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Plant DNA viruses and gene silencing

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Abstract

Gene silencing is a multifaceted phenomenon leading to propagative down-regulation of gene expression. Gene silencing, first observed in plants containing transgenes, can operate both at the transcriptional and post-transcriptional levels. Silencing effects can be triggered by nuclear transgenes and by cytoplasmic RNA viruses, and it can be propagated between these elements and endogenous plant genes that share sequence homology. Although some aspects of gene silencing are becoming better understood, little is yet known about the relationship between nuclear and cytoplasmic events. Plant DNA viruses – both the ssDNA geminiviruses and the reverse-transcribing pararetroviruses – have properties with the potential to initiate gene silencing in the nucleus and in the cytoplasm. Characteristics include production of multiple copies of viral DNA genomes in the nucleus, illegitimate integration of viral DNA into host chromosomes mimicking transgene transformation, and generation of abundant viral RNAs in the cytoplasm. Evidence is emerging that geminiviruses and plant pararetroviruses can interact with the gene silencing system either from introduced DNA constructs or during viral pathogenesis. Some observations suggest there are complex relationships between DNA viral activity, transcriptional and post-transcriptional gene silencing mechanisms. DNA viruses also have properties consistent with an ability to counteract the plant silencing response. In this article, features of plant DNA viruses are discussed in relation to gene silencing phenomena, and the prospects for understanding the interaction between nuclear and cytoplasmic silencing processes.

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References

  • Ach, R.A., Durfee, T., Miller, A.B., Taranto, P., Hanley-Bowdoin, L., Zambryski, P.C. and Gruissem, W. 1997. RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Mol. Cell. Biol. 17: 5077–5086.

    PubMed  Google Scholar 

  • Al-Kaff, N.S. and Covey S.N. 1995. Biological diversity of cauliflower mosaic virus isolates expressed in two Brassica species. Plant Path. 44: 516–526.

    Google Scholar 

  • Al-Kaff, N.S. and Covey, S.N. 1996. Unusual accumulations of cauliflower mosaic virus in local lesions, dark green leaf tissue and roots of infected plants. Mol. Plant-Microbe Interact. 9: 357–363.

    Google Scholar 

  • Al-Kaff, N.S., Covey, S.N., Kreike, M., Page, A., Pinder, R. and Dale, P. 1998. Transcriptional and posttranscriptional plant gene silencing in response to a pathogen. Science 279: 2113–2115.

    PubMed  Google Scholar 

  • Ashby, M.K., Warry, A., Bejarano, E.R., Khashoggi, A., Burrell, M. and Lichtenstein, C.P. 1997. Analysis of multiple copies of geminiviral DNA in the genome of four closely related Nicotiana species suggest a unique integration event. Plant Mol. Biol. 35: 313–321.

    PubMed  Google Scholar 

  • Atkinson, R.G., Bielski, L.R.F., Gleave, A.P., Janssen, B.-J. and Morris, B.A.M. 1998. Post-transcriptional silencing of chalcone synthse in petunia using a geminivirus-based episomal vector. Plant J. 15: 593–604.

    Google Scholar 

  • Baughman, G.A., Jacobs, J.D. and Howell, S.H. 1988. Cauliflower mosaic virus geneVI produces a symptomatic phenotype in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 85: 733–737.

    Google Scholar 

  • Bejarano, E.R., Khashoggi, A., Witty, M. and Lichtenstein, C. 1996. Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proc. Natl. Acad. Sci. USA 93: 759–764.

    PubMed  Google Scholar 

  • Benfey, P.N. and Chua, N.H. 1990. The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250: 959–966.

    Google Scholar 

  • Brough, C.L., Gardiner, W.E., Inamdar, N.M., Zhang, X.Y., Ehrlich, M. and Bisaro, D.M. 1992. DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol. Biol. 18: 703–712.

    PubMed  Google Scholar 

  • Carrington, J.C. and Whitham, S. A. 1998. Viral invasion and host defense: strategies and counter-strategies. Curr. Opin. Plant Biol. 1: 336–341.

    PubMed  Google Scholar 

  • Cecchini, E., Gong, Z., Geri, C., Covey, S.N. and Milner, J.J. 1997. Transgenic Arabidopsis expressing gene VI from cauliflower mosaic virus variants exhibits a range of symptom-like phenotypes and accumulates inclusion bodies. Mol. Plant-Microbe Interact 10: 1094–1101.

    PubMed  Google Scholar 

  • Covey, S. N. and Turner, D.S. 1993. Changes in populations of cauliflower mosaic virus DNA and RNA forms during turnip callus proliferation. J. Gen. Virol. 74: 1887–1893.

    PubMed  Google Scholar 

  • Covey, S.N., Lomonossoff, G.P. and Hull, R. 1981. Characterisation of cauliflower mosaic virus DNA sequences which encode major polyadenylated transcripts. Nucl. Acids Res. 9: 6735–6747.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Covey, S.N., Al-Kaff, N.S., Langara, A. and Turner, D.S. 1997. Plants combat infection by gene silencing. Nature 385: 781–782.

    Google Scholar 

  • Covey, S.N., McCallum, D.G., Turner, D.S., Al-Kaff, N.S., Dale, P., Cecchini, E. and Milner, J.J. 2000. Parararetrovirus-crucifer interactions: attack and defence or modus vivendi? Mol. Plant Path. 1: 77–86.

    Google Scholar 

  • Daubert, S. 1988. Sequence determinants of symptoms in the genomes of plant viruses. Mol. Plant-Microbe Interact. 1: 317–325.

    PubMed  Google Scholar 

  • Dougherty, W.G. and Parks, T.D. 1995. Transgenes and gene suppression: telling us something new? Curr. Opin. Cell Biol. 7: 399–405.

    PubMed  Google Scholar 

  • Duan, Y.-P., Powell, C.A., Webb, S.E., Purcifull, D.E. and Hiebert, E. 1997. Geminivirus resistance in transgenic tobacco expressing mutated BC1 protein. Mol. Plant-Microbe Interact. 10: 617–623.

    Google Scholar 

  • Elmayan, T. and Vaucheret, H. 1996. Expression of single copies of a strongly expressed 35S transgene can silence posttranscriptionally. Plant J. 9: 787–797.

    Google Scholar 

  • English, J.J., Mueller, E. and Baulcombe, D.C. 1996. Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8: 179–188.

    Article  PubMed  Google Scholar 

  • Ermak, G., Paszkowski, U., Wohlmuth, M., Scheid, O.M. and Paszkowski, J. 1993. Cytosine methylation inhibits replication of African cassava mosaic virus by two distinct mechanisms. Nucl. Acids Res. 21: 3445–3450.

    PubMed  Google Scholar 

  • Fire, A. 1999. RNA-triggered gene silencing. Trends Genet. 15: 358–363.

    PubMed  Google Scholar 

  • Hamilton, A.J. and Baulcombe, D.C. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286: 950–952.

    PubMed  Google Scholar 

  • Hanley-Bowdoin, L., Settlage, S.B., Orozco, B.M., Nagar, S. and Robertson, D. 1999. Geminiviruses: models for plant DNA replication, transcription and cell cycle regulation. Crit. Rev. Plant Sci. 18: 71–106.

    Google Scholar 

  • Harper, G., Osuji. J.O., Heslop-Harrison, J.S. and Hull, R. 1999. Integration of banana streak badnavirus into the Musa genome: molecular and cytogenetic evidence. Virology 255: 207–213.

    PubMed  Google Scholar 

  • Hayes, R.J., Petty, I.T.D., Coutts, R.H.A. and Buck, K.W. 1988. Gene amplification and expression in plants by a replicating geminivirus vector. Nature 334: 179–182.

    Article  Google Scholar 

  • Hohn T. and Fütterer, J. 1997. The proteins and functions of plant pararetroviruses: knowns and unknowns. Crit. Rev. Plant Sci. 16: 133–161.

    Google Scholar 

  • Hong, Y.G. and Stanley, J. 1996. Virus resistance in Nicotiana benthamiana conferred by African cassava mosaic virus replicationassociated protein (AC1) transgene. Mol. Plant-Microbe Interact. 9: 219–225.

    Google Scholar 

  • Hong, Y., Saunders, K., Hartley, M.R., and Stanley, J. 1996. Resistance to geminivirus infection by virus-induced expression of dianthin in transgenic plants. Virology 220: 119–127.

    PubMed  Google Scholar 

  • Hong, Y.G., Saunders, K. and Stanley, J. 1997. Transactivation of dianthin transgene expression by African cassava mosaic virus AC2. Virology 228: 383–387.

    PubMed  Google Scholar 

  • Howell, S.H. 1985. The molecular biology of plant DNA viruses. Crit. Rev. Plant Sci. 2: 287–316.

    Google Scholar 

  • Hull, R. 1999. Classification of reverse transcribing elements: a discussion document. Arch. Virol. 144: 209–214.

    PubMed  Google Scholar 

  • Hull, R. and Covey, S.N. 1996. Retroelements: propagation and adaptation. Virus Genes 11: 105–118.

    Google Scholar 

  • Jakowitsch, J., Mette, M.F., van der Winden, J., Matzke, M.A. and Matzke, A.J.M. 1999. Integrated pararetroviral sequences define a unique class of dispersed repetitive DNA in plants. Proc. Natl. Acad. Sci. USA 96: 13241–13246.

    PubMed  Google Scholar 

  • Jorgensen, R.A., Atkinson, R.G., Forster, R.L.S. and Lucas, W.J. 1998. An RNA-based information superhighway in plants. Science 279: 1486–1487.

    PubMed  Google Scholar 

  • Kjemtrup, S., Sampson, K.S., Peele, C.G., Nguyen, L.V., Conkling, M.A., Thompson, W.F. and Robertson, D. 1998. Gene silencing from plant DNA carried by a geminivirus. Plant J. 14: 91–100.

    PubMed  Google Scholar 

  • Kooter, J.M., Matzke, M.A. and Meyer, P. 1999. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci. 4: 340–347.

    PubMed  Google Scholar 

  • Kunik, T., S alomon, R., Zamir, D., Navot, N., Zeidan, M., Michelson, I. and Gafni, Y. 1994. Transgenic tomato plants expressing the tomato yellow leaf curl virus capsid protein are resistant to the virus. Bio/technology 12: 500–504.

    PubMed  Google Scholar 

  • Kupiec, J.-J. and Sonigo, P. 1996. Reverse transcriptase jumps and gaps. J. Gen. Virol. 77: 1987–1991.

    PubMed  Google Scholar 

  • Latham, J.R., Saunders, K., Pinner, M.S. and Stanley, J. 1997. Induction of plant cell division by beet curly top virus gene C4. Plant J. 11: 1273–1283.

    Google Scholar 

  • Leclerc, D., Chapdelaine, Y. and Hohn, T. 1999. Nuclear targeting of the cauliflower mosaic virus coat protein. J. Virol. 73: 553–560.

    PubMed  Google Scholar 

  • Lomonossoff, G.P. 1995. Pathogen-derived resistance to plant viruses. Annu. Rev. Phytopath. 33: 323–343.

    Google Scholar 

  • Matzke, M.A. and Matzke, A.J.M. 1995. How and why do plants inactivate homologous transgenes? Plant Physiol. 107: 679–685.

    PubMed  Google Scholar 

  • Mraz, I., Petrzik. K., Franova-Honetslegrova, J. and Sip, M. 1997. Detection of strawberry vein banding virus by polymerase chain reaction and dot blot hybridization. Acta Virol. 41: 241–242.

    PubMed  Google Scholar 

  • Nagar, S., Pedersen, T.J., Carrick, K., Hanley-Bowdoin, L. and Robertson, D. 1995. A geminivirus induces expression of a host DNA replication protein in terminally differentiated plant cells. Plant Cell 7: 715–719.

    Google Scholar 

  • Ndowora, T., Dahal, G., LaFleur, D., Harper, G., Hull, R., Olszewski, N.E. and Lockhart, B. 1999. Evidence that badnavirus infection in Musa can originate from integrated pararetroviral sequences. Virology 255: 214–220.

    PubMed  Google Scholar 

  • Noad, R.J., Turner, D.S. and Covey, S.N. 1997. Expression of functional elements inserted into the 35S promoter region of infectious cauliflower mosaic virus replicons. Nucl. Acids Res. 25: 1123–1129.

    PubMed  Google Scholar 

  • Noris, E., Accotto, G.P., Tavazza, R., Brunetti, A., Crespi, S. and Tavazza, M. 1996. Resistance to tomato yellow leaf curl geminivirus in Nicotiana benthamiana plants transformed with a truncated C1 gene. Virology 224: 130–138.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Palmer, K.E. and Rybicki, EP. 1997. The use of geminiviruses in biotechnology and plant molecular biology, with particular focus on mastreviruses. Plant Sci. 129: 115–130

    Google Scholar 

  • Porta, C. and Lomonossoff, G.P. 1996. Use of viral replicons for the expression of genes in plants. Mol. Biotechnol. 5: 209–221.

    PubMed  Google Scholar 

  • Qin, X.F., Holuigue, L., Horvath, D.M. and Chua, N.H. 1994. Immediate-early transcription activation by salicylic acid via the cauliflower mosaic-virus as-1 element. Plant Cell 6: 863–874.

    Article  PubMed  Google Scholar 

  • Ratcliff, F.G., Harrison, B.D. and Baulcombe, D.C. 1997. A similarity between viral defense and gene silencing in plants. Science 276: 1588–1560.

    Google Scholar 

  • Rollo, F. and Covey, S. N. 1985. Cauliflower mosaic virus DNA persists as supercoiled forms in cultured turnip cells. J. Gen. Virol. 66: 603–608.

    Google Scholar 

  • Rothnie, H.M., Chaplelaine, Y. and Hohn, T. 1994. Pararetroviruses and retroviruses: a comparative review of viral structure and gene expression strategies. Adv. Virus Res. 44: 1–67.

    PubMed  Google Scholar 

  • Ruiz, M.T., Voinnet, O. and Baulcombe, D.C. 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10: 937–946.

    PubMed  Google Scholar 

  • Sangaré, A., Deng, D., Fauquet, C.M. and Beachy, R.N. 1999. Resistance to African cassava mosaic virus conferred by a mutant of the putative NTP-binding domain of the Rep gene (AC1) in Nicotiana benthamiana. Mol. Biol. Rep. 5: 95–102.

    Google Scholar 

  • Sano, Y., Wada, M., Hashimoto, Y., Matsumoto, T. and Kojima, M. 1998. Sequences of ten circular ssDNA components associated with the milk vetch dwarf virus genome. J. Gen. Virol.79: 3111–3118.

    PubMed  Google Scholar 

  • Saunders, K., Lucy, A.P. and Covey, S.N. 1990. 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.

    PubMed  Google Scholar 

  • Sinisterra, X.H., Polston, J.E., Abouzid, A.M. and Hiebert, E. 1999. Tobacco plants transformed with a modified coat protein of tomato mottle begomovirus show resistance to virus infection. Virology 89: 701–706.

    Google Scholar 

  • Stam, M., de Bruin, R., Kenter, S., van der Hoorn, R.A.L., van Blokland, R., Mol, J.N.M. and Kooter, J.M. 1997. Post-transcriptional silencing of chalcone synthase in Petunia by inverted transgene repeats Plant J. 12: 63–82.

    Google Scholar 

  • Stanley, J., Boulton, M.I. and Davies, J.W. 1999. Geminiviridae, in: Embryonic encyclopedia of Life Sciences. Nature Publishing group, London. Http:/www.els.net/elsonline/html/

    Google Scholar 

  • Tang, W. and Leisner, S. 1998. Methylation of nonintegrated multiple copy DNA in plants. Biochem. Biophys. Res. Comm. 245: 403–406.

    PubMed  Google Scholar 

  • Timmermans, M.C.P., Das, O.P. and Messing, J. 1994. Geminiviruses and their uses as extrachromosomal replicons. Annu. Rev. Plant Physiol. 45: 79–112.

    Google Scholar 

  • Turner, D.S., McCallum, D.G. and Covey, S.N. 1996. The role of the 35S promoter and multiple overlapping domains in the pathogenicity of the pararetrovirus cauliflower mosaic virus. J. Virol. 70: 5414–5421.

    Google Scholar 

  • Vaucheret, H., Béclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J.-B., Mourrain, P., Palauqui, J.-C. and Vernhettes, S. 1998. Transgene-induced gene silencing in plants. Plant J. 16: 651–659.

    PubMed  Google Scholar 

  • Voinnet, O., Pinto, Y.M. and Baulcombe, D. C. 1999. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96: 14147–14152.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Zijlstra, C., Scharer-Hernandez, N., Gal, S. and Hohn, T. 1996. Arabidopsis thaliana expressing the cauliflower mosaic virus ORF-VI transgene has a late flowering phenotype. Virus Genes 13: 5–17.

    PubMed  Google Scholar 

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  1. John Innes Centre, Norwich Research Park, Colney, Norwich, NR4 7UH, UK

    Simon N. Covey & Nadia S. Al-Kaff

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Covey, S.N., Al-Kaff, N.S. Plant DNA viruses and gene silencing. Plant Mol Biol 43, 307–322 (2000). https://doi.org/10.1023/A:1006408101473

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