Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T03:54:00.618Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic engineering of virus resistance: a successful genetical alchemy

Published online by Cambridge University Press:  05 December 2011

B. D. Harrison
B. D. Harrison
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, Scotland, U.K.
Get access

Synopsis

Some of the most successful early applications of genetic engineering in crop improvement have been in the production of virus-resistant plants. This has been achieved not by the transfer of naturally occurring resistance genes from one plant species or variety to another but by transformation with novel resistance genes based on nucleotide sequences derived from the viruses themselves or from virus-associated nucleic acids. Transformation of plants with a DNA copy of the particle protein gene of viruses that have positive-sense single-stranded RNA genomes typically confers resistance to infection with the homologous and closely related viruses. Transformation with a gene that is transcribed to produce a benign viral satellite RNA can confer virus-specific tolerance of infection. In addition, recent work with viral poly-merase gene-related sequences offers much promise, and research is active on other strategies such as the use of virus-specific ribozymes.

Already the field trialling of plants incorporating transgenic virus resistance has begun, with encouraging results, and effects on virus spread are being studied. Deployment strategies for the resistant plants must now be devised and the conjectural hazards of growing them assessed. Genetically engineered virus resistance promises to make a major contribution to the control of plant virus diseases by non-chemical methods.

Type
Research Article
Information
Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences , Volume 99 , Issue 3-4: Opportunities and Problems in Plant Biotechnology , 1992 , pp. 61 - 77
Copyright
Copyright © Royal Society of Edinburgh 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, E. J., Stark, D. M., Nelson, R. S., Powell, P. A., Turner, N. E. & Beachy, R. N. 1989. Transgenic plants that express the coat protein genes of tobacco mosaic virus or alfalfa mosaic virus interfere with disease development of some nonrelated viruses. Phytopathology 79, 1284–90.CrossRefGoogle Scholar
Barker, H. & Harrison, B. D. 1986. Restricted distribution of potato leafroll virus antigen in resistant potato genotypes and its effect on transmission of the virus by aphids. Annals of Applied Biology 109, 595–604.CrossRefGoogle Scholar
Barker, H., Reavy, B., Kumar, A., Webster, K. D. & Mayo, M. A. 1992. Restricted virus multiplication in potatoes transformed with the coat protein gene of potato leafroll luteovirus: similarities with a type of host gene-mediated resistance. Annals of Applied Biology 120, 55–64.CrossRefGoogle Scholar
Baulcombe, D. C., Saunders, G. R., Bevan, M. W., Mayo, M. A. & Harrison, B. D. 1986. Expression of biologically active viral satellite RNA from the nuclear genome of transformed plants. Nature, London 321, 446–49.CrossRefGoogle Scholar
Baulcombe, D. C., Hamilton, W. D. O., Mayo, M. A. & Harrison, B. D. 1987. Resistance to virus disease through expression of genetic material from the plant genome. In Plant resistance to viruses, pp. 170–8, eds Evered, D., Chichester, John Wiley.Google Scholar
Baulcombe, D. C., Devic, M., Jaegle, M. & Harrison, B. D. 1989. Control of viral infection in transgenic plants by expression of satellite RNA of cucumber mosaic virus. In Molecular biology of plant–pathogen interactions, pp. 257–267, eds Staskawicz, B., Ahlquist, P. & Yoder, O. eds New York: Alan R. Liss.Google Scholar
Beachy, R. N., Loesch-Fries, S. & Turner, N. E. 1990. Coat protein-mediated resistance against virus infection. Annual Review of Phytopathology 28, 451–74.CrossRefGoogle Scholar
Bujarski, J. J. & Kaesberg, P. 1986. Genetic recombination between RNA components of a multipartite plant virus. Nature, London 321, 528–31.CrossRefGoogle ScholarPubMed
Cuozzo, M., O'Connell, K. M., Kaniewski, W., Fang, R-X., Chua, N-H. & Turner, N. E. 1988. Viral protection in transgenic tobacco plants expressing the cucumber mosaic virus coat protein or its antisense RNA. Bio/Technology 6, 549–57.Google Scholar
Devic, M., Jaegle, M. & Baulcombe, D. 1990. Cucumber mosaic virus satellite RNA (strain Y): analysis of sequences which affect systemic necrosis on tomato. Journal of General Virology 71, 1443–9.CrossRefGoogle ScholarPubMed
Forster, A. C. & Symons, R. H. 1987. Self-cleavage of virusoid RNA is performed by the proposed 55-nucleotide active site. Cell 50, 9–16.CrossRefGoogle ScholarPubMed
Gerlach, W. L., Llewellyn, D. & Haseloff, J. 1987. Construction of a plant disease resistance gene from the satellite RNA of tobacco ringspot virus. Nature, London 328, 802–5.CrossRefGoogle Scholar
Gerlach, W. L., Haseloff, J. P., Young, M. J. & Bruening, G. 1990. Use of plant virus satellite RNA sequences to control gene expression. In Viral genes and plant pathogenesis pp. 177–84, eds Pirone, T. P. & Shaw, J. G. New York: Springer–Verlag.CrossRefGoogle Scholar
Golemboski, D. B., Lomonossoff, G. P. & Zaitlin, M. 1990. Plants transformed with a tobacco mosaic virus nonstructural gene sequence are resistant to the virus. Proceedings of the National Academy of Sciences USA 87, 6311–5.CrossRefGoogle ScholarPubMed
Hamilton, R. I. 1980. Defenses triggered by previous invaders: viruses. In Plant disease: an advanced treatise, Vol. 5, pp. 279–303, eds Horsfall, J. G. & Cowling, E. B. New York: Academic Press.Google Scholar
Halk, E. L., Merlo, D. J., Liao, L. W., Jarvis, N. P., Nelson, S. E., Krahn, K. J., Hill, K. K., Rashka, K. E. & Loesch-Fries, L. S. 1989. Resistance to alfalfa mosaic virus in transgenic tobacco and alfalfa. In Molecular biology of plant–pathogen interactions, pp. 283–296, eds Staskawicz, B., Ahlquist, P. & Yoder, O. New York: Alan R. Liss.Google Scholar
Harrison, B. D. & Murant, E. A. 1989. Genetic engineering of virus resistance. Report of the Scottish Crop Research Institute for 1988, 164–6.Google Scholar
Harrison, B. D., Mayo, M. A. & Baulcombe, D. C. 1987a. Virus resistance in transgenic plants that express cucumber mosaic virus satellite RNA. Nature, London 328, 799–802.CrossRefGoogle Scholar
Harrison, B. D., Mayo, M. A., Robinson, D. J., Clark, J., Murant, E. A. & Baulcombe, D. C. 1987b. Genetic engineering of virus resistance. Report of the Scottish Crop Research Institute for 1986, 167–9.Google Scholar
Harrison, B. D., Murant, E. A. & Baulcombe, D. C. 1988. Genetic engineering of virus resistance. Report of the Scottish Crop Research Institute for 1987, 182–3.Google Scholar
Haseloff, J. & Gerlach, W. L. 1988. Simple RNA enzymes with new and highly specific endoribonuclease activities. Nature, London 334, 585–91.CrossRefGoogle ScholarPubMed
Hemenway, C., Fang, R-X., Kaniewski, W. K., Chua, N-H. & Turner, N. E. 1988. Analysis of the mechanism of protection in transgenic plants expressing the potato virus X coat protein or its antisense RNA. EMBO Journal 7, 1273–80.CrossRefGoogle ScholarPubMed
Hillman, B. I., Carrington, J. C. & Morris, T. J. 1987. A defective interfering RNA that contains a mosaic of a plant virus genome. Cell 51, 427–33.CrossRefGoogle ScholarPubMed
Hoekema, A., Huisman, M. J., Molendijk, L., van den Elzen, P. J. M. & Cornelissen, B. J. C. 1989. The genetic engineering of two commercial potato cultivars for resistance to potato virus X. Bio/Technology 7, 273–8.Google Scholar
Hull, R. 1989. The movement of viruses in plants. Annual Review of Phytopathology 27, 213–240.CrossRefGoogle Scholar
Jaegle, M., Devic, M., Longstaff, M. & Baulcombe, D. 1990. Cucumber mosaic virus satellite RNA (Y strain): analysis of sequences which affect yellow mosaic symptoms on tobacco. Journal of General Virology 71, 1905–12.CrossRefGoogle ScholarPubMed
Kallerhoff, J., Perez, P., Bouzoubaa, S., Ben Tahar, S. & Perret, J. 1990. Beet necrotic yellow vein virus coat protein-mediated protection in sugarbeet (Beta vulgaris L.) protoplasts. Plant Cell Reports 9, 224–8.CrossRefGoogle ScholarPubMed
Kaniewski, W., Lawson, C., Sammons, B., Haley, L., Hart, J., Delannay, X. & Turner, N. E. 1990. Field resistance of transgenic Russet Burbank potato to effects of infection by potato virus X and potato virus Y. Bio/Technology 8, 750–4.Google Scholar
Kawchuk, L. M., Martin, R. R. & McPherson, J. 1990. Resistance in transgenic potato expressing the potato leafroll virus coat protein gene. Molecular Plant–Microbe Interactions 3, 301–7.CrossRefGoogle Scholar
Lamb, J. & Hay, R. 1990. Ribozymes that cleave potato leafroll virus RNA within the coat protein and polymerase genes. Journal of General Virology 71, 2257–64.CrossRefGoogle ScholarPubMed
Lawson, C., Kaniewski, W., Haley, L., Rozman, R., Newell, C., Sanders, P. & Turner, N. E. 1990. Engineering resistance to multiple virus infection in a commercial potato cultivar: resistance to potato virus X and potato virus Y in transgenic Russet Burbank potato. Bio/Technology 8, 127–34.Google Scholar
Li, X. H., Heaton, L. A., Morris, T. J. & Simon, A. E. 1989. Turnip crinkle virus defective interfering RNAs intensify viral symptoms and are generated de novo. Proceedings of the National Academy of Sciences USA 86, 9173–7.CrossRefGoogle ScholarPubMed
MacKenzie, D. J. & Tremaine, J. H. 1990. Transgenic Nicotiana debneyii expressing viral coat protein are resistant to potato virus S infection. Journal of General Virology 71, 2167–70.CrossRefGoogle ScholarPubMed
Mayo, M. A. & Jolly, C. A. 1991. The 5'-terminal sequence of potato leafroll virus RNA: evidence of recombination between virus and host RNA. Journal of General Virology 72, 2591–2595.CrossRefGoogle Scholar
Murant, A. F. & Mayo, M. A. 1982. Satellites of plant viruses. Annual Review of Phytopathology 20, 49–70.CrossRefGoogle Scholar
Murphy, J. F., Hunt, A. G., Rhoads, R. E. & Shaw, J. G. 1990. Expression of potyviral genes in transgenic tobacco plants. Abstracts of the VIIIth International Congress of Virology, Berlin, p.471.Google Scholar
Nakayama, M., Yoshida, T., Okuno, T. & Furusawa, I. 1990. Protection against cucumber mosaic virus and its RNA infection in transgenic tobacco plants expressing coat protein and antisense RNA of the virus. Abstracts of the VIIIth International Congress of Virology, Berlin, p. 457.Google Scholar
Nejidat, A. & Beachy, R. N. 1989. Decreased levels of TMV coat protein in transgenic tobacco plants at elevated temperatures reduce resistance to TMV infection. Virology 173, 531–8.CrossRefGoogle ScholarPubMed
Nejidat, A. & Beachy, R. N. 1990. Transgenic tobacco plants expressing a coat protein gene of tobacco mosaic virus are resistant to some other tobamoviruses. Molecular Plant-Microbe Interactions 3, 247–51.CrossRefGoogle ScholarPubMed
Nelson, R. S., Powell Abel, P. & Beachy, R. N. 1987. Lesions and virus accumulation in inoculated transgenic tobacco plants expressing the coat protein gene of tobacco mosaic virus. Virology 158, 126–32.CrossRefGoogle ScholarPubMed
Nelson, R. S., McCormick, S. M., Delannay, X., Dube, P., Layton, J., Anderson, E. J., Kaniewska, M., Proksch, R. K., Horsch, R. B., Rogers, S. G., Fraley, R. T. & Beachy, R. N. 1988. Virus tolerance, plant growth, and field performance of transgenic tomato plants expressing coat protein from tobacco mosaic virus. Bio/Technology 6, 403–09.Google Scholar
Osbourn, J. K., Watts, J. W., Beachy, R. N. & Wilson, T. M. A. 1989. Evidence that nucleocapsid disassembly and a later step in virus replication are inhibited in transgenic tobacco protoplasts expressing TMV coat protein. Virology 172, 370–3.CrossRefGoogle Scholar
Powell, P. A., Sanders, P. R., Turner, N., Fraley, R. T. & Beachy, R. N. 1990. Protection against tobacco mosaic virus infection in transgenic plants requires accumulation of coat protein rather than coat protein RNA sequences. Virology 175, 124–30.CrossRefGoogle ScholarPubMed
Powell Abel, P., Nelson, R. S., De, B., Hoffman, N., Rogers, S. G., Fraley, R. T. & Beachy, R. N. 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232, 738–43.CrossRefGoogle Scholar
Reavy, B. & Mayo, M. A. 1992. Genetic engineering of virus resistance. In Plant genetic manipulation for crop protection, 183–214, eds. Gatehouse, A. M. R., Hilder, V. A. & Boulter, D. Wallingford: CAB International.Google Scholar
Register, J. C. & Beachy, R. N. 1988. Resistance to TMV in transgenic plants results from interference with an early event in infection. Virology 166, 524–32.CrossRefGoogle ScholarPubMed
Roberts, I. M. & Harrison, B. D. 1970. Inclusion bodies and tubular structures in Chenopodium amaranticolor plants infected with strawberry latent ringspot virus. Journal of General Virology 7, 47–54.CrossRefGoogle ScholarPubMed
Robinson, D. J., Hamilton, W. D. O., Harrison, B. D. & Baulcombe, D. C. 1987. Two anomalous tobravirus isolates: evidence for RNA recombination in nature. Journal of General Virology 68, 2551–61.CrossRefGoogle Scholar
Sanford, J. C. & Johnston, S. A. 1985. The concept of parasite-derived resistance-deriving resistance genes from the parasite's own genome. Journal of Theoretical Biology 113, 395–405.CrossRefGoogle Scholar
Sequeira, L. 1984. Cross protection and induced resistance: their potential for plant disease control. Trends in Biotechnology 2, 25–30.CrossRefGoogle Scholar
Stanley, J. & Townsend, R. 1985. Characterisation of DNA forms associated with cassava latent virus infection. Nucleic Acids Research 13, 2189–206.CrossRefGoogle ScholarPubMed
Stanley, J., Frischmuth, T. & Ellwood, S. 1990. Defective viral DNA ameliorates symptoms of geminivirus infection in transgenic plants. Proceedings of the National Academy of Sciences USA 87, 6291–5.CrossRefGoogle ScholarPubMed
Stark, D. M. & Beachy, R. N. 1989. Protection against potyvirus infection in transgenic plants: evidence for broad spectrum resistance. Bio/Technology 7, 1257–62.Google Scholar
Tien, P., Zhang, X., Qiu, B., Qin, B. & Wu, G. 1987. Satellite RNA for the control of plant diseases caused by cucumber mosaic virus. Annals of Applied Biology 111, 143–52.CrossRefGoogle Scholar
Tien, P., Zhao, S. Z., Wang, X., Wang, G. J., Zhang, C. X. & Wu, S. X. 1990. Virus resistance in transgenic plants that express the monomer gene of cucumber mosaic virus (CMV) satellite RNA in greenhouse and field. Abstracts of the VIIIth International Congress of Virology, Berlin, p. 123.Google Scholar
Turner, N. E., O'Connell, K. M., Nelson, R. S., Sanders, P. R., Beachy, R. N., Fraley, R. T. & Shah, D. M. 1987. Expression of alfalfa mosaic virus coat protein gene confers cross-protection in transgenic tobacco and tomato plants. EM BO Journal 6, 1181–8.Google Scholar
Van Dun, C. M. P. & Bol, J. F. 1988. Transgenic tobacco plants accumulating tobacco rattle virus coat protein resist infection with tobacco rattle virus and pea early browning virus. Virology 167, 649–52.CrossRefGoogle ScholarPubMed
Van Dun, C. M. P., Overduin, B., Van Vloten-Doting, L. & Bol, J. F. 1988. Transgenic tobacco expressing tobacco streak virus or mutated alfalfa mosaic virus coat protein does not cross-protect against alfalfa mosaic virus infection. Virology 164, 383–9.CrossRefGoogle Scholar
van Lent, J., Wellink, J. & Goldbach, R. 1990. Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. Journal of General Virology 71, 219–23.CrossRefGoogle Scholar
Waterhouse, P. M. & Murant, A. F. 1983. Further evidence on the nature of the dependence of carrot mottle virus on carrot red leaf virus for transmission by aphids. Annals of Applied Biology 103, 455–64.CrossRefGoogle Scholar
Waterworth, H. E., Kaper, J. M. & Tousignant, M. E. 1979. CARNA 5, the small cucumber mosaic virus-dependent replicating RNA, regulates disease expression. Science 204, 845–7.CrossRefGoogle ScholarPubMed
Wellink, J. & van Kammen, A. 1989. Cell-to-cell transport of cowpea mosaic virus requires both the 58K/48K proteins and the capsid proteins. Journal of General Virology 70, 2279–86.CrossRefGoogle Scholar
Wilson, T. M. A. 1985. Nucleocapsid disassembly and early gene expression by positive-strand RNA viruses. Journal of General Virology 66, 1201–7.CrossRefGoogle ScholarPubMed
Wisniewski, L. A., Powell, P. A., Nelson, R. S. & Beachy, R. N. 1990. Local and systemic spread of tobacco mosaic virus in transgenic tobacco. The Plant Cell 2, 559–67.Google ScholarPubMed
Young, N. D. & Tanksley, S. D. 1989. RFLP analysis of the size of chromosomal segments retained around the Tm-2 locus of tomato during backcross breeding. Theoretical and Applied Genetics 77, 353–9.CrossRefGoogle ScholarPubMed