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Resistance to plant viruses: Obtaining genes by non-conventional approaches

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Summary

Plant viruses cause considerable losses to crops and none of the three current approaches to disease control are likely to give the long-term answer. The new concept of non-conventional protection, in which the expression of a viral or virus-related sequence in the plant genome interferes with the virus infection cycle, holds considerable promise for designing new resistance or protection ‘genes’. A series of targets in the viral genome is identified and a range of mechanisms for attacking those targets is discussed. There are several current systems which have been proved to give protection, at least to a certain extent, and many systems which are being researched upon for the future. Some of these are described to give a picture of the current situation and of the thinking for the future. The problems of field deployment of the transgenic plants are discussed, especially those associated with the risk to the environment. Various questions which molecular biologists and plant breeders will have to consider include what are desirable characters to have in protection ‘genes’ and how these new ’genes’ should be deployed.

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References

  • Anderson, J.M., P.Palukaitis & M.Zaitlin, 1992. A defective replicase gene induces resistance to cucumber mosaic virus in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA. 89: 8759–8763.

    Google Scholar 

  • Atreya, C.D., B.Raccah & T.P.Pirone, 1990. A point mutation in the coat protein abolishes the aphid transmissibility of a potyvirus. Virology 178: 161–165.

    Google Scholar 

  • Atreya, P.L., C.D.Atreya & T.P.Pirone, 1991. Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc. Natl. Acad. Sci. USA. 88: 7887–7891.

    Google Scholar 

  • Baulcombe, D., 1989. Strategies for virus resistance in plants. Trends in Genetics. 5: 56–60.

    Google Scholar 

  • Baulcombe, D.C., G.R.Saunders, M.W.Bevan, M.A.Mayo & B.D.Harrison, 1986. Expression of biologically active viral satellite RNA from the nuclear genome of transformed plants. Nature. 321: 446–449.

    Google Scholar 

  • Beachy, R.N., 1988. Genetic engineering for virus protection in plants: current results and future prospects. In: T.J.Mabry (Ed.), Research Bottlenecks for Commercialization and Beyond. pp. 39–47. Univ. of Texas, Austin.

    Google Scholar 

  • Beachy, R.N. (Ed.) 1993. Transgenic resistance to plant viruses. Seminars in Virology. 4: 327–416.

  • Bertioli, D.J., J.I.Cooper, M.L.Edwards & W.S.Hawes, 1992. Arabis mosaic nepovirus coat protein in transgenic tobacco lessens disease severity and virus replication. Ann Appl. Biol. 140: 47–54.

    Google Scholar 

  • Plane, S., M.Cerutti, M.Usmany, J.M.Vlak & R.Hull, 1993. Biological activity of cauliflower mosaic virus aphid transmission factor expressed in a heterologous system. Virology. 192: 643–650.

    Google Scholar 

  • Braun, C.J. & C.L.Hemenway, 1992. Expression of amino-terminal portions or full-length viral replicase genes in transgenic plants confers resistance to potato virus X infection. Plant Cell. 4: 735–744.

    Google Scholar 

  • Burgyan, J., L.Rubino & M.Russo, 1991. De novo generation of cymbidium ringspot virus defective interfering RNA. J. gen. Virol. 72: 505–509.

    Google Scholar 

  • Candelier-Harvey, P. & R.Hull, 1993. Cucumber mosaic virus genome is encapsidated in alfalfa mosaic virus coat protein expressed in transgenic plants. Transgenic Res. 2: 277–285.

    Google Scholar 

  • Carr, J.P. & M.Zaitlin, 1993. Replicase-mediated resistance. Seminars in Virology. 4: 339–347.

    Google Scholar 

  • Cascone, P.J., C.D.Carpenter, X.H.Li & A.E.Symon, 1990. Recombination between satellite RNAs of turnip crinkle virus. EMBO J 9: 1709–1715.

    Google Scholar 

  • Cohen, M., 1976. A comparison of some tristeza isolates and a cross-protection trial in Florida, Proc. 7th Conf. Int. Org. Citrus Virol., Gainsville, Fla., 50.

  • Costa, A.S. & G.W.Müller, 1980. Tristeza control by cross protection: a US-Brazil cooperative success. Plant Dis. 64: 538–541.

    Google Scholar 

  • Dahal, G., H.Hibino H. & R.C.Saxena, 1990. Association of leafhopper feeding behavior with transmission of rice tungro to susceptible and resistant rice cultivars. Phytopathology. 80: 371–377.

    Google Scholar 

  • deHaan, P., J.J.L.Gielen, M.Prins, I.G.Wijkamp, A.vanSchepen, D.Peters, M.Q.J.M.vanGrinsven & R.Goldbach, 1992. Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco plants. Bio/Technology. 10: 1133–1137.

    Google Scholar 

  • Day, A.G., E.R.Bejarano, K.W.Buck, M.Burrell, & C.P.Lichtenstein, 1991. Expression of an antisense viral gene in transgenic tobacco confers resistance to the DNA virus tomato golden mosaic virus. Proc. Natl. Acad. Sci. USA. 88: 6721–1625.

    Google Scholar 

  • Delannay, X., R.T.Fraley, S.G.Rogers, R.B.Horsch, G.M.Kishore, R.N.Beachy, N.N.Tumer, D.A.Fischoff, H.J.Klee & D.M.Shah, 1989. Development and field testing of crops improved through genetic engineering. In: J.J.Cohen (Ed.), Strengthening collaboration in biotechnology: international agricultural research and the private sector. pp 185–195. Agency for International Development, Washington DC.

    Google Scholar 

  • Devic, M., M.Jaegle & D.Baulcombe, 1990. Cucumber mosaic virus satellite RNA (strain Y); analysis of sequences which affect systemic necrosis on tomatoes. J. gen. Virol. 71: 1443–1449.

    Google Scholar 

  • deZoeten, G.A. 1991. Risk assessment: do we let history repeat itself? Phytopathology. 81: 585–586.

    Google Scholar 

  • Donson, J., C.M.Kearney, T.H.Turpen, I.A.Khan, G.Kurath, A.M.Turpen, G.E.Jones, W.O.Dawson & D.J.Lewandowski, 1993. Broad resistance to tobamoviruses is mediated by a modified tobacco mosaic virus replicase transgene. Molec. Plant Microb. Interactns. 6: 636–642.

    Google Scholar 

  • Fauquet, C. & D.Fargette, 1990. African cassava virus: etiology, epidemiology and control. Plant Disease. 74: 404–411.

    Google Scholar 

  • Fitchen, J.H. & R.N.Beachy, 1993. Genetically engineered protection against viruses in transgenic plants. Annu. Rev. Microbiol. 47: 739–763.

    Google Scholar 

  • Fraley, R.T., 1989. Field testing genetically engineered plants. In R.T.Fraley & J.Schell (Eds.), Current communications in molecular biology, genetic improvement of agriculturally important crops-progress and issues. pp. 83–86. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  • Fraser, R.S.S., 1990. Genetics of plant resistance to viruses. Ann. Rev. Phytopathol. 28: 179–200.

    Google Scholar 

  • Fraser, R.S.S., 1992. The genetics of plant-virus interactions: implications for plant breeding. Euphytica. 63: 175–185.

    Google Scholar 

  • Gadani, F., L.M.Mansky, R.Medici, W.A.Miller & J.H.Hill, 1990. Genetic engineering of plants for virus resistance. Archives of Virology. 115: 1–21.

    Google Scholar 

  • Golemboski, D.B., G.P.Lomonossoff & M.Zaitlin, 1990. Plants transformed with tobacco mosaic virus nonstructural gene sequence are resistant to the virus. Proc. Natl. Acad. Sci. USA. 87: 6311–6315.

    Google Scholar 

  • Gonsalves, D. & J.L.Slightom, 1993. Coat protein-mediated protection: analysis of trangenic plants for resistance in a variety of crops. Seminars in Virology. 4: 397–405.

    Google Scholar 

  • Harms, C.T., 1992. Engineering genetic disease resistance into crops: biotechnological approaches to crop protection. Crop. Prot. 11: 291–306.

    Google Scholar 

  • Harrison, B.D., M.A.Mayo & D.C.Baulcombe, 1987. Virus resistance in transgenic plants that express cucumber mosaic virus satellite RNA. Nature. 328: 799–802.

    Google Scholar 

  • Harrison, B.D. & D.J.Robinson, 1988. Molecular variations in vector-borne plant viruses: epidemiological significance. Phil. Trans. R. Soc. London B. 321: 447–462.

    Google Scholar 

  • Hemenway, C., R.-X.Fang, W.K.Kaniewski, N.-H.Chua & N.E.Tumer, 1988. Analysis of the mechanism of protection in transgenic plants expressing the potato virus X coat protein or its antisense RNA. EMBO J. 7: 1273–1280.

    Google Scholar 

  • Herdt, R.W., 1991. Research priorities for rice biotechnology. In: G.S.Khush & G.H.Toenniessen (Eds.), Rice Biotechnology, pp. 19–54, C.A.B. International, Wallingford, UK.

    Google Scholar 

  • Hull, R., 1984. Rapid diagnosis of plant virus infections by spot hybridization. Trends in Biotechnology. 2: 88–91.

    Google Scholar 

  • Hull, R., 1990a. Non-conventional resistance to viruses in plants — concepts and risks. In: J.P.Gustafson (Ed.), Gene Manipulation and Plant Improvement II, pp. 289–303. Stadler Genetics Symposium, Plenum Press, New York.

    Google Scholar 

  • Hull, R., 1990b. Virus resistant plants: Potential and risks. Chemistry and Industry. No. 17: 543–546.

  • Hull, R., 1991c. Plant virus pathogenesis. Seminars in Virology. 1: 239–247.

    Google Scholar 

  • Hull, R., 1991. The movement of viruses within plants. Seminars in Virology 2: 89–95.

    Google Scholar 

  • Hull, R., 1994. Molecular biology of plant virus-vector interactions. Adv. Disease Vector Res. 10: 361–386.

    Google Scholar 

  • Hull, R. & J.W.Davies, 1992. Approaches to nonconventional control of plant virus diseases. Crit. Rev. Plant Sci. 11: 17–33.

    Google Scholar 

  • Jeegle, M., M.Devic, M.Longstaff & D.Baulcombe, 1990. Cucumber mosaic virus satellite RNA (Y strain): analysis of sequences which affect yellow mosaic symptoms on tobacco. J. gen. Virol. 71: 1905–1912.

    Google Scholar 

  • Jones, R.W., A.O.Jackson & T.J.Morris, 1990. Defective-interfering RNAs and elevated temperatures inhibit replication of tomato bushy virus in inoculated protoplasts. Virology. 176: 539–545.

    Google Scholar 

  • Jongedijk, E., A.A.J.M.deSchutter, T.Stolte, P.J.M.vanElzen & B.J.C.Cornelissen, 1992. Increased resistance to potato virus X and preservation of cultivar properties in transgenic potato under field conditions. Bio/Technology. 10: 422–429.

    Google Scholar 

  • Jongedijk, E., M.J.Huisman & B.J.C.Cornelissen, 1993. Agronomic performance and field resistance of genetically modified, virus resistant potato plants. Seminars in Virology. 4: 407–416.

    Google Scholar 

  • Joshi, R.L. & V.Joshi, 1991. Strategies for expression of foreign genes in plants. Potential use of engineered plants. FEBS Letters. 281: 1–8.

    Google Scholar 

  • Kaniewski, W.K. & P.E.Thomas, 1993. Field testing of virus resistant transgenic plants. Seminars in Virology. 4: 389–396.

    Google Scholar 

  • Kawchuk, L.M., R.R.Martin, & J.McPherson, 1991. Sense and antisense RNA-mediated resistance to potato leafroll virus in Russet Burbank potato plants. Molec. Plant-Microb. Ineractn. 3: 247–253.

    Google Scholar 

  • Knorr, D.A., R.H.Mullin, P.Q.Hearne & T.A.Morris, 1991. De novo generation of defective interfering RNAs of tomato bushy stunt virus by high multiplicity passage. Virology. 181: 193–202.

    Google Scholar 

  • Kollàr, À, T.Dalmay & Burguàn, 1993. Defective interfering RNA-mediated resistance against cymbidium ringspot tombusvirus in transgenic plants. Virology. 193: 313–318.

    Google Scholar 

  • Koonin, E.V. & V.V.Dolja, 1993. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. and Molec. Biol. 28: 375–430.

    Google Scholar 

  • Lawson, C., W.Kaniewski, L.Haley, R.Rozman, C.Newell, P.Saunders & N.E.Tumer, 1990. Engineering resistance to mixed virus infection in a commercial potato cultivar: resistance to potato virus X and potato virus Y in transgenic Russet Burbank. Bio/Technology. 6: 127–134.

    Google Scholar 

  • Lecoq, H., M.Ravelonandro, C.Wopf-Scheibel, M.Monsion, B.Raccah & J.Dunez, 1993. Aphid transmission of a non-aphidtransmissible strain of zucchini yellow mosaic polyvirus from transgenic plants expressing the capsid protein of plum pox potyvirus. Molec. Plant Microbe Interns. 6: 403–406.

    Google Scholar 

  • Lindbo, J.A. & W.G.Dougherty, 1992. Untranslatable transcripts of the tobacco etch virus coat protein gene sequence can interfere with tobacco etch virus replication in transgenic plants and protoplasts. Virology. 189: 725–733.

    Google Scholar 

  • Lindbo, J.A., L.Silva-Rosales & W.G.Dougherty, 1993. Pathogen derived resistance to potyviruses: working, but why? Seminars in Virology. 4: 369–379.

    Google Scholar 

  • Lister, R.M. & M. Bar-Joseph, 1981. Closteroviruses. In: E. Kurstak (Ed.), Handbook of Plant Virus Infection and Comparative Diagnosis, pp. 809–844, Elsevier/North Holland Biomedical Press.

  • Loesch-Fries, L.S., 1990. Transgenic plants resistant to viruses. In: R.Baker & P.Dunn (Eds.), New Directions in Biological Control, pp. 629–639. UCLA Symposia on Molecular and Cellular Biology, New Series. 112. New York, Alan Liss.

    Google Scholar 

  • Lomonossoff, G.P., 1992. Virus resistance mediated by a nonstructural viral gene. In: A.Hiatt (Ed.), Transgenic Plants: Fundamentals and Applications, pp. 79–112. Marcel Dekker Inc., New York.

    Google Scholar 

  • Longstaff, M., G.Brigneti, F.Boccard, S.Chapman & D.Baulcombe, 1993. Extreme resistance to potato virus X infection in plants expressing a modified component of the putative viral replicase. EMBO J. 12: 379–386.

    Google Scholar 

  • Lucas, W.J. & S.Wolf, 1993. Plasmodesmata: the intercellular organelles of green plants. Trends in Cell Biol 3: 308–315.

    Google Scholar 

  • MacFarlane, S.A. & J.W.Davies, 1992. Plants transformed with a region of the 201-kilodalton replicase gene from pea early browning virus RNA1 are resistant to virus infection. Proc. Natl. Acad. Sci. USA. 89: 5829–5833.

    Google Scholar 

  • MacKenzie, D.J., & J.H.Tremaine, 1990. Transgenic Nicotiana debneyii expressing viral coat protein are resistant to potato virus S infection. J. gen. Virol. 71: 2167–2170.

    Google Scholar 

  • Marsh, L.E., G.P.Pogue, J.P.Connell & T.C.Hall, 1991. Artificial defective interfering RNAs derived from brome mosaic virus. J. gen. Virol. 72: 1787–1792.

    Google Scholar 

  • Mayo, M.A. & H.Barker, 1990. Induction of resistance to plant viruses by transformation with virus genes: the poacher turned gamekeeper. Aspects of Applied Biology. 24: 65–77.

    Google Scholar 

  • Meshi, T., F.Motoyoshi, A.Adachi, Y.Watanabe, N.Takamatsu & Y.Okada, 1988. Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J. 7: 1575–1581.

    Google Scholar 

  • Meshi, T., F.Motoyoshi, T.Maeda, S.Yoshiwoka, H.Watanable & Y.Okada, 1989. Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell. 1: 515–522.

    Google Scholar 

  • Morch, M.D., R.L.Joshi, T.M.Denial & A.L.Haenni, 1987. A new ‘sense’ RNA approach to block viral RNA replication in vitro. Nucl. Acids Res. 15: 4123–1430.

    Google Scholar 

  • Mori, M., K.Mise, T.Okuno, & I.Furusawa, 1992. Expression of brome mosaic virus-encoded replicase genes in transgenic tobacco plants. J. gen. Virol. 73: 169–172.

    Google Scholar 

  • Neijidat, A. & R.N.Beachy, 1989. Decreased levels of TMV coat protein in transgenic tobacco plants at elevated temperatures reduce resistance to TMV infection. Virology. 173: 531–538.

    Google Scholar 

  • Okuno, T., M.Nakayama & I.Furusawa, 1993. Cucumber mosaic virus coat protein-mediated protection. Seminars in Virology 4: 357–361.

    Google Scholar 

  • Ollennu, L.A.A., G.K. Owusu, & J.M. Thresh, 1989. The control of cocoa swollen shoot disease in Ghana. Cocoa Grower's Bulletin No. 42: 25–35.

  • Pang, S.-Z., J.L.Slightom & D.Gonsalves, 1993. Different mechanisms protect transgenic tobacco against tomato spotted wilt and Impatiens necrotic spot tospoviruses. Bio/Technology 11: 819–824.

    Google Scholar 

  • Ploeg, A.T., A.Mathis, J.F.Bol, D.J.F.Brown & D.J.Robinson, 1993. Susceptibility of transgenic tobacco plants expressing tobacco rattle virus coat protein to nematode-transmitted and mechanically inoculated tobacco rattle virus. J. gen. Virol. 74: 2709–2715.

    Google Scholar 

  • Ponz, F., A.Rowhani, S.M.Mircetich & G.Bruening, 1987. Cherry leafroll virus infections are affected by a satellite RNA that the virus does not support. Virology. 160: 183–190.

    Google Scholar 

  • Powell, C.A., R.R.Pelosi & M.Cohen, 1992. Superinfection of orange trees containing mild isolates of citrus tristeza virus with severe florida isolates of citrus tristeza virus. Plant Dis. 76: 141–144.

    Google Scholar 

  • Rast, A.T.B., 1975. Variability of tobacco mosaic virus in relation to control of tomato mosaic in glasshouse crops by resistance breeding and cross protection. Agric. Res. Rep. No. 834, Wageningen, The Netherlands.

  • Reimann-Philipp, U. & R.N.Beachy, 1993. The mechanism(s) of coat protein-mediated resistance against tobacco mosaic virus. Seminars in Virology. 4: 349–356.

    Google Scholar 

  • Sarna, S., A.Hasanuddin, I.Manwan, R.C.Cabeenagan, & H.Hibino H., 1990. Integrated management rice tungro disease in South Sulawesi, Indonesia. Crop Protection. 10: 34–41.

    Google Scholar 

  • Sanford, J.C. & S.A.Johnston, 1985. The concept of parasitederived resistance-deriving resistance genes from the parasite's own genome. J. theor. Biol. 113: 395–405.

    Google Scholar 

  • Sloat, D.E. & P.Palukaitis, 1992. A single nucleotide change within a virus satellite RNA alters the host specificity of disease induction. Plant J. 2: 43–49.

    Google Scholar 

  • Stanley, J., T.Frischmuch & S.Ellwood, 1990. Defective viral DNA ameliorates symptoms of geminivirus infection in transgenic plants. Proc. Natl. Acad. Sci. USA. 87: 6291–6295.

    Google Scholar 

  • Tavladoraki, P., E.Benvenuto, S.Trinca, D.deMartinis, A.Cattaneo & P.Galeffi, 1993. Transgenic plants expressing a functional single-chain Fv antibody are specifically protected from virus attack. Nature. 366: 469–472.

    Google Scholar 

  • Tepfer, M., 1993. Viral genes and transgenic plants. Bio/Technology. 11: 1125–1132.

    Google Scholar 

  • Truve, E., A.Aaspôllu, J.Honkanen, R.Puska, M.Mehto, A.Hassi, T.H.Teeri, M.Kelve, P.Seppänen & M.Saarma, 1993. Transgenic potato plants expressing mammalian 2′–5′ oligoadenylate synthetase are protected from potato virus X infection under field conditions. Bio/Technology. 11: 1048–1052.

    Google Scholar 

  • Tumer, N.E., W.Kaniewski, L.Haley, L.Gehrke, J.K.Lodge & P.Sanders, 1991. The second amino acid of alfalfa mosaic virus coat protein is critical for coat protein-mediated protection. Proc. Natl. Acad. Sci. USA. 88: 2331–2335.

    Google Scholar 

  • Urban, L.A., J.L.Sherwood, J.A.M.Rezende & U.Melcher U., 1990. Examination of mechanisms of cross protection with non-transgenic plants, In: R.S.S.Fraser (Ed.), Recognition and Response in Plant-Virus Interactions, pp. 415, Springer Verlag, Berlin.

    Google Scholar 

  • van denElzen, P.J.M., M.J.Huisman, D.P.-L.Willink, E.Jongedijk, A.Hoekema, & B.J.C.Cornelissen, 1989. Engineering virus resistance in agricultural crops. Pl. Molec. Biol. 13: 337–346.

    Google Scholar 

  • vanDun, C.M., L.vanVloten-Doting & J.Bol, 1989. Expression of alfalfa mosaic virus cDNA 1 and 2 in transgenic tobacco plants. Virology. 163: 572–578.

    Google Scholar 

  • vonArnim, A. & J.Stanley, 1992. Inhibition of African cassava mosaic virus systemic infection by a movement protein from a related geminivirus tomato golden mosaic virus. Virology. 187: 555–564.

    Google Scholar 

  • Wilson, T.M.A., 1993. New strategies to protect crop plants against viruses-pathogen-derived resistance blossoms. Proc. Natl. Acad. Sci. USA. 90: 3134–3141.

    Google Scholar 

  • Yeh, S-D., D.Gonsalves, H.-L.Wang, R.Namba, & R.-J.Chiu, 1988. Control of papaya ringspot virus by cross protection. Plant Dis. 72: 375–380.

    Google Scholar 

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  1. Virus Research Department, John Innes Institute, AFRC Centre for Plant Science Research, Colney Lane, NR4 7UH, Norwich, UK

    Roger Hull

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Hull, R. Resistance to plant viruses: Obtaining genes by non-conventional approaches. Euphytica 75, 195–205 (1994). https://doi.org/10.1007/BF00025604

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