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Strategies for engineering virus resistance in transgenic plants

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Summary

Transgenic virus-resistant plants were first produced in 1986 by genetically engineering tobacco plants to express the coat protein of tobacco mosaic virus. The introduction of coat protein transgenes has since proved to be an extremely effective and generally applicable approach to engineering virus resistance in crop plants. Extensive field trials with transgenic, virus-resistant tobacco, tomato, potato and cucumber lines have confirmed not only the durability of the resistance under natural conditions but the ease with which virus-resistant lines retaining the original cultivar traits can be recovered.

A number of alternative anti-viral strategies based on transgenes from a surprisingly wide variety of sources have also been developed. These include the use of viral genes coding for proteins involved in the replication cycle and in systemic transport of viruses within the plant, the use of interfering viral RNA sequences, and the use of transgenes derived from plant and animal sources. In the latter category, the use of mammalian antibodies to confer disease resistance in plants is a particularly exciting new development. Considerable progress has also been made towards the molecular cloning of natural anti-viral resistance genes in plants.

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References

  • Adams S.E., R.A.C. Jones & R.H.A. Coutts, 1986. Expression of potato virus X resistance gene Rx in potato leaf protoplasts. J. Gen. Virol. 67: 2341–2345.

    Article  CAS  Google Scholar 

  • Alexander D., R.M. Goodman, M. Gut-Rella, C. Glascock, K. Weyman, L. Friedrich, D. Maddox, P. Ahl-Goy, T. Lunz, E. Ward & J. Ryals, 1993. Increased tolerance of two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1 a. Proc. Natl. Acad. Sci. USA 90: 7327–7331.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Audy P., P. Palukaitis, S.A. Slack & M. Zaitlin, 1994. Replicasemediated resistance to potato virus Y in transgenic tobacco plants. Mol. Plant-Microbe Interact. 7: 15–22.

    PubMed  CAS  Google Scholar 

  • Barker H., B. Reavy, K.D. Webster, C.A. Jolly, A. Kumar & M.A. Mayo, 1993. Relationship between transcript production and virus resistance in tobacco expressing the potato leafroll virus coat protein gene. Plant Cell Rep. 13: 54–58.

    Article  CAS  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.

    Article  PubMed  CAS  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: 6721–6725.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Deom C.M., M. Lapidot & R.N. Beachy, 1992. Plant virus movement proteins. Cell 69: 221–224.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Dinant S., F. Blaise, C. Kusiak, S. Astier-Manifacier & J. Albouy, 1993. Heterologous resistance to potato virus Y in transgenic tobacco plants expressing the coat protein gene of lettuce mosaic potyvirus. Phytopathology 83: 818–824.

    Article  CAS  Google Scholar 

  • Dixon R.A. & C.J. Lamb, 1990. Molecular communication in interactions between plants and microbial pathogens. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41: 339–367.

    Article  CAS  Google Scholar 

  • Donson J., C.M. Keamey, 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 gene. Mol. Plant-Microbe Interact. 6: 635–642.

    PubMed  CAS  Google Scholar 

  • Falk B.W. & G. Breuning, 1994. Will transgenic crops generate new viruses and new diseases? Science 263: 1395–1396.

    Article  PubMed  CAS  Google Scholar 

  • Farinelli L. & P. Malnoe, 1993. Coat protein gene-mediated resistance to potato virus Y in tobacco: examination of the resistance mechanisms-Is the transgenic coat protein required for protection? Mol. Plant-Microbe Interact. 6: 284–292.

    PubMed  CAS  Google Scholar 

  • Fraser R.S.S., 1990. Genes for resistance to plant viruses. Crit. Rev. Plant Sci. 3: 275–294.

    Google Scholar 

  • Fulton R.W., 1986. Practices and precautions in the use of cross protection for plant virus disease control. Ann. Rev. Phytopath. 24: 67–93.

    Article  Google Scholar 

  • Gaffney T., L. Friedrich, B. Vernooij, D. Negrotto, G. Nye, S. Uknes, E. Ward & J. Ryals, 1993. Requirement for salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756.

    Article  PubMed  CAS  Google Scholar 

  • Gerlach W.L., D. Llewellyn & J. Haseloff, 1987. Construction of a disease resistance gene using the satellite RNA of tobacco ringspot virus. Nature 328: 802–806.

    Article  CAS  Google Scholar 

  • Gielen J.J.L., P.de Haan, A.J. Kool, D. Peters, M.Q.J.M. van Grinsven & R.W. Goldbach, 1991. Engineered resistance to tomato spotted wilt virus, a negative strand RNA virus. Bio/Technology 9: 1363–1367.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gonsalves D., P. Chee, R. Provvidenti, R. Seem & J.L. Slightom, 1992. Comparison of coat protein-mediated and genetically-derived resistance in cucumbers to infection by cucumber mosaic virus under field conditions with natural challenge inoculations by vectors. Bio/Technology 10: 1562–1570.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hemenway C., R.-X. Fang, J.J. 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.

    PubMed  CAS  Google Scholar 

  • Hiatt A., R. Cafferkey & K. Bowdish, 1989. Production of antibodies in transgenic plants. Nature 342: 76–78.

    Article  PubMed  CAS  Google Scholar 

  • Hooftvan Huijsduijnen, R.A.M., S.W. Alblas, R.H.De Rijk & J.F. Bol, 1986b. Induction by salicylic acid of pathogenesis-related proteins and resistance to alfalfa mosaic virus infection in various plant species. J. Gen. Virol. 67: 2135–2143.

    Article  Google Scholar 

  • Hooftvan Huijsduijnen, R.A.M., L.C.Van Loon & J.F. Bol, 1986a. cDNA cloning of six mRNAs induced by TMV infection of tobacco and a characterization of their translation products. EMBO J. 5: 2057–2061.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jones, J.D.G., M. Dixon, K. Hammond-Kosack, K. Harrison, K. Hatzixanthis, D. Jones & C. Thomas, 1994. Characterization of tomato genes that confer resistance to Cladosporium fulvum. Abstracts, 4th International Congress of Plant Molecular Biology.

  • Jongedijk E., A.J.M.de Schutter, T. Stolte, P.J.M.van den Elzen & 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.

    Article  PubMed  CAS  Google Scholar 

  • Kaniewski W., C. Lawson, B. Sammons, L. Haley, J. Hart, X. Delannay & N.E. Tumer, 1990. Field resistance of transgenic russet burbank potato to effects of infection by potato virus X and potato virus Y. Bio/Technology 8: 750–754.

    Article  Google Scholar 

  • Kauffman S., M. Legrand, P. Geoffroy & G. Fritig, 1987. Biological function of ‘pathogenesis-related’ proteins: Four PR proteins of tobacco have 1,3-beta glucanase activity. EMBO J. 6: 3209–3212.

    Google Scholar 

  • Kavanagh T., M. Goulden, S. Santa Cruz, S. Chapman, I. Barker & D.C. Baulcombe, 1992. Molecular analysis of a resistancebreaking strain of potato virus X. Virology 189: 609–617.

    Article  PubMed  CAS  Google Scholar 

  • Kohm B.A., M.G. Goulden, J.E. Gilbert, T.A. Kavanagh & D.C. Baulcombe, 1993. A potato virus X resistance gene mediates an induced, non-specific resistance in protoplasts. The Plant Cell 5: 913–920.

    Article  PubMed  CAS  Google Scholar 

  • Kallar A., T. Dalmay & J. Burgyan, 1993. Defective interfering RNA-mediated resistance against cymbidium ringspot tombusvirus in transgenic plants. Virology 193: 313–318.

    Article  Google Scholar 

  • Kulaeva O.N., A.B. Fedina, E.A. Burkhanova, N.N. Karaivako, M.Y. Karpeisky, I.B. Kaplan, M.E. Taliansky & J.G. Atabekov, 1992. Biological activities of human interferon and 2′–5′ oligoad-enylates in plants. Plant Mol. Biol. 20: 383–393.

    Article  PubMed  CAS  Google Scholar 

  • Kunik T., R. Salomon, D. Zamir, N. Navot, M. Zeidan, I. Michelson, Y. Gafni & H. Czosnek, 1994. Transgenic tomato plants expressing the tomato leaf curl virus capsid protein are resistant to the virus. Bio/Technology 12: 500–506.

    Article  PubMed  CAS  Google Scholar 

  • Lapidot M., R. Gafny, B. Ding, S. Wolf, W.J. Lucas & R.N. Beachy, 1993. A dysfunctional movement protein of tobacco mosaic virus that partially modifies the plasmodesmata and limits virus spread in transgenic plants. Plant J. 4: 959–970.

    Article  CAS  Google Scholar 

  • Legrand M., S. Kauffman, P. Geoffrey & B. Fritig, 1987. Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. Proc. Natl. Acad. Sci. USA 84: 6750–6754.

    Article  PubMed  CAS  Google Scholar 

  • Linthorst H.J.M., R.L.J. Meuwissen, S. Kauffman & J.F. Bol, 1989. Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus infection. The Plant Cell 1: 285–291.

    Article  PubMed  CAS  Google Scholar 

  • Lodge J.K., W.K. Kaniewski & N.E. Tumer, 1993. Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proc. Natl. Acad. Sci. USA 90: 7089–7093.

    Article  PubMed  CAS  Google Scholar 

  • Loesch-Fries L.S., D. Merlo, T. Zinnen, L. Burhop, K. Hill, K. Krahn, N. Jarvis, S. Nelson & E. Halk, 1987. Expression of alfalfa mosaic virus RNA 4 in transgenic plants confers virus resistance. EMBO J. 6: 1845–1851.

    PubMed  CAS  Google Scholar 

  • Longstaff M., G. Brigneti, F. Boccard, S. Chapman & D.C. 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.

    PubMed  CAS  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: 5829–2833.

    Article  PubMed  CAS  Google Scholar 

  • Maiti I.B., J.F. Murphy, J.G. Shaw & A.G. Hunt, 1993. Plants that express a potyvirus proteinase gene are resistant to virus infection. Proc. Natl. Acad. Sci. USA 90: 6110–6114.

    Article  PubMed  CAS  Google Scholar 

  • Martin G.B., S.H. Brommoschenkels, J. Chunwongse, A. Frary, M.W. Ganal, R. Spivey, T. Wu, E.D. Earle & S.D. Tanksley, 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432–1436.

    Article  PubMed  CAS  Google Scholar 

  • Nakajima M., T. Hayakawa, I. Nakamura & M. Suzuki, 1993. Protection against cucumber mosaic virus (CMV) strains O and Y and chrysanthemum mild mottle virus in transgenic plants expressing CMV-O coat protein. J. Gen. Virol. 74: 319–322.

    Article  PubMed  CAS  Google Scholar 

  • Nejidat A. & R.N. Beachy, 1990. Transgenic tobacco plants expressing a tobacco virus coat protein gene are resistant to some tobamoviruses. Mol. Plant Microb. Interact. 3: 247–251.

    CAS  Google Scholar 

  • Nelson R.S., D.A. Roth & J.D. Johnson, 1993. Tobacco mosaic virus infection of transgenic Nicotiana tabacum plants is inhibited by antisense constructs directed a the 5′ region of viral-RNA. Gene 127: 227–232.

    Article  PubMed  CAS  Google Scholar 

  • Palukaitis P., M.J. Roosinck, R.G. Dietzgen & R.I.B. Francki, 1992. Cucumber mosaic virus. Adv. Virus Res. 41: 281–348.

    Article  PubMed  CAS  Google Scholar 

  • Powell-Abel P.A., R.S. Nelson, B.De, N. Hoffman, S.G. Rogers, R.T. Fraley & R.N. Beachy, 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232: 738–743.

    Article  Google Scholar 

  • Ritter E., T. Debener, A. Barone, F. Salamini & C. Gebhart, 1991. RFLP mapping on potato chromosomes of two genes controlling extreme resistance to potato virus X (PVX). Mol. Gen. Genet. 227: 81–85.

    Article  PubMed  CAS  Google Scholar 

  • Roberts W.K. & C.P. Selitrennikoff, 1990. Zeamatin, an antifungal protein from maize with membrane-permeabilizing activity. J. Gen. Microbiol. 136: 1171–1778.

    Google Scholar 

  • Rubino L., R. Lopo & M. Russo, 1993. Resistance of cymbidium ringspot virus infection in transgenic Nicotiana benthamiana plants expressing full-length viral replicase gene. Mol. Plant-Microbe Interact. 6: 729–734.

    CAS  Google Scholar 

  • Sanders P.R., B. Sammons, W. Kaniewski, L. Haley, J. Layton, B.J. Lavallee, X. Delannay & N.E. Tumer, 1992. Field resistance of transgenic tomatoes expressing the tobacco mosaic virus or tomato mosaic virus coat protein genes. Phytopathology 82: 683–690.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Stark D.M. & R.N. Beachy, 1989. Protection against potyvirus infection in transgenic plants: evidence for broad spectrum resistance. Bio/Technology 7: 1257–1262.

    Google Scholar 

  • Stirpe F., L. Barbieri, M.G. Battelli, M. Soria & D.A. Lappi, 1992. Ribosome-inactivating proteins from plants: present status and future prospects. Bio/Technology 10: 405–412.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Taylor S., A. Massiah, G. Lomonossoff, L.M. Roberts, J.M. Lord & M. Hartley, 1994. Correlation between the activities of five ribosome-inactivating proteins in depurination of tobacco ribosomes and inhibition of tobacco mosaic virus infection. Plant J. 5: 827–835.

    Article  PubMed  CAS  Google Scholar 

  • Tepfer M., 1993. Viral genes and transgenic plants. Bio/Technology 11: 1125–1129.

    CAS  Google Scholar 

  • Tomlinson J.A., V.M. Walker, T.H. Flewett & G.R. Barclay, 1974. The inhibition of infection by cucumber mosaic virus by extracts from Phytolacca americana. J. Gen. Virol. 22: 225–232.

    Article  PubMed  CAS  Google Scholar 

  • Truve E., A. Aaspollu, J. Honkanen, R. Puska, M. Mehto, A. Hassi, T.H. Teeri, M. Kelve, P. Seppanen & 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.

    Article  PubMed  CAS  Google Scholar 

  • Vardi E., I. Sela, O. Edelbaum, O. Livneh, L. Kuznetsova & Y. Stram, 1993. Plants transformed with a cistron of a potato virus Y protease (NIa) are resistant to virus infection. Proc. Natl. Acad. Sci. USA 90: 7513–7517.

    Article  PubMed  CAS  Google Scholar 

  • Ward E.R., S.J. Uknes, S.C. Williams, S.S. Dincher, D.L. Wiederhold, D.C. Alexander, P. Ahl-Goy, J.P. Metraux & J.A. Ryals, 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085–1094.

    Article  PubMed  CAS  Google Scholar 

  • Whitham S., S.P. Dinesh-Kumar, D. Choi, R. Hehl, C. Corr & B. Baker, 1994. The product of the tobacco mosaic virus resistance gene N: Similarity to Toll and the Interleukin 1 receptor. Cell 78, 1101–1115.

    Article  PubMed  CAS  Google Scholar 

  • Zaccomer B., F. Cellier, J-C. Boyer, A-L. Haenni & M. Tepfer, 1993. Transgenic plants that express genes including the 3′ untranslated region of the turnip yellow mosaic virus (TYMV) genome are partially protected against TYMV infection. Gene 136: 87–94.

    Article  PubMed  CAS  Google Scholar 

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Kavanagh, T.A., Spillane, C. Strategies for engineering virus resistance in transgenic plants. Euphytica 85, 149–158 (1995). https://doi.org/10.1007/BF00023943

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