopath. Soc. Japan50 (1984) 600–609.

    Article  CAS  Google Scholar 

  32. Matthews, D. E., Gregory, P., and Gracen, V. E.,Helminthosporium maydis race T toxin induces leakage of NAD+ from T cytoplasm corn mitochondria. Plant Physiol.63 (1979) 1149–1153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mihara, H., Aoyagi, H., Ueno, T., Kato, T., and Izumiya, N., Cyclic peptides. XXIII. Synthesis of retro-enantio-AM-toxin I. Bull chem. Soc. Japan59 (1986) 2651–2653.

    Article  CAS  Google Scholar 

  34. Nakashima, T., Ueno, T., and Fukami, H., Structure elucidation of AK-toxins, host-specific phytotoxic metabolites, produced byAlternaria kikuchiana Tanaka. Tetrahedron Lett.23 (1982) 4469–4472.

    Article  CAS  Google Scholar 

  35. Nakashima, T., Ueno, T., Fukami, H., Taga, T., Masuda, H., Osaki, K., Otani, H., Kohmoto, K., and Nishimura, S., Isolation and structures of AK-toxin I and II, host-specific phytotoxic metabolites produced byAlternaria alternata Japanese pear pathotype. Agric. Biol. Chem.49, (1985) 807–815.

    CAS  Google Scholar 

  36. Nakatsuka, S., Ueda, K., Goto, T., Yamamoto, M., Nishimura, S., and Kohmoto, K., Structure of AF-toxin II, one of the host-specific toxins produced byAlternaria alternata strawberry pathotype. Tetrahedron Lett.27 (1986) 2753–2756.

    Article  CAS  Google Scholar 

  37. Nakatsuka, S., Goto, T., Itoh, Y., Kohmoto, K., Otani, H., Kodama, K., and Nishimura, S., Chemical studies on structures and host-specificities of ACT-toxins produced byAlternaria alternata tangerine pathotype causing citrus brown spot disease. Papers of 31st Symposium on the Chemistry of Natural Products, Nagoya 1989, pp. 671–676.

  38. Namiki, F., Yamamoto, M., Nishimura, S., Nakatsuka, S., Goto, T., Kohmoto, K., and Otani, H., Studies on host-specific AF-toxins produced byAlternaria alternata strawberry pathotype causing Alternaria black spot of strawberry. 4. Protective effect of AF-toxin II on AF-toxin I-induced toxic action and fungal infection. Ann. phytopath. Soc. Japan52 (1986) 428–436.

    Article  CAS  Google Scholar 

  39. Namiki, F., Okamoto, H., Katou, K., Yamamoto, M., Nishimura, S., Nakatsuka, S., Goto, T., Kohmoto, K., Otani, H., and Novacky, A., Studies on host-specific AF-toxins produced byAlternaria alternata strawberry pathotype causing Alternaria black spot of strawberry. 5. Effect of toxins on membrane potential of susceptible plants as assessed by electrophysiological method. Ann. Phytopath. Soc. Japan52 (1986) 610–619.

    Article  Google Scholar 

  40. Nishimura, S., and Kohmoto, K., Host-specific toxins and chemical structures fromAlternaria species. A. Rev. Phytopath.21 (1983) 87–116.

    Article  CAS  Google Scholar 

  41. Nishimura, S., and Kohmoto, K., Roles of toxins in pathogenesis, in: Toxins and Plant Pathogenesis, pp. 137–157. Eds J. M. Daly and B. J. Deverall. Academic Press, Sydney, New York 1983.

    Google Scholar 

  42. Nishimura, S., and Nakatsuka, S., Trends in host-selective toxin research in Japan. in: Host-Specific Toxins: Recognition and Specificity Factors in Plant Disease, pp. 19–31. Eds K. Kohmoto and R. D. Durbin. Tottori Univ. Press, Tottori 1989.

    Google Scholar 

  43. Nishimura, S., and Scheffer, R. P., Interactions betweenHelminthosporium victoriae spores and oat tissue. Phytopathology55 (1965) 629–634.

    Google Scholar 

  44. Nishimura, S., Vance, C. P., and Doke, N., Molecular Determinants of Plant Diseases. Japan Sci. Soc. Press/Springer-Verlag, Tokyo, Berlin 1987.

    Google Scholar 

  45. Otani, H., Kohmoto, K., Kodama, M., and Nishimura, S., Role of host-specific toxins in pathogenesis ofAlternaria alternata, in: Molecular Strategies of Pathogens and Host Plants, pp. 139–148. Eds S. S. Patil, S. Ouchi, D. I. Mills and C. P. Vance. Springer-Verlag, Berlin, New York 1991.

    Chapter  Google Scholar 

  46. Otani, H., Tomiyama, K., Okamoto, H., Nishimura, S., and Kohmoto, K., Effect of AK-toxin produced byAlternaria alternata Japanese pear pathotype on membrane potential of pear cell. Ann. phytopath. Soc. Japan55 (1989) 466–468.

    Article  Google Scholar 

  47. Otani, H., Kohmoto, K., Nishimura, S., Nakashima, S., Ueno, T., and Fukami, H., Biological activities of AK-toxins I and II, host-specific toxins fromAlternaria alternata Japanese pear pathotype. Ann. phytopath. Soc. Japan51 (1985) 285–293.

    Article  CAS  Google Scholar 

  48. Park, P., Ohno, T., Nishimura, S., Kohmoto, K., and Otani, H., Leakage of sodium ions from plasma membrane modification, associated with permeability change, in host cells treated with a host-specific toxin from a Japanese pear pathotype ofAlternaria alternata. Canad. J. Bot.65, (1987) 330–339.

    Article  CAS  Google Scholar 

  49. Pringle, R. B., and Scheffer, R. P., Host-specific plant toxins. A. Rev. Plant Path.2 (1964) 133–156.

    CAS  Google Scholar 

  50. Rasmussen, J. B., and Scheffer, R. P., Isolation and bioloical activities of four selective toxins fromHelminthosporium carbonum. Plant Physiol.86 (1988) 187–191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Scheffer, R. P., and Livingston, R. S., Host-selective toxins and their role in plant diseases. Science223 (1984) 17–21.

    Article  CAS  PubMed  Google Scholar 

  52. Schröter, H., Novacky, A., and Macko, V., Effect ofHelminthosporium sacchari-toxin on cell membrane potential susceptible sugarcane. Physiol. Plant Path.26 (1985) 165–174.

    Article  Google Scholar 

  53. Sequeira, L., Recognition and specificity between plants and pathogens, in: Challenging Problems in Plant Health, pp. 301–310. Eds T. Kommendahl and P. M. Williams. Am. Phytopath. Soc., St. Paul 1983.

    Google Scholar 

  54. Shimomura, N., Otani, H., Park, P., Kodama, M., Kohmoto, K., and Nishimura, S., Effect of light on AM-toxin action to chloroplasts in apple leaves. Ann. phytopath. Soc. Japan55 (1989) 95.

    Google Scholar 

  55. Tabira, H., Otani, H., Shimomura, N., Kodama, M., Kohmoto, K., and Nishimura, S., Light-induced insensitivity of apple and Japanese pear leaves to AM-toxin fromAlternaria alternata apple pathotype. Ann. phytopath. Soc. Japan55 (1989) 567–578.

    Article  CAS  Google Scholar 

  56. Witsenboer, H. M. A., Griend, E. G. van, Tiersma, J. B., Nijkamp, H. J. J., and Hille, J., Tomato resistance toAlternaria stem canker: localization in host genotypes and functional expression compared to non-host resistance. Theor. appl. Genet.78 (1989) 457–462.

    Article  CAS  PubMed  Google Scholar 

  57. Witsenboer, H. M. A., Schaik, C. E. van, Bino, R. J., Löffler, H. J. M., Nijkamp, H. J. J., and Hille, J., Effects ofAlternaria alternata f. sp.lycopersici toxins at different levels of tomato plant cell development. Plant Sci.56 (1988) 253–260.

    Article  CAS  Google Scholar 

  58. Wolpert, T. J., and Macko, V., Specific binding of victorin to a 100-kDa protein from oats. Proc. natl Acad. Sci. USA86 (1989) 4092–4096.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Wolpert, T. J., Macko, V., Acklin, W., and Arigoni, D., Molecular features affecting the biological activity of the host-selective toxins fromCochliobolus victoriae. Plant Physiol.88 (1988) 37–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wolpert, T. J., Macko, V., Acklin, W., Jaun, B., Seibl, J., Meili, J., and Arigoni, D., Structure of victorin C, the major host-selective toxin fromCochliobolus victoriae. Experientia41 (1985) 1524–1529.

    Article  CAS  Google Scholar 

  61. Yoder, O. C., Toxins in pathogenesis. A. Rev. Phytopath.18 (1980) 103–129.

    Article  CAS  Google Scholar 

  62. Yoder, O. C., and Scheffer, R. P., Role of toxin in early interactions ofHelminthosporium victoriae with susceptible and resistant oat tissues. Phytopathology59 (1969) 1954–1959.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kohmoto, K., Otani, H. Host recognition by toxigenic plant pathogens. Experientia 47, 755–764 (1991). https://doi.org/10.1007/BF01922454

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01922454

Key words

Navigation