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Plants rendered herbicide-susceptible by cauliflower mosaic virus–elicited suppression of a 35S promoter-regulated transgene

Abstract

Crop plants genetically modified for herbicide tolerance were some of the first to be released into the environment. Frequently, the cauliflower mosaic virus (CaMV) 35S promoter is used to drive expression of the herbicide tolerance transgene. We analyzed the response to CaMV infection of a transgenic oilseed rape line containing the bialaphos tolerance gene (BAR) from Streptomyces hygroscopicus, regulated by the 35S promoter. Oilseed rape is susceptible to CaMV, but plants recover from infection. CaMV infection altered the expression of the herbicide tolerance gene such that plants became susceptible to the herbicide. The effect on transgene expression differed in infections with viral pathogenic variants typical of those found in natural situations worldwide. Susceptibility to the herbicide was most likely a result of transcriptional gene silencing of the transgene. Our results show that transgene phenotypes can be modified by pathogen invasion.

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Figure 1: Effect of CaMV infection on herbicide tolerance in transgenic oilseed rape plants.
Figure 2: Effect of CaMV infection on BAR transgene expression in oilseed rape.
Figure 3: Effect of CaMV infection on herbicide tolerance and transgene expression in leaves of flowering transgenic oilseed rape plants.
Figure 4: Effects of CaMV pathogenic variants on herbicide suppression.

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References

  1. Vaucheret, H. et al. Transgene-induced gene silencing in plants. Plant J. 16, 651–659 (1998).

    Article  CAS  Google Scholar 

  2. Kooter, J.M., Matzke, M.A. & Meyer, P. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci. 4, 340–346 (1999).

    Article  CAS  Google Scholar 

  3. Selker, E.U. Gene silencing: Repeats that count. Cell 97, 157–160 (1999).

    Article  CAS  Google Scholar 

  4. Waterhouse, P.M., Smith, N.A. & Wang, M.B. Virus resistance and gene silencing: killing the messenger. Trends Plant Sci. 4, 452–457 (1999).

    Article  CAS  Google Scholar 

  5. Baulcombe, D.C. Gene silencing: RNA makes RNA makes no protein. Curr. Biol. 9, 599–601 (1999).

    Article  Google Scholar 

  6. Covey, S.N., Al-Kaff, N.S., Lángara, A. & Turner D.S. Plant combat infection by gene silencing. Nature 385, 781–782 (1997).

    Article  CAS  Google Scholar 

  7. Ratcliff, F., Harrison, B.D. & Baulcombe, D.C. A similarity between viral defense and gene silencing in plants. Science 276, 1558–1560 (1997).

    Article  CAS  Google Scholar 

  8. Al-Kaff, N.S. et al. Transcriptional and post-transcriptional plant gene silencing in response to a pathogen. Science 279, 2113–2115 (1998).

    Article  CAS  Google Scholar 

  9. Covey, S.N., Lomonossoff, G.P. & Hull, R. Characterisation of cauliflower mosaic virus DNA sequences which encode major polyadenylated transcripts. Nucleic Acids Res. 24, 6735–6747 (1981).

    Article  Google Scholar 

  10. Odell, J.T., Nagy, F. & Chua, N-H. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313, 810–812 (1985).

    Article  CAS  Google Scholar 

  11. Benfey, P.N. & Chua, N-H. The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250, 959–966 (1990).

    Article  CAS  Google Scholar 

  12. Shepherd, R.J. DNA plant viruses. Ann. Rev. Plant Physiol. 30, 405–423 (1979).

    Article  CAS  Google Scholar 

  13. Tomlinson, J.A. Epidemiology and control of virus diseases of vegetables. Ann. Appl. Biol. 110, 661–681 (1987).

    Article  Google Scholar 

  14. Hardwick, N.V., Davies, J.M.L. & Wright, D.M. The incidence of three virus diseases of winter oilseed rape in England and Wales in the 1991/92 and 1992/93 growing seasons. Plant Pathol. 43, 1045–1049 (1994).

    Article  Google Scholar 

  15. Raybould, A.F., Maskell, L.C., Edwards, M.L., Cooper, J.I. & Gray, A.J. The prevalence and spatial distribution of viruses in natural populations of Brassica oleracea. New Phytol. 141, 265–275 (1999).

    Article  Google Scholar 

  16. Jones, J.D.G. et al. Effective vectors for transformation, expression of heterologous and assaying transposon excision in transgenic plants. Transgenic Res. 1, 285–297 (1992).

    Article  CAS  Google Scholar 

  17. Hull, R. Structure of cauliflower mosaic virus genome. III. Restriction endonuclease mapping of thirty-three isolates. Virology 100, 76–90 (1980).

    Article  CAS  Google Scholar 

  18. Al-Kaff, N.S. & Covey, S.N. Biological diversity of cauliflower mosaic virus isolates expressed in two Brassica species. Plant Pathol. 44, 516–526 (1995).

    Article  Google Scholar 

  19. Saunders, K., Lucy, A.P. & Covey, S.N. Susceptibility of Brassica species to cauliflower mosaic virus infection is related to a specific stage in the virus multiplication cycle. J. Gen. Virol. 71, 1641–1647 (1990).

    Article  CAS  Google Scholar 

  20. Covey, S.N., Turner, D.S., Lucy, A.P. & Saunders, K. Host regulation of cauliflower mosaic virus. Proc. Natl. Acad. Sci. USA 87, 1633–1637 (1990).

    Article  CAS  Google Scholar 

  21. Qin, X.F., Holuigue, L., Horvath, D.M. & Chua, N.H. Immediate-early transcription activation by salicylic acid via the cauliflower mosaic virus AS-1 element. Plant Cell 6, 863–874 (1994).

    Article  CAS  Google Scholar 

  22. De Block, M. et al. Engineering herbicide tolerance in plants by expression of a detoxifying enzyme. EMBO J. 6, 2513–2518 (1987).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Non Owen and Chris Jones for producing the transgenic lines and J. Jones for providing the transgene constructs. We also thank R. Hull, C. Jenner, and J. Walsh for CaMV variants, and Mike Hill for treating plants with the herbicide. We gratefully acknowledge funds provided by Food Standards Agency FSA (FS0230) and the BBSRC. The work was carried out under MAFF license PHL 11B/3013(3/1999).

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Correspondence to Nadia S. Al-Kaff.

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Al-Kaff, N., Kreike, M., Covey, S. et al. Plants rendered herbicide-susceptible by cauliflower mosaic virus–elicited suppression of a 35S promoter-regulated transgene. Nat Biotechnol 18, 995–999 (2000). https://doi.org/10.1038/79501

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