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21 - RNAi and gene silencing phenomena mediated by viral suppressors in plants

Published online by Cambridge University Press:  31 July 2009

Ramachandran Vanitharani
Affiliation:
International Laboratory for Tropical Agricultural Biotechnology, Donald Danforth Plant Science Center
Padmanabhan Chellappan
Affiliation:
International Laboratory for Tropical Agricultural Biotechnology, Donald Danforth Plant Science Center
Claude M. Fauquet
Affiliation:
International Laboratory for Tropical Agricultural Biotechnology, Donald Danforth Plant Science Center
Krishnarao Appasani
Affiliation:
GeneExpression Systems, Inc., Massachusetts
Andrew Fire
Affiliation:
Stanford University, California
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Summary

Introduction

Posttranscriptional gene silencing (PTGS) is a natural, universal mechanism that degrades both cellular and viral mRNA in a homology-dependant manner in diverse eukaryotes, and has now become a major area of research and development in both plants and animals. It was first discovered in plants (Napoli et al., 1990), while a mechanistically similar phenomenon is known to occur in a wide range of organisms, including Caenorhabditis elegans, Drosophila melanogaster and mammals termed RNA-interference (RNAi) (Fire et al., 1998, Hammond et al., 2000) and in Neurospora crassa termed quelling (Cogoni and Macino, 1997). Transgenes and viruses can induce PTGS in plants, and it is now recognized as a natural defense mechanism against virus infection (Hamilton and Baulcombe, 1999). Recent studies at the molecular level revealed that all of these phenomena are considered as manifestations of a general RNA-targeting pathway (Vance and Vaucheret, 2001). The mechanism by which a virus infection triggers PTGS in plants is not fully understood, but it is evident that dsRNA is a strong inducer of PTGS (Waterhouse et al., 2001). Such dsRNA molecules are produced during RNA virus replication using their own RNA-dependent RNA polymerase (RdRP), or alternatively host RdRPs convert any “aberrant” ssRNA in the cell, from viral origin or cell origin, into dsRNA (Dalmay et al., 2000; Ahlquist, 2002). The biology and biochemistry of RNAi was discussed in detail in Section I of this book.

Type
Chapter
Information
RNA Interference Technology
From Basic Science to Drug Development
, pp. 280 - 300
Publisher: Cambridge University Press
Print publication year: 2005

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References

Abel, P. P., Nelson, R. S., De, B., Hoffmann, N., Rogers, S. G., Fraley, R. T., and Beachy, R. N., (1986). Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science, 232, 738–743CrossRefGoogle ScholarPubMed
Ahlquist, P., (2002). RNA-dependent RNA polymerases, viruses, and RNA silencing. Science, 296, 1270–1273CrossRefGoogle ScholarPubMed
Anandalakshmi, R., Marathe, R., Ge, X., Herr, J. M. Jr., Mau, C., Mallory, A., Pruss, G., Bowman, L., and Vance, V. B., (2000). A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science, 290, 142–144CrossRefGoogle ScholarPubMed
Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H., and Vance, V. B., (1998). A viral suppressor of gene silencing in plants. Proceedings of the National Academy of Sciences USA, 95, 13079–13084CrossRefGoogle ScholarPubMed
Baulcombe, D. C. (1999). Fast forward genetics based on virus-induced gene silencing. Current Opinion in Plant Biology, 2, 109–113CrossRefGoogle ScholarPubMed
Beclin, C., Berthome, R., Palauqui, J. C., Tepfer, M., and Vaucheret, H., (1998). Infection of tobacco or Arabidopsis plants by CMV counteracts systemic post-transcriptional silencing of nonviral (trans) genes. Virology, 252, 313–317CrossRefGoogle ScholarPubMed
Brigneti, G., Voinnet, O., Li, W., Ji, L., Ding, S., and Baulcombe, D. C. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. European Molecular Biology Organization Journal, 17, 6739–6746CrossRefGoogle ScholarPubMed
Bucher, E., Sijen, T., Haan, P., Goldbach, R., and Prins, M., (2003). Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. Journal of Virology, 77, 1329–1336CrossRefGoogle ScholarPubMed
Chellappan, P., Vanitharani, R., and Fauquet, C. M. (2004a). Short-interfering RNA accumulation correlates with host recovery in DNA virus infected hosts and gene silencing targets specific viral sequences. Journal of Virology, 78, 7465–7477CrossRefGoogle Scholar
Chellappan, P., Masona, M. V., Vanitharani, R., Taylor, N. J. and Fauquet, C. M. (2004b). Broad spectrum resistance to ssDNA viruses associated with transgene-induced gene silencing in cassava. Plant Molecular Biology, In press
Cogoni, C., and Macino, G., (1997). Isolation of quelling-defective (qde) mutants impaired in posttranscriptional transgene-induced gene silencing in Neurospora crassa. Proceedings of the National Academy of Sciences USA, 94, 10233–10238CrossRefGoogle ScholarPubMed
Covey, S. N., Al-Kaff, N. S., Langara, A., and Turner, D. S. (1997). Plants combat infection by gene silencing. Nature, 385, 781–782CrossRefGoogle Scholar
Dalmay, T., Hamilton, A., Rudd, S., Angell, S., and Baulcombe, D. C. (2000). An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell, 101, 543–553CrossRefGoogle Scholar
Depicker, A., and Montagu, M. V. (1997). Post-transcriptional gene silencing in plants. Current Opinion in Cell Biology, 9, 373–382CrossRefGoogle ScholarPubMed
Dong, X., Wezel, R., Stanley, J., and Hong, Y., (2003). Functional characterization of the nuclear localization signal for a suppressor of posttranscriptional gene silencing. Journal of Virology, 77, 7026–7033CrossRefGoogle ScholarPubMed
Dunoyer, P., Pfeffer, S., Fritsch, C., Hemmer, O., Voinnet, O., and Richards, K. E., (2002). Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant Journal, 29, 555–567CrossRefGoogle ScholarPubMed
Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T., (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature, 411, 494–498CrossRefGoogle ScholarPubMed
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, 179–188CrossRefGoogle ScholarPubMed
Fauquet, C. M. and Stanley, J. (2003). Geminivirus classification and nomenclature: Progress and problems. Annals of Applied Biology, 142, 165–189CrossRefGoogle Scholar
Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806–811CrossRefGoogle ScholarPubMed
Fondong, V. N., Pita, J. S., Rey, M. E., Kochko, A., Beachy, R. N. and Fauquet, C. M. (2000). Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. Journal of General Virology, 81, 287–297CrossRefGoogle Scholar
Gitlin, L., Karelsky, S. and Andino, R. (2002). Short interfering RNA confers intracellular antiviral immunity in human cells. Nature, 418, 430–434CrossRefGoogle ScholarPubMed
Goodwin, J., Chapman, K., Swaney, S., Parks, T. D., Wernsman, E. A. and Dougherty, W. G. (1996). Genetic and biochemical dissection of transgenic RNA-mediated virus resistance. Plant Cell, 8, 95–105CrossRefGoogle ScholarPubMed
Guo, H. and Ding, S. (2002). A viral protein inhibits the long range signaling activity of the gene silencing signal. European Molecular Biology Organization Journal, 21, 398–407CrossRefGoogle Scholar
Hamilton, A. J. and Baulcombe, D. C. (1999). A species of small antisense RNA in posttranscriptional gene silencing in plants. Science, 286, 950–952CrossRefGoogle ScholarPubMed
Hammond, S. M., Bernstein, E., Beach, D. and Hannon, G. J. (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature, 404, 293–6CrossRefGoogle ScholarPubMed
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. Critical Reviews in Plant Sciences, 18, 71–106CrossRefGoogle Scholar
Harrison, B. D., Zhou, X., Otim-Nape, G. W., Liu, Y. and Robinson, D. J. (1997). Role of a novel type of double infection in the geminivirus-induced epidemic of severe cassava mosaic in Uganda. Annals of Applied Biology, 131, 437–448CrossRefGoogle Scholar
Jones, A. L., Thomas, C. L. and Maule, A. J. (1998). De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. European Molecular Biology Organization Journal, 17, 6385–6393CrossRefGoogle ScholarPubMed
Jorgensen, R. (1992). Silencing of plant genes by homologous transgenes. Agbiotech News and Information, 4, 265N–273NGoogle Scholar
Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A. and Carrington, J. C. (2003). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Developmental Cell, 4, 205–217CrossRefGoogle Scholar
Kasschau, K. D. and Carrington, J. C. (1998). A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell, 95, 461–470CrossRefGoogle ScholarPubMed
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. The Plant Journal: for Cell and Molecular Biology, 14, 91–100CrossRefGoogle ScholarPubMed
Klahre, U., Crete, P., Leuenberger, S. A., Iglesias, V. A. and Meins, F. Jr. (2002). High molecular weight RNAs and small interfering RNAs induce systemic posttranscriptional gene silencing in plants. Proceedings of the National Academy of Sciences USA, 99, 11981–11986CrossRefGoogle ScholarPubMed
Kumagai, M. H., Donson, J., Della-Cioppa, G., Harvey, D., Hanley, K. and Grill, L. K. (1995). Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proceedings of the National Academy of Sciences USA, 92, 1679–1683CrossRefGoogle ScholarPubMed
Li, H., Li, W. X. and Ding, S. W. (2002). Induction and suppression of RNA silencing by an animal virus. Science, 296, 1319–1321CrossRefGoogle ScholarPubMed
Li, H., Lucy, A. P., Guo, H., Li, W., Ji, L., Wong, S. and Ding, S. (1999). Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism. European Molecular Biology Organization Journal, 18, 2683–2691CrossRefGoogle ScholarPubMed
Lindbo, J. A. and Dougherty, W. G. (1992). Pathogen-derived resistance to a potyvirus: Immune and resistant phenotypes in transgenic tobacco expressing altered forms of a potyvirus coat protein nucleotide sequence. Molecular Plant Microbe Interactions, 5, 144–153CrossRefGoogle ScholarPubMed
Llave, C., Kasschau, K. D. and Carrington, J. C. (2000). Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proceedings of the National Academy of Sciences USA, 97, 13401–13406CrossRefGoogle ScholarPubMed
Lucioli, A., Noris, E., Brunetti, A., Tavazza, R., Ruzza, V., Castillo, A. G., Bejarano, E. R., Accotto, G. P. and Tavazza, M. (2003). Tomato yellow leaf curl Sardinia virus rep-derived resistance to homologous and heterologous geminiviruses occurs by different mechanisms and is overcome if virus-mediated transgene silencing is activated. Journal of Virology, 77, 6785–6798CrossRefGoogle ScholarPubMed
Mallory, A. C., Reinhart, B. J., Bartel, D., Vance, V. B. and Bowman, L. H. (2002). A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proceedings of the National Academy of Sciences USA, 99, 15228–15233CrossRefGoogle ScholarPubMed
Mette, M. F., Winden, J. V. D., Matzke, M. A. and Matzke, A. J. M. (1999). Production of aberrant promoter transcripts contributes to methylation and silencing of unlinked homologous promoters in trans. European Molecular Biology Organization Journal, 18, 241–248CrossRefGoogle ScholarPubMed
Napoli, C., Lemieux, C. and Jorgensen, R. (1990). Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell, 2, 279–289CrossRefGoogle ScholarPubMed
Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C. and Weigel, D. (2003). Control of leaf morphogenesis by microRNAs. Nature, 425, 257–263CrossRefGoogle ScholarPubMed
Palauqui, J. C., Elmayan, T., Pollien, J. M. and Vaucheret, H. (1997). Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. European Molecular Biology Organization Journal, 16, 4738–4745CrossRefGoogle ScholarPubMed
Peele, C., Jordan, C. V., Muangsan, N., Turnage, M., Egelkrout, E., Eagle, P., Hanley-Bowdoin, L. and Robertson, D. (2001). Silencing of a meristematic gene using geminivirus-derived vectors. The Plant Journal: for Cell and Molecular Biology, 27, 357–366CrossRefGoogle ScholarPubMed
Pfeffer, S., Dunoyer, P., Heim, F., Richards, K. E., Jonard, G. and Ziegler-Graff, V., (2002). P0 of beet Western yellows virus is a suppressor of posttranscriptional gene silencing. Journal of Virology, 76, 6815–6824CrossRefGoogle ScholarPubMed
Pinto, Y. M., Kok, R. A. and Baulcombe, D. C. (1999). Resistance to rice yellow mottle virus (RYMV) in cultivated African rice varieties containing RYMV transgenes. Nature Biotechnology, 17, 702–707CrossRefGoogle ScholarPubMed
Pita, J. S., Fondong, V. N., Sangare, A., Otim-Nape, G. W., Ogwal, S. and Fauquet, C. M. (2001). Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. Journal of General Virology, 82, 655–665CrossRefGoogle ScholarPubMed
Plasterk, R. H. (2002). RNA silencing: The genome's immune system. Science, 296, 1263–1265CrossRefGoogle ScholarPubMed
Pruss, G., Ge, X., Shi, X. M., Carrington, J. C. and Vance, V. B. (1997). Plant viral synergism: The potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell, 9, 859–868CrossRefGoogle ScholarPubMed
Qu, F., Ren, T. and Morris, T. J. (2003). The coat protein of Turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. Journal of Virology, 77, 511–522CrossRefGoogle ScholarPubMed
Ratcliff, F., Harrison, B. D. and Baulcombe, D. C. (1997). A similarity between viral defense and gene silencing in plants. Science, 276, 1558–1560CrossRefGoogle ScholarPubMed
Ratcliff, F., Martin-Hernandez, A. M. and Baulcombe, D. C. (2001). Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant Journal, 25, 237–245CrossRefGoogle ScholarPubMed
Ratcliff, F. G., MacFarlane, S. A. and Baulcombe, D. C. (1999). Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell, 11, 1207–1215CrossRefGoogle ScholarPubMed
Reed, J. C., Kasschau, K. D., Prokhnevsky, A. I., Gopinath, K., Pogue, G. P., Carrington, J. C. and Dolja, V. V. (2003). Suppressor of RNA silencing encoded by Beet yellows virus. Virology, 306, 203–209CrossRefGoogle ScholarPubMed
Ruiz, M. T., Voinnet, O. and Baulcombe, D. C. (1998). Initiation and maintenance of virus-induced gene silencing. Plant Cell, 10, 937–946CrossRefGoogle ScholarPubMed
Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. A. and Fire, A. (2001). On the role of RNA amplification in dsRNA-triggered gene silencing. Cell, 107, 465–476CrossRefGoogle ScholarPubMed
Silhavy, D., Molnar, A., Lucioli, A., Szittya, G., Hornyik, C., Tavazza, M. and Burgyan, J. (2002). A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. European Molecular Biology Organization Journal, 21, 3070–3080CrossRefGoogle ScholarPubMed
Stanley, J. (1983). Infectivity of the cloned geminivirus genome requires sequences from both DNAs. Nature, 305, 643–645CrossRefGoogle Scholar
Szittya, G., Silhavy, D., Molnar, A., Havelda, Z., Lovas, A., Lakatos, L., Banfalvi, Z. and Burgyan, J. (2003). Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. European Molecular Biology Organization Journal, 22, 633–640CrossRefGoogle ScholarPubMed
Turnage, M. A., Muangsan, N., Peele, C. G. and Robertson, D. (2002). Geminivirus-based vectors for gene silencing in Arabidopsis. The Plant Journal: for Cell and Molecular Biology, 30, 107–114CrossRefGoogle ScholarPubMed
Tuschl, T., Zamore, P. D., Lehmann, R., Bartel, D. P. and Sharp, P. A. (1999). Targeted mRNA degradation by double-stranded RNA in vitro. Genes & Development, 13, 3191–3197CrossRefGoogle ScholarPubMed
Wezel, R., Dong, X., Liu, H., Tien, P., Stanley, J. and Hong, Y. (2002). Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression. Molecular Plant-Microbe Interactions: Mpmi 15, 203–208CrossRefGoogle Scholar
Vance, V. and Vaucheret, H. (2001). RNA silencing in plants – defense and counterdefense. Science, 292, 2277–2280CrossRefGoogle ScholarPubMed
Vanitharani, R., Chellappan, P. and Fauquet, C. M. (2003). Short interfering RNA-mediated interference of gene expression and viral DNA accumulation in cultured plant cells. Proceedings of the National Academy of Sciences USA, 100, 9632–9636CrossRefGoogle ScholarPubMed
Vanitharani, R., Chellappan, P., Pita, J. S. and Fauquet, C. M. (2004). Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and posttranscriptional gene silencing suppression. Journal of Virology, In press
Voinnet, O. and Baulcombe, D. C. (1997). Systemic signalling in gene silencing. Nature, 389, 553CrossRefGoogle ScholarPubMed
Voinnet, O., Lederer, C. and Baulcombe, D. C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell, 103, 157–167CrossRefGoogle ScholarPubMed
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. Proceedings of the National Academy of Sciences USA, 96, 14147–14152CrossRefGoogle Scholar
Waterhouse, P. M., Graham, M. W. and Wang, M. (1998). Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proceedings of the National Academy of Sciences USA, 95, 13959–13964CrossRefGoogle ScholarPubMed
Waterhouse, P. M., Wang, M. and Lough, T. (2001). Gene silencing as an adaptive defence against viruses. Nature, 411, 834–842CrossRefGoogle ScholarPubMed
Yelina, N. E., Savenkov, E. I., Solovyev, A. G., Morozov, S. Y. and Valkonen, J. P. (2002). Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei- and potyviruses: complementary functions between virus families. Journal of Virology, 76, 12981–12991CrossRefGoogle ScholarPubMed
Zaitlin, M., Anderson, J. M., Perry, K. L., Zhang, L. and Palukaitis, P. (1994). Specificity of replicase-mediated resistance to cucumber mosaic virus. Virology, 201, 200–205CrossRefGoogle ScholarPubMed

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