Skip to main content

Milestones in the Development and Applications of Plant Virus Vector as Gene Silencing Platforms

  • Chapter
  • First Online:
Book cover Plant Viral Vectors

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 375))

Abstract

One of the main post-genomics challenges facing scientists remains the identification of gene function in a large number of plant species. Plant viruses offer great potential in linking genes to phenotypes through epigenetic expression or knockdown of selected genes. The past decade has seen the development and ever increasing applications of a gene knockdown technique termed virus-induced gene silencing (VIGS). VIGS recapitulates an RNA-mediated antiviral defense mechanism, mediating a homology-based post-transcriptional degradation of selected plant RNAs, leading to a loss-of-function phenotype. Due to its rapidity and increasing number of virus vectors developed as gene silencing platforms, VIGS has become a powerful technology to determine the function of genes in an increasing number of crop species, where the routinely available transgenesis or mutagenesis approaches are often not amenable to large genomes and complex genetic backgrounds.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Al-Kaff NS, Covey SN, Kreike MM, Page AM, Pinder R, Dale PJ (1998) Transcriptional and posttranscriptional plant gene silencing in response to a pathogen. Science 279:2113–2115

    Article  PubMed  CAS  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280

    Article  PubMed  CAS  Google Scholar 

  • Bruun-Rasmussen M, Madsen CT, Jessing S, Albrechtsen M (2007) Stability of Barley stripe mosaic virus-induced gene silencing in barley. Mol Plant Microbe Interact 20:1323–1331

    Article  PubMed  CAS  Google Scholar 

  • Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–746

    Article  PubMed  CAS  Google Scholar 

  • Cakir C, Gillespie ME, Scofield SR (2010) Rapid determination of gene function by virus-induced gene silencing in wheat and barley. Crop Sci 50:S77–S84

    Article  CAS  Google Scholar 

  • Constantin GD, Grønlund M, Johansen IE, Stougaard J, Lund OS (2008) Virus-induced gene silencing (VIGS) as a reverse genetic tool to study development of symbiotic root nodules. Mol Plant Microbe Interact 21:720–727

    Article  PubMed  CAS  Google Scholar 

  • Ding XS, Schneider WL, Chaluvadi SR, Mian MA, Nelson RS (2006) Characterization of a Brome mosaic virus strain and its use as a vector for gene silencing in monocotyledonous hosts. Mol Plant Microbe Interact 19:1229–1239

    Article  PubMed  CAS  Google Scholar 

  • Donaire L, Barajas D, Martínez-García B, Martínez-Priego L, Pagán I, Llave C (2008) Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J Virol 82:5167–5177

    Article  PubMed  CAS  Google Scholar 

  • Dong Y, Burch-Smith TM, Liu Y, Mamillapalli P, Dinesh-Kumar SP (2007) A ligation-independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral development. Plant Physiol 145:1161–1170

    Article  PubMed  CAS  Google Scholar 

  • Dunoyer P, Voinnet O (2005) The complex interplay between plant viruses and host RNA-silencing pathways. Curr Opin Plant Biol 8:415–423

    Article  PubMed  CAS  Google Scholar 

  • Dubreuil G, Magliano M, Dubrana MP, Lozano J, Lecomte P, Favery B, Abad P, Rosso MN (2009) Tobacco rattle virus mediates gene silencing in a plant parasitic root-knot nematode. J Exp Bot 60:4041–4050

    Article  PubMed  CAS  Google Scholar 

  • Faivre-Rampant O, Gilroy EM, Hrubikova K, Hein I, Millam S, Loake GJ, Birch P, Taylor M, Lacomme C (2004) Potato virus X-induced gene silencing in leaves and tubers of potato. Plant Physiol 134:1308–1316

    Article  PubMed  CAS  Google Scholar 

  • Fitzmaurice WP, Holzberg S, Lindbo JA, Padgett HS, Palmer KE, Wolfe GM, Pogue GP (2002) Epigenetic modification of plants with systemic RNA viruses. OMICS 6:137–151

    Article  PubMed  CAS  Google Scholar 

  • Fofana IB, Sangaré A, Collier R, Taylor C, Fauquet CM (2004) A geminivirus-induced gene silencing system for gene function validation in cassava. Plant Mol Biol 56:613–624

    Article  PubMed  CAS  Google Scholar 

  • Fu DQ, Zhu BZ, Zhu HL, Jiang WB, Luo YB (2005) Virus-induced gene silencing in tomato fruit. Plant J 43:299–308

    Article  PubMed  CAS  Google Scholar 

  • Fulci V, Macino G (2007) Quelling: post-transcriptional gene silencing guided by small RNAs in Neurospora crassa. Curr Opin Microbiol 10:199–203

    Article  PubMed  CAS  Google Scholar 

  • Gilroy EM, Hein I, van der Hoorn R, Boevink PC, Venter E, McLellan H, Kaffarnik F, Hrubikova K, Shaw J, Holeva M, López EC, Borras-Hidalgo O, Pritchard L, Loake GJ, Lacomme C, Birch PR (2007) Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 52:1–13

    Article  PubMed  CAS  Google Scholar 

  • Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant-Microbe Interact 21:1015–1026

    Article  PubMed  CAS  Google Scholar 

  • Gosselé V, Faché I, Meulewaeter F, Cornelissen M, Metzlaff M (2002) SVISS—a novel transient gene silencing system for gene function discovery and validation in tobacco plants. Plant J 32:859–866

    Article  PubMed  Google Scholar 

  • Grishok A (2005) RNAi mechanisms in caenorhabditis elegans. FEBS Lett 579:5932–5939

    Article  PubMed  CAS  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    Article  PubMed  CAS  Google Scholar 

  • Hein I, Barciszewska-Pacak M, Hrubikova K, Williamson S, Dinesen M, Soenderby IE, Sundar S, Jarmolowski A, Shirasu K, Lacomme C (2005) Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiol 138:2155–2164

    Article  PubMed  CAS  Google Scholar 

  • Herr AJ, Molnàr A, Jones A, Baulcombe DC (2006) Defective RNA processing enhances RNA silencing and influences flowering of arabidopsis. Proc Natl Acad Sci U S A 103:14994–15001

    Article  PubMed  CAS  Google Scholar 

  • Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22:4523–4533

    Article  PubMed  CAS  Google Scholar 

  • Hiriart JB, Aro EM, Lehto K (2003) Dynamics of the VIGS-mediated chimeric silencing of the Nicotiana benthamiana ChlH gene and of the tobacco mosaic virus vector. Mol Plant Microbe Interact 16:99–106

    Article  PubMed  CAS  Google Scholar 

  • Ho T, Pallett D, Rusholme R, Dalmay T, Wang H (2006) A simplified method for cloning of short interfering RNAs from Brassica juncea infected with Turnip mosaic potyvirus and Turnip crinkle carmovirus. J Virol Methods 136:217–223

    Article  PubMed  CAS  Google Scholar 

  • Ho T, Wang H, Pallett D, Dalmay T (2007) Evidence for targeting common siRNA hotspots and GC preference by plant dicer-like proteins. FEBS Lett 581:3267–3272

    Article  PubMed  CAS  Google Scholar 

  • Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J 30:315–327

    Article  PubMed  CAS  Google Scholar 

  • Igarashi A, Yamagata K, Sugai T, Takahashi Y, Sugawara E, Tamura A, Yaegashi H, Yamagishi N, Takahashi T, Isogai M, Takahashi H, Yoshikawa N (2009) Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology 386:407–416

    Article  PubMed  CAS  Google Scholar 

  • Karrer EE, Beachy RN, Holt CA (1998) Cloning of tobacco genes that elicit the hypersensitive response. Plant Mol Biol 36:681–690

    Article  PubMed  CAS  Google Scholar 

  • Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A Jr, Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci U S A 103:18002–18007

    Article  PubMed  CAS  Google Scholar 

  • Kerényi Z, Mérai Z, Hiripi L, Benkovics A, Gyula P, Lacomme C, Barta E, Nagy F, Silhavy D (2008) Inter-kingdom conservation of mechanism of nonsense-mediated mRNA decay. EMBO J 27:1585–1595

    Article  PubMed  Google Scholar 

  • Kjemtrup S, Sampson KS, Peele CG, Nguyen LV, Conkling MA, Thompson WF, Robertson D (1998) Gene silencing from plant DNA carried by a geminivirus. Plant J 14:91–100

    Article  PubMed  CAS  Google Scholar 

  • Kumagai MH, Donson J, della-Cioppa G, Harvey D, Hanley K, Grill LK (1995) Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc Natl Acad Sci U S A 92:1679–1683

    Article  PubMed  CAS  Google Scholar 

  • Lacomme C, Hrubikova K, Hein I (2003) Enhancement of virus-induced gene silencing through viral-based production of inverted-repeats. Plant J 34:543–553

    Article  PubMed  CAS  Google Scholar 

  • Lacomme C, Pogue GP, Wilson TMA, Santa Cruz S (2001) Plant viruses. In: Ring CJA, Blair E (eds) Genetically engineered viruses: development and applications. BIOS Scientific Publishing Limited, Oxford

    Google Scholar 

  • Lacomme C, Santa Cruz S (1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci U S A 96:7956–7961

    Article  PubMed  CAS  Google Scholar 

  • Lindbo JA, Dougherty WG (1992) Pathogen-derived resistance to a potyvirus: immune and resistant phenotypes in transgenic tobacco expressing altered forms of a potyvirus coat protein nucleotide sequence. Mol Plant Microbe Interact 5:144–153

    Article  PubMed  CAS  Google Scholar 

  • Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG (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

    PubMed  CAS  Google Scholar 

  • Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  PubMed  CAS  Google Scholar 

  • Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, Rathjen JP, Bendahmane A, Day L, Baulcombe DC (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22:5690–5699

    Article  PubMed  CAS  Google Scholar 

  • Matthews REF (1991) Plant virology, 3rd edn. Academic Press Inc, London

    Google Scholar 

  • Meng Y, Moscou MJ, Wise RP (2009) Blufensin1 negatively impacts basal defense in response to barley powdery mildew. Plant Physiol 149:271–285

    Article  PubMed  CAS  Google Scholar 

  • Mlotshwa S, Pruss GJ, Vance V (2008) Small RNAs in viral infection and host defense. Trends Plant Sci 13:375–382

    Article  PubMed  CAS  Google Scholar 

  • Molnár A, Csorba T, Lakatos L, Várallyay E, Lacomme C, Burgyán J (2005) Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol 79:7812–7818

    Article  PubMed  Google Scholar 

  • Moore CJ, Sutherland PW, Forster RL, Gardner RC, MacDiarmid RM (2001) Dark green islands in plant virus infection are the result of posttranscriptional gene silencing. Mol Plant Microbe Interact 14:939–946

    Article  PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    Article  PubMed  CAS  Google Scholar 

  • Nelson RS, Citovsky V (2005) Plant viruses. Invaders of cells and pirates of cellular pathways. Plant Physiol 138:1809–1814

    Article  PubMed  CAS  Google Scholar 

  • Pantaleo V, Szittya G, Burgyán J (2007) Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J Virol 81:3797–3806

    Article  PubMed  CAS  Google Scholar 

  • Peele C, Jordan CV, Muangsan N, Turnage M, Egelkrout E, Eagle P, Hanley-Bowdoin L, Robertson D (2001) Silencing of a meristematic gene using geminivirus-derived vectors. Plant J 27:357–366

    Article  PubMed  CAS  Google Scholar 

  • Pflieger S, Blanchet S, Camborde L, Drugeon G, Rousseau A, Noizet M, Planchais S, Jupin I (2008) Efficient virus-induced gene silencing in Arabidopsis using a ‘one-step’ TYMV-derived vector. Plant J 56:678–690

    Article  PubMed  CAS  Google Scholar 

  • Ratcliff F, Harrison BD, Baulcombe DC (1997) A similarity between viral defense and gene silencing in plants. Science 276:1558–1560

    Article  PubMed  CAS  Google Scholar 

  • Robertson D (2004) VIGS vectors for gene silencing: many targets, many tools. Annu Rev Plant Biol 55:495–519

    Article  PubMed  CAS  Google Scholar 

  • Rommens CM, Salmeron JM, Baulcombe DC, Staskawicz BJ (1995) Use of a gene expression system based on potato virus X to rapidly identify and characterize a tomato Pto homolog that controls fenthion sensitivity. Plant Cell 7:249–257

    PubMed  CAS  Google Scholar 

  • Schwach F, Vaistij FE, Jones L, Baulcombe DC (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852

    Article  PubMed  CAS  Google Scholar 

  • Scofield SR, Huang L, Brandt AS, Gill BS (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138:2165–2173

    Article  PubMed  CAS  Google Scholar 

  • Szittya G, Silhavy D, Molnár A, Havelda Z, Lovas A, Lakatos L, Bánfalvi Z, Burgyán J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–640

    Article  PubMed  CAS  Google Scholar 

  • Takken FL, Luderer R, Gabriels SH, Westerink N, Lu R, de Wit PJ, Joosten MH (2000) A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens. Plant J 24:275–283

    Article  PubMed  CAS  Google Scholar 

  • Tang Y, Wang F, Zhao J, Xie K, Hong Y, Liu Y (2010) Virus-based microRNA expression for gene functional analysis in plants. Plant Physiol 153:632–641

    Article  PubMed  CAS  Google Scholar 

  • Thomas CL, Jones L, Baulcombe DC, Maule AJ (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

    Article  PubMed  CAS  Google Scholar 

  • Tuttle JR, Idris AM, Brown JK, Haigler CH, Robertson D (2008) Geminivirus-mediated gene silencing from cotton leaf crumple virus is enhanced by low temperature in cotton. Plant Physiol 148:41–50

    Article  PubMed  CAS  Google Scholar 

  • Turnage MA, Muangsan N, Peele CG, Robertson D (2002) Geminivirus-based vectors for gene silencing in arabidopsis. Plant J 30:107–114

    Article  PubMed  CAS  Google Scholar 

  • Valentine T, Shaw J, Blok VC, Phillips MS, Oparka KJ, Lacomme C (2004) Efficient virus-induced gene silencing in roots using a modified tobacco rattle virus vector. Plant Physiol 136:3999–4009

    Article  PubMed  CAS  Google Scholar 

  • Valentine TA, Randall E, Wypijewski K, Chapman S, Jones J, Oparka KJ (2007) Delivery of macromolecules to plant parasitic nematodes using a tobacco rattle virus vector. Plant Biotechnol J 5:827–834

    Article  PubMed  CAS  Google Scholar 

  • van Kammen A (1997) Virus-induced gene silencing in infected and transgenic plants. Trends Plant Sci 2:409–411

    Article  Google Scholar 

  • Voinnet O (2005) Non-cell autonomous RNA silencing. FEBS Lett 579:5858–5871

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O, Pinto YM, Baulcombe DC (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96:14147–14152

    Article  PubMed  CAS  Google Scholar 

  • Wege S, Scholz A, Gleissberg S, Becker A (2007) Highly efficient virus-induced gene silencing (VIGS) in California poppy (Eschscholzia Californica): an evaluation of VIGS as a strategy to obtain functional data from non-model plants. Ann Bot 100:641–649

    Article  PubMed  Google Scholar 

  • Wypijewski K, Hornyik C, Shaw JA, Stephens J, Goraczniak R, Gunderson SI, Lacomme C (2009) Ectopic 5′ splice sites inhibit gene expression by engaging RNA surveillance and silencing pathways in plants. Plant Physiol 151:955–965

    Article  PubMed  CAS  Google Scholar 

  • Yang SJ, Carter SA, Cole AB, Cheng NH, Nelson RS (2004) A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by nicotiana benthamiana. Proc Natl Acad Sci U S A 101:6297–6302

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christophe Lacomme .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lacomme, C. (2011). Milestones in the Development and Applications of Plant Virus Vector as Gene Silencing Platforms. In: Palmer, K., Gleba, Y. (eds) Plant Viral Vectors. Current Topics in Microbiology and Immunology, vol 375. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2011_186

Download citation

Publish with us

Policies and ethics