Skip to main content
SpringerLink
Log in

Role of toxins in evolution and ecology of plant pathogenic fungi

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

Abstract

Many fungal pathogens of plants adapt readily to changes in agriculture. Among the most revealing is a fungal group whose species produce host-selective toxins as key determinants of disease. Several lines of evidence support the hypothesis that these fungi evolved from opportunistic, low-grade pathogens by gaining new genetic information leading to toxin production; in some species, toxin production is known to be under single gene control. as a result of this evolution, these fungi became virulent and host-specialized. The best-known model cases belong to the generaCochliobolus andAlternaria; there are suggestions of evolutionary lines among these genera, with species that range from saprophytes to opportunists to specialized pathogens. Host specialization can lead to genetic isolation, a first step in speciation. Ability to produce host-selective toxin has allowed these fungi to exploit the monocultures and genetic uniformity of modern agriculture. Destructive epidemics have been the result.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bednarski, M. A., Izawa, S., and Scheffer, R. P., Reversible effects of toxin fromHelminthosporium maydis race T on oxidative phosphorylation by mitochondria from maize. Plant Physiol.59 (1977) 540–545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Brasier, C. M., The dynamics of fungal speciation, in: Evolutionary Biology of the Fungi, pp. 231–260. Eds A. D. M. Rayner, C. M. Brasier and D. Moore. Cambridge Univ. Press, Cambridge 1987.

    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. Bronson, C. R., and Scheffer, R. P., Heat and aging-induced tolerance of sorghum and oat tissues to host-selective toxins. Phytopathology67 (1977) 1232–1238.

    Article  CAS  Google Scholar 

  5. Christensen, J. J., Physiological specialization and parasitism ofHelminthosporium sativum. Univ. Minn. Agr. Exp. Sta., Tech. Bull.37 (1926), St. Paul.

  6. Domsch, K. H., Gams, W., and Anderson, T. H., Compendium of Soil Fungi, Vols 1 and 2. Academic Press, New York 1980.

    Google Scholar 

  7. Ellis, M. B., Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew 1971.

  8. El-Nashaar, H. M., and Stack, R. W., Effect of long-term continuous cropping of spring wheat on aggressiveness ofCochliobolus sativus. Can. J. Plant Sci.69 (1989) 395–400.

    Article  Google Scholar 

  9. Garrett, S. D., Biology of Root Infecting Fungi. Cambridge Univ. Press, Cambridge 1956.

    Book  Google Scholar 

  10. Hamid, A. H., Ayers, J. E., and Hill, R. R., The inheritance of resistance in corn toCochliobolus carbonum race 3. Phytopathology72 (1982) 1173–1177.

    Article  Google Scholar 

  11. Hansen, E. M., Speciation inPhytophthora: evidence from thePhytophthora megasperma complex, in: Evolutionary Biology of the Fungi, pp. 325–337. Eds A. D. M. Rayner, C. M. Brasier and D. Moore. Cambridge Univ. Press, Cambridge 1987.

    Google Scholar 

  12. Kleinkauf, H., and von Dohren, H. (Eds), Peptide Antibiotics, Biosynthesis and Functions. DeGruyten, Berlin 1982.

    Google Scholar 

  13. Kline, D. M., and Nelson, R. R., Pathogenicity of isolates ofCochliobolus sativus from cultivated and wild gramineous hosts from the western hemisphere to species of Gramineae. Plant Dis. Reptr47 (1963) 890–894.

    Google Scholar 

  14. Kline, D. M., and Nelson, R. R., Inheritance of factors inCochliobolus carbonum conditioning symptom expression on grass hosts. Phytopathology59 (1969) 1133–1135.

    Google Scholar 

  15. Kline, D. M., and Nelson, R. R., The inheritance of factors inCochliobolus sativus conditioning lesion induction on gramineous hosts. Phytopathology61 (1971) 1052–1054.

    Article  Google Scholar 

  16. Kohmoto, K., Scheffer, R. P., and Whiteside, J. O., Host-selective toxins fromAlternaria citri. Phytopathology69 (1979) 667–671.

    Article  CAS  Google Scholar 

  17. 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, Berlin 1989.

    Chapter  Google Scholar 

  18. Leonard, K. J., Races ofBipolrais maydis in the southeastern U.S. from 1974 to 1976. Plant Dis. Reptr61 (1977) 914–915.

    Google Scholar 

  19. Livingston, R. S., and Scheffer, R. P., Toxic and protective effects of analogs ofHelminthosporium sacchari toxin on sugarcane tissues. Physiol. Plant Path.24 (1984) 133–144.

    Article  CAS  Google Scholar 

  20. Luke, H. H., Murphy, H. C., and Petr, F. C., Inheritance of spontaneous mutations of the Victoria locus in oats. Phytopathology56 (1966) 210–212.

    Google Scholar 

  21. Macko, V., Structural aspects of toxins, in: Toxins and Plant Pathogenesis, pp. 41–80. Eds J. M. Daly and B. J. Deverall. Academic Press, Sydney 1983.

    Google Scholar 

  22. Macko, V., Wolpert, T. J., Acklin, W., and Arigoni, D., Biological activities and structural variants of host-selective toxins fromCochliobolus victoriae, in: Phytotoxins and Plant Pathogenesis, pp. 31–41. Eds A. Graniti, R. D. Durbin and A. Ballio. Springer-Verlag, Berlin 1989.

    Chapter  Google Scholar 

  23. Nakajima, H., and Scheffer, R. P., Interconversions of aglycone and host-selective toxin fromHelminthosporium sacchari. Phytochemistry26 (1987) 1607–1611.

    Article  CAS  Google Scholar 

  24. Nelson, R. R., A correlation of interspecific fertility and conidial morphology in species ofHelminthosporium exhibiting bipolar germination. Mycologia52 (1960) 753–761.

    Article  Google Scholar 

  25. Nelson, R. R., Evolution of sexuality and pathogenicity. I. Interspecific crosses in the genusHelminthosporium. Phytopathology50 (1960) 375–377.

    Google Scholar 

  26. Nelson, R. R., Evidence of gene pools for pathogenicity in species ofHelminthosporium. Phytopathology51 (1961) 736–737.

    Google Scholar 

  27. Nelson, R. R., and Kline, D. M., Intraspecific variation in pathogenicity in the genusHelminthosporium to gramineous species. Phytopathology52 (1962) 1045–1049.

    Google Scholar 

  28. Nelson, R. R., and Kline, D. M., Genes for pathogenicity inCochliobolus heterostrophus. Can. J. Bot.47 (1969) 1311–1314.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. 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 University, tottori, Japan 1989.

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rodriguez, A. E., and Ullstrup, A. J., Pathogenicity of monoascosporic progenies ofTrichometasphaeria turcica. Phytopathology52 (1962) 599–601.

    Google Scholar 

  34. Scheffer, R. P., Host-specific toxins in relation to pathogenesis and disease resistance, in: Physiological Plant Pathology, pp. 247–269. Eds R. Heitefuss and P. H. Williams. Springer-Verlag, Berlin 1976.

    Chapter  Google Scholar 

  35. Scheffer, R. P., Toxins as chemical determinants of plant disease, in: Toxins and Plant Pathogenesis, pp. 1–40. Eds J. M. Daly and B. J. Deverall. Academic Press, Sydney 1983.

    Google Scholar 

  36. Scheffer, R. P., Ecological consequences of toxin production byCochliobolus and related fungi, in: Phytotoxins and Plant Pathogenesis, pp. 285–300. Eds A. Graniti, R. D. Durbin and A. Ballio. Springer-Verlag, Berlin 1989.

    Chapter  Google Scholar 

  37. Scheffer, R. P., and Livingston, R. S., Sensitivity of sugarcane clones to toxin fromHelminthosporium sacchari as determined by electrolyte leakage. Phytopathology70 (1980) 400–404.

    Article  CAS  Google Scholar 

  38. Scheffer, R. P., and Livingston, R. S., Host-selective toxins and their role in plant diseases. Science23 (1984) 17–21.

    Article  Google Scholar 

  39. Scheffer, R. P., Nelson, R. R., and Ullstrup, A. J., Inheritance of toxin production and pathogenicity inCochliobolus carbonum andCochliobolus victoriae. Phytopathology57 (1967) 1288–1291.

    Google Scholar 

  40. Scheffer, R. P., and Pringle, R. B., A selective toxin produced byPericonia circinata. Nature191 (1961) 912–913.

    Article  CAS  PubMed  Google Scholar 

  41. Schertz, K. F., and Tai, Y. P., Inheritance of reaction ofSorghum bicolor to toxin produced byPericonia circinata. Crop Sci.9 (1969) 621–624.

    Article  Google Scholar 

  42. Stakman, E. C., and Harrar, J. G., Principles of Plant Pathology. The Ronald Press, New York 1957.

    Google Scholar 

  43. Stoessl, A., Structure and biogenetic relations: Fungal nonhostspecific, in: Toxins in Plant Disease, pp. 109–219. Ed. R. D. Durbin. Academic Press, New York 1981.

    Chapter  Google Scholar 

  44. Takai, S., Host-specific factors in Dutch elm disease, in: Host-Specific Toxins: Recognition and Specificity Factors in Plant Disease, pp. 75–96. Eds K. Kohmoto and R. D. Durbin. Tottori University, Tottori, Japan 1989.

    Google Scholar 

  45. Tegtmeier, K. J., Daly, J. M., and Yoder, O. C., T-toxin production by near-isogenic isolates ofCochliobolus heterostrophus races O and T. Phytopathology72 (1982) 1492–1495.

    Article  CAS  Google Scholar 

  46. Turner, G., and Ballance, D. J., Structural variations and expression of fungal chromosomal genes, in: Evolutionary Biology of the Fungi, pp. 17–32. Eds A. D. M. Rayner, C. M. Brasier and D. Moore. Cambridge Univ. Press, Cambridge 1987.

    Google Scholar 

  47. Ullstrup, A. J., The impacts of the southern corn leaf blight epidemics of 1970–1971. A. Rev. Phytopath.10 (1972) 37–50.

    Article  Google Scholar 

  48. Walton, J. D., Earle, E. D., Yoder, O. C., and Spanswick, R. M., Reduction of adenosine triphosphate levels in susceptible maize mesophyll protoplasts byHelminthosporium maydis race T toxin. Plant Physiol.63 (1979) 806–810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wolfe, M. S., and Schwarzbach, E., The recent history of the evolution of barley mildew in Europe, in: The Powdery Mildews, pp. 127–157. Ed. D. M. Spencer. Academic Press, London 1978.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany and Plant Pathology, Michigan State University, 48824, East Lansing, Michigan, USA

    R. P. Scheffer

Authors
  1. R. P. Scheffer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scheffer, R.P. Role of toxins in evolution and ecology of plant pathogenic fungi. Experientia 47, 804–811 (1991). https://doi.org/10.1007/BF01922460

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01922460

Key words

Search

Navigation