Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Research
  • Published:

Inhibition of Fungal Disease Development in Plants by Engineering Controlled Cell Death

Bio/Technology volume 13, pages 1085–1089 (1995)Cite this article

Abstract

We have tested a new strategy for engineering fungal disease resistance in crops which is based on inhibition of fungal growth and reproduction by controlled generation of necrotic lesions at infection sites, analogous to the naturally occurring hypersensitive cell death. The approach relies on the use of two chimeric genes. On the one hand, a promoter fragment of the potato prp1-1 gene which mediates rapid and localized transcriptional activation selectively in response to pathogen attack is used to drive the expression of the bacterial ribonuclease, barnase. On the other hand, transgenic plants express barstar, a specific inhibitor of barnase, to minimize the detrimental effects of potential background barnase synthesis in non-infected tissue. Sporulation of the late-blight fungus Phytophthora infestans was considerably reduced on leaves from transgenic potato lines harboring this two-component system. Treatment of leaves from such plants with ethylene, a chemical stimulus of prp1-1 promoter activity, resulted in rapid tissue destruction, indirectly indicating the inducibility and action of barnase. Furthermore, the reduction of fungal sporulation cosegregated with the transgenes in an F1 population.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Broglie, K., Chet, I., Holliday, M., Cressman, R., Biddle, P., Knowlton, S., Mauvais, C.J. and Broglie, R. 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194–1197.

    Article  CAS  Google Scholar 

  2. Logemann, J., Jach, G., Tommerup, H., Mundy, J. and Schell, J. 1992. Expression of a barley ribosome-inactivating protein leads to increased fungal protection in transgenic tobacco plants. Bio/Technology 10: 305–308.

    CAS  Google Scholar 

  3. Cornelissen, B.J.C and Melchers; L.S. 1993. Strategies for control of fungal diseases with transgenic plants. Plant Physiol. 101: 709–712.

    Article  CAS  Google Scholar 

  4. Hain, R., Reif, H.-J., Krause, E., Langebartels, R., Kindl, H., Vornam, B., Wiese, W., Schmelzer, E., Schreier, P.H., Stöcker, R.H. and Stenzel, K. 1993. Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361: 153–156.

    Article  CAS  Google Scholar 

  5. Strittmatter, G. and Wegener, D. 1993. Genetic engineering of disease and pest resistance in plants: present state of the art. Z. Naturforsch. 48c: 673–688.

    Article  Google Scholar 

  6. Liu, D., Raghothama, K.G., Hasegawa, P.M. and Bressan, R.A. 1994. Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad. Sci. USA 91: 1888–1892.

    Article  CAS  Google Scholar 

  7. Zhu, Q., Maher, E.A., Masoud, S., Dixon, R.A. and Lamb, C.J. 1994. Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Bio/Technology 12: 807–812.

    CAS  Google Scholar 

  8. Pryor, T. 1987. The origin and structure of fungal disease resistance genes in plants. Trends in Genet. 3: 157–161.

    Article  Google Scholar 

  9. De Wit, P.J.G.M. 1992. Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annu. Rev. Phytopathol. 30: 391–418.

    Article  CAS  Google Scholar 

  10. Martini, N., Egen, M., Rüntz, I. and Strittmatter, G. 1993. Prompter sequences of a potato pathogenesis-related gene mediate transcriptional activation selectively upon fungal infection. Mol. Gen. Genet. 236: 179–186.

    Article  CAS  Google Scholar 

  11. Mariani, C., De Beukeleer, M., Truettner, J., Leemans, J. and Goldberg, R.B. 1990. Induction of male sterility in plants by a chimaeric ribonuclease gene. Nature 347: 737–741.

    Article  CAS  Google Scholar 

  12. Hartley, R.W. 1988. Barnase and barstar—Expression of its cloned inhibitor permits expression of a cloned ribonuclease. J. Mol. Biol. 202: 913–915.

    Article  CAS  Google Scholar 

  13. Hartley, R.W. 1989. Barnase and barstar: two small proteins to fold and fit together. Trends Biochem. Sci. 14: 450–454.

    Article  CAS  Google Scholar 

  14. Mariani, C., Gossele, V., De Beuckeleer, M., De Block, M., Goldberg, R.B., De Greef, W. and Leemans, J. 1992. A chimaeric ribonuclease-inhibitor gene restores fertility to male sterile plants. Nature 357: 384–387.

    Article  CAS  Google Scholar 

  15. Cuypers, B. and Hahlbrock, K. 1988. Immunohistochemical studies of compatible and incompatible interactions of potato leaves with Phytophthora infestans and of the nonhost response to Phytophthora megasperma. Can. J. Bot. 66: 700–705.

    Article  Google Scholar 

  16. Freytag, S., Arabatzis, N., Hahlbrock, K. and Schmelzer, E. 1994. Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta 184: 123–135.

    Google Scholar 

  17. Taylor, J.L., Fritzemeier, K.-H., Hänser, I., Kombrink, E., Rohwer, F., Schröder, M., Strittmatter, G. and Hahlbrock, K. 1990. Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato, Mol. Plant-Microbe Interact. 3: 72–77.

    CAS  PubMed  Google Scholar 

  18. Hahn, K. and Strittmatter, G. 1994. Pathogen defence gene prp1-1 from potato encodes an auxin-responsive glutathione S-transferase. Eur. J. Biochem. 226: 619–626.

    Article  CAS  Google Scholar 

  19. Deblaere, R., Reynaerts, A., Hofte, H., Hernalsteens, J.P., Leemans, J. and Van Montagu, M. 1987. Vectors for cloning in plant cells. Methods Enzymol. 153: 277–292.

    Article  CAS  Google Scholar 

  20. De Block, M. 1988. Genotype-independent leaf disc transformation of potato (Solanum tuberosum) using Agrobacterium tumefaciens. Theor. Appl. Genet. 76: 767–774.

    Article  CAS  Google Scholar 

  21. Hodgson, W.A. 1961. Laboratory testing of the potato for partial resistance to Phytophthora infestans. Am. Potato J. 38: 259–264.

    Article  Google Scholar 

  22. Sachs, L. 1972. Statistische Auswertungsmethoden. Springer-Verlag, Berlin.

  23. Jefferson, R., Goldsbrough, A. and Bevan, M. 1990. Transcriptional regulation of a patatin-1 gene in potato. Plant Mol. Biol. 14: 995–1006.

    Article  CAS  Google Scholar 

  24. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

  25. Depicker, A., Stachel, S., Dhaese, P., Zambryski, P. and Goodman, H.M. 1982. Nopaline synthase: transcript mapping and DNA sequence. J. Mol. Appl. Genet. 1: 561–573,

    CAS  Google Scholar 

  26. Velten, J. and Schell, J. 1985. Selection-expression plasmid vectors for use in genetic transformation of higher plants. Nucl. Acids Res. 13: 6981–6998.

    Article  CAS  Google Scholar 

  27. Simmons, C.R., Litts, J.C., Huang, N. and Rodriguez, R.L. 1992. Structure of a rice β-glucanase gene regulated by ethylene. cytokinin, wounding, salicylic acid and fungal elicitors. Plant Mol. Biol. 18: 33–45.

    Article  CAS  Google Scholar 

  28. Rohwer, F., Fritzemeier, K.-H., Scheel, D. and Hahlbrock, K. 1987. Biochemical reactions of different tissues of potato (Solanum tuberosum) to zoospores or elicitors from Phytophthora infestans. Planta 170: 556–561.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Max-Planck-Institut für Züchtungsforschung, Abteilung Biochemie, Carl-von-Linné-Weg 10, D-50829, Köln, Germany

    Günter Strittmatter

  2. Plant Genetic Systems, Jozef Plateaustraat 22, B-9000, Gent, Belgium

    Jan Janssens, Chris Opsomer & Johan Botterman

Authors
  1. Günter Strittmatter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan Janssens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris Opsomer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Johan Botterman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Günter Strittmatter.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Strittmatter, G., Janssens, J., Opsomer, C. et al. Inhibition of Fungal Disease Development in Plants by Engineering Controlled Cell Death. Nat Biotechnol 13, 1085–1089 (1995). https://doi.org/10.1038/nbt1095-1085

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt1095-1085

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing