The potential of virus-induced gene silencing for speeding up functional characterization of plant genes

Genetics and Molecular Research

Volumn 3, Issue 3, 2004, Pages 323-341

  Benedito, Vagner A ^a   Visser, Peter B ^a   Angenent, Gerco C ^a   Krens, Frans A ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Nicotiana benthamiana; Post transcriptional gene silencing; Reverse genetics

Indexed keywords

VIRUS VECTOR;

CONTROLLED STUDY; GENE; GENE FUNCTION; GENE SILENCING; GENETIC ANALYSIS; INOCULATION; METHODOLOGY; MOLECULAR MECHANICS; NONHUMAN; PLANT; PLANT GENETICS; REVIEW; VIRUS;

DNA, VIRAL; FLOWERS; GENE SILENCING; GENES, PLANT; GENETIC VECTORS; GENOMICS; MODELS, GENETIC; PLANT VIRUSES; PLANTS, GENETICALLY MODIFIED; TOBACCO; TRANSCRIPTION, GENETIC; TRANSFORMATION, GENETIC;

LILIOPSIDA; NICOTIANA; NICOTIANA BENTHAMIANA; TRANSPOSONS;

EID: 4844222798     PISSN: 16765680     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (87)

1. Al-Kaff, N.S., Covey, S.N., Kreike, M.M., Page, A.M., Pinder, R. and Dale, P.J. (1998). Transcriptional and post-transcriptional plant gene silencing in response to a pathogen. Science 279: 2113-2115.
2. Angenent, G.C., Linthorst, H.J.M., van Belkum, A.F., Cornelissen, B.J.C. and Bol, J.F. (1986). RNA2 of tobacco rattle virus strain TCM encodes an unexpected gene. Nucleic Acids Res. 14: 4673-4682.
3. Bartel, B. and Bartel, D.P. (2003). MicroRNAs: at the root of plant development? Plant Physiol. 132: 709-717.
4. Bateman, A. (2002). The SGS3 protein involved in PTGS finds a family. BMC Bioinformatics 3: 21-24 [http://www.biomedcentral.com/1471-2105/3/21]. Accessed August 15, 2002.
5. Baulcombe, D.C. (1999). Fast forward genetics based on virus-induced gene silencing. Curr. Opin. Plant Biol. 2: 109-113.
6. Baulcombe, D.C. (2002). An RNA microcosm. Science 297: 2002-2003.
7. Bernstein, E., Caudy, A.A., Hammond, S.M. and Hannon, C.J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
8. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M. and Benning, C. (1998). AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17: 170-180.
9. Brunt, A.A., Crabtree, K., Dallwitz, M.J., Gibbs, A.J., Watson, L. and Zurcher, E.J. (Eds.) (1996). Plant viruses online: descriptions and lists from the VIDE Database [http://biology.anu.edu.au/Groups/MES/vide]. Accessed June 29, 2003.
10. Burton, R.A., Gibeaut, D.M., Bacic, A., Findlay, K., Roberts, K., Hamilton, A., Baulcombe, D.C. and Fincher, G.B. (2000). Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12: 691-705.
11. Cerutti, H. (2003). RNA interference: travelling in the cell and gaining functions? Trends Genet. 19: 39-46.
12. Cerutti, L., Mian, N. and Baterman, A. (2000). Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem. Sci. 25: 481-482.
13. Chen, X., Liu, J., Cheng, Y. and Jia, D. (2002). HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129: 1085-1094.
14. Chuang, C.-F. and Meyerowitz, E.M. (2000). Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97: 4985-4990.
15. Cogoni, C. and Macino, G. (2000). Post-transcriptional gene silencing across kingdoms. Curr. Opin. Genet. Dev. 10: 638-643.
16. Cogoni, C., Romano, N. and Macino, G. (1994). Suppression of gene expression by homologous transgenes. Antonie Leeuwenhoek Int. J. Gen. Mol. Microbiol. 65: 205-209.
17. Covey, S.N., Al-Kaff, N.S., Langara, A. and Turner, D.S. (1997). Plants combat infection by gene silencing. Nature 385: 781-782.
18. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. and Baulcombe, D.C. (2000). An RNA-dependent RNA polymerase gene in Arabidopsis is required for post-transcriptional gene silencing mediated by a transgene but not by a virus. Cell 101: 543-553.
19. Dalmay, T., Horsefield, R., Braunstein, T.H. and Baulcombe, D.C. (2001). SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J. 20: 2069-2077.
20. Demmig-Adams, B. and Adams, W.W. (1992). Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant. Physiol. 43: 599-626.
21. Ding, X. and Nelson, R. (2003). Analysis of gene function in rice by virus-induced RNA silencing. In: Proceedings of the 7th International Congress of Plant Molecular Biology, June 23-28, 2003, Barcelona, 467: W04-11.
22. Elmayan, T., Balzergue, S., Béon, F., Bourdon, V., Daubremet, J., Guénet, Y., Mourrain, P., Palauqui, J.-C., Vernhettes, S., Vialle, T., Wostrikoff, K. and Vaucheret, H. (1998). Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747-1757.
23. English, J.J., Davenport, G.F., Elmayan, T., Vaucheret, H. and Baulcombe, D.C. (1997). Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J. 12: 597-603.
24. Fagard, M., Boutet, S., Morel, J.B., Bellini, C. and Vaucheret, H. (2000). AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl. Acad. Sci. USA 97: 11650-11654.
25. Finnegan, E.J., Margis, R. and Waterhouse, P.M. (2003). Post-transcriptional gene silencing is not compromised in the Arabidopsis CARPEL FACTORY (DICER-LIKE1) mutant, a homolog of Dicer-1 from Drosophila. Curr. Biol. 13: 236-240.
26. Fire, A., Xu, S.Q., 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: 806-811.
27. Golden, T.A., Schauer, S.E., Lang, J.D., Pien, S., Mushegian, A.R., Grossniklaus, U., Meinke, D.W. and Ray, A. (2002). SHORT INTEGUMENTS1/ SUSPENSOR1/ CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol. 130: 808-822.
28. Gosselé, V., Fache, I., Meulewaeter, F., Cornelissen, M. and Metzlaff, M. (2002). SVISS - a novel transient gene silencing system for gene function discovery and validation in tobacco plants. Plant J. 32: 859-866.
29. Guo, S. and Kemphues, K. (1995). par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81: 611-620.
30. Gura, T. (2000). A silence that speaks volumes. Nature 404: 804-808.
31. Hall, I.M., Shankaranarayana, G.D., Noma, K.I., Ayoub, N., Cohen, A. and Grewal, S.I.S. (2002). Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237.
32. Hamilton, A., Voinnet, O., Chappell, L. and Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. EMBO J. 21: 4671-4679.
33. Hamilton, A.J. and Baulcombe, D.C. (1999). A species of small antisense RNA in post-transcriptional gene silencing in plants. Science 286: 950-952.
34. Hammond, S.M., Bernstein, E., Beach, D. and Hannon, C.J. (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404: 293-296.
35. Hammond, S.M., Boettcher, S., Caudy, A.A., Kobayashi, R. and Hannon, C.J. (2001). Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293: 1146-1150.
36. Holzberg, S., Brosio, P., Gross, C. and Pogue, G. (2002). Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J. 30: 315-327.
37. Hunter, C. and Poethig, R.S. (2003). Missing links: miRNAs and plant development. Curr. Opin. Genet. Dev. 13: 372-378.
38. Immink, R.G.H., Hannapel, D.J., Ferrario, S., Busscher, M., Franken, J., Lookeren Campagne, M.M. and Angenent, G.C. (1999). A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126: 5117-5126.
39. Ingelbrecht, I.L., Irvine, J.E. and Mirkov, T.E. (1999). Post-transcriptional gene silencing in transgenic sugarcane. Dissection of homology-dependent virus resistance in a monocot that has a complex polyploid genome. Plant Physiol. 119: 1187-1198.
40. Iyer, L.M., Kumpatla, S.P., Chandrasekharan, M.B. and Hall, T.C. (2000). Transgene silencing in monocots. Plant Mol. Biol. 43: 323-346.
41. Jacobsen, S.E., Running, M.P. and Meyerowitz, E.M. (1999). Disruption of an RNA helicase/RNA III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126: 5231-5243.
42. Jones, L. (2002). Revealing micro-RNAs in plants. Trends Plant Sci. 7: 473-475.
43. Kanno, T., Naito, S. and Shimamoto, K. (2000). Post-transcriptional gene silencing in cultured rice cells. Plant Cell Physiol. 41: 321-326.
44. 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.
45. Krysan, P.J., Young, J.C. and Sussman, M.R. (1999). T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11: 2283-2290.
46. 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. Proc. Natl. Acad. Sci. USA 92: 1679-1683.
47. Lindbo, J.A., Silva-Rosales, L., Proebsting, W.M. and Dougherty, W.G. (1993). Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5: 1749-1759.
48. Lipardi, C., Wei, Q. and Paterson, B.M. (2001). RNAi as random degradative PCR: siRNA primers convert mRNA into dsRNAs that are degraded to generate new siRNAs. Cell 107: 297-307.
49. Liu, Y., Schiff, M. and Dinesh-Kumar, S.P. (2002a). Virus-induced gene silencing in tomato. Plant J. 31: 777-786.
50. Liu, Y., Schiff, M., Marathe, R. and Dinesh-Kumar, S.P. (2002b). Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30: 415-429.
51. MacFarlane, S.A. (1999). Molecular biology of the tobraviruses. J. Gen. Virol. 80: 2799-2807.
52. Maeda, I., Kohara, Y., Yamamoto, M. and Sugimoto, A. (2001). Large-scale analysis of gene function in Caenorhabditis elegans by high throughput RNAi. Curr. Biol. 11: 171-176.
53. Mochizuki, K., Fine, N.A., Fujisawa, T. and Gorovsky, M.A. (2002). Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110: 689-699.
54. Mourrain, P., Béclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J.B., Jouette, D., Lacombe, A.M., Nikic, S., Picault, N., Rémoué, K., Sanial, M., Vo, T.A. and Vaucheret, H. (2000). Arabidopsis SGS2 and SGS3 genes are required for post-transcriptional gene silencing and natural virus resistance. Cell 101: 533-542.
55. Napoli, C., Lemieux, C. and Jorgensen, R. (1990). Introduction of a chimeric chalcone synthase gene into Petunia results in reversible cosuppression of homologous genes in trans. Plant Cell 2: 279-289.
56. Nishikura, K. (2001). A short primer on RNAi: RNA-directed RNA polymerase acts as a key catalyst. Cell 107: 415-418.
57. Nykänen, A., Haley, B. and Zamore, P.D. (2001). ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107: 309-321.
58. 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. EMBO J. 16: 4738-4745. Erratum (1998) 17: 2137.
59. Pal-Bhadra, M., Bhadra, U. and Birchler, J.A. (2002). RNAi related mechanisms affect both transcriptional and post-transcriptional transgene silencing in Drosophila. Mol. Cell. 9: 315-327.
60. Parinov, S., Sevugan, M., Ye, D., Yang, W.C., Kumaran, M. and Sundaresan, V. (1999). Analysis of flanking sequences from dissociation insertion lines: a database for reverse genetics in Arabidopsis. Plant Cell 11: 2263-2270.
61. Park, W., Li, J., Song, R., Messing, J. and Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, an HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12: 1484-1495.
62. Peele, C., Jordan, C.V., Muangsan, N., Turnage, M., Egelkrout, E., Eagle, P., Hanley-Bowdoin, L. and Robertson, D. (2001). Silencing of a meristem gene using geminivirus-derived vectors. Plant J. 27: 357-366.
63. 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. Nat. Biotechnol. 17: 702-707.
64. Ratcliff, F., Harrison, B.D. and Baulcombe, D.C. (1997). A similarity between viral defense and gene silencing in plants. Science 276: 1558-1560.
65. Ratcliff, F., Martin-Hernandez, A.M. and Baulcombe, D. (2001). Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 25: 237-245.
66. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B. and Bartel, D.P. (2002). MicroRNAs in plants. Gene Dev. 16: 1616-1626.
67. Robinson-Beers, K., Pruitt, R.E. and Gasser, C.S. (1992). Ovule development in wild-type Arabidopsis and two female sterile mutants. Plant Cell 4: 1237-1249.
68. Rothstein, S.J., Dimaio, J., Strand, M. and Rice, D. (1987). Stable and inheritable inhibition of the expression of nopaline synthase in tobacco expressing antisense RNA. Proc. Natl. Acad. Sci. USA 84: 8439-8443.
69. Ruiz, M.T., Voinnet, O. and Baulcombe, D.C. (1998). Initiation and maintenance of virus-induced gene silencing. Plant Cell 10: 937-946.
70. Schauer, S.E., Jacobsen, S.E., Meinke, D.W. and Ray, A. (2002). DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci. 7: 487-491.
71. Schiebel, W., Pelissier, T., Riedel, L., Thalmeir, S., Schiebel, R., Kempe, D., Lottspeich, F., Sanger, H.L. and Wassenegger, M. (1998). Isolation of an RNA-directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10: 2087-2101.
72. Schwartz, B.W., Yeung, E.C. and Meinke, D.W. (1994). Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120: 3235-3245.
73. Schweizer, P., Pokorny, J., Schulze-Lefert, P. and Dudler, R. (2000). Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant J. 24: 895-903.
74. Smith, N.A., Singh, S.P., Wang, M.-B., Stoutjesdijk, P.A., Green, A.G. and Waterhouse, P.M. (2000). Total silencing by intron-spliced hairpin RNAs. Nature 407: 319-320.
75. Speulman, E., Metz, P.L.J. van, Arkel, G., Hekkert, P.T.L., Stiekema, W.J. and Pereira, A. (1999). A two-component enhancer-inhibitor transposon mutagenesis system for functional analysis of the Arabidopsis genome. Plant Cell 11: 1853-1866.
76. Tang, G., Reinhart, B.J., Bartel, D.P. and Zamore, P.D. (2003). A biochemical framework for RNA silencing in plants. Gene Dev. 17: 49-63.
77. Taverna, S., Coyne, R. and Allis, C. (2002). Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110: 701-711.
78. Thomas, C.L., Jones, L., Baulcombe, D.C. and Maule, A.J. (2001). Size constraints for targeting post-transcriptional gene silencing and for RNA-directed methylation in Nicotiana benthamiana using a potato virus X vector. Plant J. 25: 417-425.
79. Turnage, M.A., Muangsan, N., Peele, C.G. and Robertson, D. (2002). Geminivirus-based vectors for gene silencing in Arabidopsis. Plant J. 30: 107-114.
80. Vaistij, F.E., Jones, L. and Baulcombe, D.C. (2002). Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA dependent RNA polymerase. Plant Cell 14: 857-867.
81. van der Krol, A.R., Mur, L.A., Beld, M., Mol, J.N.M. and Stuitje, A.R. (1990). Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2: 291-299.
82. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I.S. and Martienssen, R.A. (2002). Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837.
83. Wang, E. and Wagner, G.J. (2003). Elucidation of the functions of genes central to diterpene metabolism in tobacco trichomes using post-transcriptional gene silencing. Planta 216: 686-691.
84. Waterhouse, P.M., Wang, M.-B. and Lough, T. (2001). Gene silencing as an adaptive defence against viruses. Nature 411: 834-842.
85. Xu, J., Schubert, J. and Altpeter, F. (2001). Dissection of RNA-mediated ryegrass mosaic virus resistance in fertile transgene perennial ryegrass (Lolium perenne L.). Plant J. 26: 265-274.
86. Zamore, P.D., Tuschl, T., Sharp, P.A. and Bartel, D.P. (2000). RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101: 25-33.
87. Zilberman, D., Cao, X. and Jacobsen, S.E. (2003). ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719.