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Virus-induced cell death in plants expressing the mammalian 2′,5′ oligoadenylate system

Nature Biotechnology volume 14, pages 1566–1569 (1996)Cite this article

Abstract

The major components of the 2-5A system, responsible for the mammalian interferon-induced antiviral response, are the 2′,5′ oligoadenylate synthetase (2-5Aase) and 2′,5′ oligoadenylate (2-5A) dependent ribonuclease (RNase L). Transgenic tobacco plants expressing these two enzyme activities were produced by crossing the transgenic plants expressing RNase L with those expressing 2-5Aase. The double transgenic plants showed complete resistance against cucumber mosaic virus (CMV), infection with necrotic spots only forming on the virus-inoculated leaf. On the other hand, although plants inoculated with potato virus Y (PVY) formed necrotic spots on the inoculated leaf and virus amplification could not be detected, all plants died within 20 days of inoculation. The transgenic tobacco plants expressing either 2-5Aase or RNase L activity showed typical disease symptoms with CMV- or PVY-inoculation. These results suggest that the introduced 2-5A system is activated in tobacco cells by dsRNA, the replicating intermediates of RNA viruses, leading to death of the host cells, which has not been observed in mammalian cells.

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References

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

    Article  CAS  Google Scholar 

  2. Lodge, J.K., Kaniewsky, W.K., and Turner, N.E. 1994. Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proc. Natl. Acad. Sci. USA 90: 7089–7093.

    Article  Google Scholar 

  3. Truve, E., Aaspollu, A., Honkanen, J., Puska, R., Mehto, M., Hassi, A., et al. 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.

    CAS  PubMed  Google Scholar 

  4. Watanabe, Y., Ogawa, T., Takahashi, H., Ishida, I., Takeuchi, Y., Yamamoto, M., and Okada, Y. 1995. Resistance against multiple plant viruses in plants mediated by a double stranded-RNA specific ribonuclease. FEBS Letters 372: 165–168.

    Article  CAS  Google Scholar 

  5. Lawson, C., Kaniewski, W., Haley, L., Rozman, R., Newell, C., Sanders, P., and Turner, N.E. 1990. Engineering resistance to mixed virus infection in a commercial potato cultiver: Resistance to potato virus X and potato virus Y in transgenic Russet Burbank. Bio/Technology 8: 127–134

    CAS  Google Scholar 

  6. Lengyel, P. 1982. Biochemistry of interferons and their action. Annu. Rev. Biochem. 51: 251–282.

    Article  CAS  Google Scholar 

  7. Benech, P., Mory, Y., and Chebath, J. 1985. Structure of two forms of the inter-feron-induced (2′-5′) oligo A synthetase of human cells based on cDNAs and gene sequences. EMBO J. 4: 2249–2256.

    Article  CAS  Google Scholar 

  8. Zhou, A., Hassel, B.A., and Silverman, R.H. 1993. Expression cloning of 2-5A-dependent RNAase: A uniquely regulated mediator of interferon action. Cell 2: 753–765.

    Article  Google Scholar 

  9. Wells, J.A., Swyryd, E.A., and Stark, G.R. 1984. An improved method for purifying 2′,5′-oligoadenylate synthetases. J. Biol. Chem. 259: 1363–1370.

    CAS  PubMed  Google Scholar 

  10. Silverman, R.H. 1985. Functional analysis of 2-5A-dependent RNase and 2-5A using 2′,5′-oligoadenylate-cellulose. Anal. Biochem. 144: 450–460.

    Article  CAS  Google Scholar 

  11. Okuno, T., Nakayama, M., Yoshida, S., Furusawa, I., and Komiya, T. 1993. Comparative susceptibility of transgenic tobacco plants and protoplasts expressing the coat protein gene of cucumber mosaic virus to infection with virions and RNA. Phytopathology 83: 542–547.

    Article  CAS  Google Scholar 

  12. Ohshima, K., Hataya, T., Sano, T., Inoue, A.K., and Shikata, E. 1991. Comparison of biological properties, serological characteristics and amino acid sequences of coat protein between potato virus Y ordinary strain and necrotic strain. Ann. Phytopath. Soc. Japan 57: 615–622.

    Article  CAS  Google Scholar 

  13. Meshi, T., Meshi, T., and Okada, Y. 1982. Nucleotide sequence and its character of cistron coding for the 30 kilodalton protein of tobacco mosaic virus DM strain. J. Biochem. 91: 1441–1444.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Devash, Y., Reichman, M., Sela, I., Reichenbach, N.L., and Suhadolnik, R.J. 1985. Plant oligoadenylates: enzymatic synthesis, isolation, and biological activities. Biochemistry 24: 593–599.

    Article  CAS  Google Scholar 

  16. Truve, E., Kelve, M., Aaspollu, A., Kuusksalu, A., Seppanen, P., and Saarma, M. 1994. Principles and background for the construction of transgenic plants displaying multiple virus resistance. Arch. Virol. [suppl] 9: 41–50.

    CAS  Google Scholar 

  17. Mehdy, M.C. 1994. Active oxygen species in plant defense against pathogens. Plant Pathol. 105: 467–472.

    CAS  Google Scholar 

  18. Valverde, R.A., Dodds, J.A., and Heick, J. 1986. Double-stranded RNA from plants infected with virus having elongated particles and undivided genomes. Phytopathology 76: 459–465.

    Article  CAS  Google Scholar 

  19. Silverman, R.H., Jung, D.D., Nolan-Sorden, N.L., Dieffenbach, C.W., Kedar, V.P., and SenGupta, D.N. 1988. Purification and analysis of murine 2-5A-dependent RNase. J. Biol. Chem. 263: 7336–7341.

    CAS  PubMed  Google Scholar 

  20. Puska, R., Seppanen, P., Honkanen, J., Truve, E., Aaspollu, A., Nigul, L., and Saarma, M. 1994. Transgenic plants show protection against RNA viruses. The 4th International Congress of Plant Molecular Biology (Amsterdam), Abstract.

  21. Mitra, A., Higgins, D.W., Langenberg, W.G., Nie, H., Sengupta, D.N., and Silverman, R. 1996. A mammalian 2-5A system functions as an antiviral pathway in transgenic plants. Proc. Natl. Acad. Sci. USA 93: 6780–6785.

    Article  CAS  Google Scholar 

  22. Towbin, H., Gordon, J., and Staehelin, T. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitro cellulose sheets—procedure and some

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Author notes

  1. Isao Ishida: e-mail: i-ishida@kirin.co.jp

Authors and Affiliations

  1. Central Laboratories for Key Technology, 1-13-5, Fukuura, Kanazawa-ku Yokohama-shi, Kanagawa, 236, Japan

    Toshiya Ogawa, Tamaki Hori & Isao Ishida

Authors
  1. Toshiya Ogawa
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  2. Tamaki Hori
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Ogawa, T., Hori, T. & Ishida, I. Virus-induced cell death in plants expressing the mammalian 2′,5′ oligoadenylate system. Nat Biotechnol 14, 1566–1569 (1996). https://doi.org/10.1038/nbt1196-1566

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  • DOI: https://doi.org/10.1038/nbt1196-1566

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