1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 73, 2022
  5. Article

Annual Review of Plant Biology

Volume 73, 2022

VIGS Goes Viral: How VIGS Transforms Our Understanding of Plant Science

Abstract

Virus-induced gene silencing (VIGS) has developed into an indispensable approach to gene function analysis in a wide array of species, many of which are not amenable to stable genetic transformation. VIGS utilizes the posttranscriptional gene silencing (PTGS) machinery of plants to restrain viral infections systemically and is used to downregulate the plant's endogenous genes. Here, we review the molecular mechanisms of DNA- and RNA-virus-based VIGS, its inherent connection to PTGS, and what is known about the systemic spread of silencing. Recently, VIGS-based technologies have been expanded to enable not only gene silencing but also overexpression [virus-induced overexpression (VOX)], genome editing [virus-induced genome editing (VIGE)], and host-induced gene silencing (HIGS). These techniques expand the genetic toolbox for nonmodel organisms even more. Further, we illustrate the versatility of VIGS and the methods derived from it in elucidating molecular mechanisms, using tomato fruit ripening and programmed cell death as examples. Finally, we discuss challenges of and future perspectives on the use of VIGS to advance gene function analysis in nonmodel plants in the postgenomic era.

Keyword(s): HIGS, PTGS, systemic silencing, VIGE, VIGS, VOX
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-102820-020542
2022-05-20
2024-05-23
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-102820-020542.html?itemId=/content/journals/10.1146/annurev-arplant-102820-020542&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alexander L, Grierson D 2002. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J. Exp. Bot. 53:3772039–55
     [Google Scholar]
  2. 2.
    Ali Z, Abul-Faraj A, Piatek M, Mahfouz MM 2015. Activity and specificity of TRV-mediated gene editing in plants. Plant Signal. Behav. 10:10e1044191
     [Google Scholar]
  3. 3.
    Andika IB, Maruyama K, Sun L, Kondo H, Tamada T, Suzuki N 2015. Differential contributions of plant Dicer-like proteins to antiviral defences against potato virus X in leaves and roots. Plant J 81:5781–93
     [Google Scholar]
  4. 4.
    Aregger M, Borah BK, Seguin J, Rajeswaran R, Gubaeva EG et al. 2012. Primary and secondary siRNAs in geminivirus-induced gene silencing. PLOS Pathog. 8:9e1002941This classical article describes how siRNAs from a circular DNA geminivirus are generated by bidirectional readthrough transcription.
     [Google Scholar]
  5. 5.
    Bakker SE, Ford RJ, Barker AM, Robottom J, Saunders K et al. 2012. Isolation of an asymmetric RNA uncoating intermediate for a single-stranded RNA plant virus. J. Mol. Biol. 417:1–265–78
     [Google Scholar]
  6. 6.
    Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF. 2014. DNA replicons for plant genome engineering. Plant Cell 26:1151–63
     [Google Scholar]
  7. 7.
    Baulcombe DC. 2015. VIGS, HIGS and FIGS: small RNA silencing in the interactions of viruses or filamentous organisms with their plant hosts. Curr. Opin. Plant Biol. 26:141–46
     [Google Scholar]
  8. 8.
    Bendandi M, Marillonnet S, Kandzia R, Thieme F, Nickstadt A et al. 2010. Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin's lymphoma. Ann. Oncol 21:122420–27
     [Google Scholar]
  9. 9.
    Bennypaul HS, Mutti JS, Rustgi S, Kumar N, Okubara PA, Gill KS. 2012. Virus-induced gene silencing (VIGS) of genes expressed in root, leaf, and meiotic tissues of wheat. Funct. Integr. Genom. 12:1143–56
     [Google Scholar]
  10. 10.
    Blevins T, Rajeswaran R, Aregger M, Borah BK, Schepetilnikov M et al. 2011. Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Res. 39:125003–14
     [Google Scholar]
  11. 11.
    Bologna NG, Voinnet O. 2014. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65:473–503
     [Google Scholar]
  12. 12.
    Boualem A, Dogimont C, Bendahmane A. 2016. The battle for survival between viruses and their host plants. Curr. Opin. Virol. 17:32–38A comprehensive discussion of the resistance genes recognizing viral proteins and avirulence factors to evade silencing.
     [Google Scholar]
  13. 13.
    Bouché N, Lauressergues D, Gasciolli V, Vaucheret H. 2006. An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25:143347–56
     [Google Scholar]
  14. 14.
    Broderick SR, Jones ML. 2014. An optimized protocol to increase virus-induced gene silencing efficiency and minimize viral symptoms in Petunia. Plant Mol. Biol. Rep. 32:219–33
     [Google Scholar]
  15. 15.
    Burch-Smith TM, Schiff M, Liu Y, Dinesh-Kumar SP. 2006. Efficient virus-induced gene silencing in Arabidopsis. Plant Physiol. 142:121–27
     [Google Scholar]
  16. 16.
    Butler NM, Baltes NJ, Voytas DF, Douches DS. 2016. Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases. Front. Plant Sci 7:1045
     [Google Scholar]
  17. 17.
    Cai Q, Qiao L, Wang M, He B, Lin F-M et al. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:63931126–29
     [Google Scholar]
  18. 18.
    Carbonell A, Carrington JC. 2015. Antiviral roles of plant ARGONAUTES. Curr. Opin. Plant Biol. 27:111–17
     [Google Scholar]
  19. 19.
    Čermák T, Baltes NJ, Čegan R, Zhang Y, Voytas DF. 2015. High-frequency, precise modification of the tomato genome. Genome Biol. 16:232
     [Google Scholar]
  20. 20.
    Chattopadhyay T, Hazra P, Akhtar S, Maurya D, Mukherjee A, Roy S. 2021. Skin colour, carotenogenesis and chlorophyll degradation mutant alleles: genetic orchestration behind the fruit colour variation in tomato. Plant Cell Rep. 40:5767–82
     [Google Scholar]
  21. 21.
    Chen W, Kastner C, Nowara D, Oliveira-Garcia E, Rutten T et al. 2016. Host-induced silencing of Fusarium culmorum genes protects wheat from infection. J. Exp. Bot. 67:174979–91
     [Google Scholar]
  22. 22.
    Chen W, Kong J, Lai T, Manning K, Wu C et al. 2015. Tuning LeSPL-CNR expression by SlymiR157 affects tomato fruit ripening. Sci. Rep. 5:7852
     [Google Scholar]
  23. 23.
    Chen W, Kong J, Qin C, Yu S, Tan J et al. 2015. Requirement of CHROMOMETHYLASE3 for somatic inheritance of the spontaneous tomato epimutation Colourless non-ripening. Sci. Rep. 5:9192
     [Google Scholar]
  24. 24.
    Chen W, Zhang X, Fan Y, Li B, Ryabov E et al. 2018. A genetic network for systemic RNA silencing in plants. Plant Physiol. 176:42700–19
     [Google Scholar]
  25. 25.
    Cheuk A, Houde M. 2018. A new barley stripe mosaic virus allows large protein overexpression for rapid function analysis. Plant Physiol. 176:31919–31A novel VOX vector system to overcome the size limit for virus-mediated protein overexpression.
     [Google Scholar]
  26. 26.
    Cody WB, Scholthof HB, Mirkov TE. 2017. Multiplexed gene editing and protein overexpression using a Tobacco mosaic virus viral vector. Plant Physiol. 175:123–35
     [Google Scholar]
  27. 27.
    Constantin GD, Krath BN, MacFarlane SA, Nicolaisen M, Johansen IE, Lund OS. 2004. Virus-induced gene silencing as a tool for functional genomics in a legume species. Plant J 40:4622–31
     [Google Scholar]
  28. 28.
    Coursey T, Regedanz E, Bisaro DM 2018. Arabidopsis RNA polymerase V mediates enhanced compaction and silencing of geminivirus and transposon chromatin during host recovery from infection. J. Virol. 92:7e01320–17
     [Google Scholar]
  29. 29.
    Csorba T, Kontra L, Burgyán J. 2015. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103
     [Google Scholar]
  30. 30.
    Cui H, Wang A. 2017. An efficient viral vector for functional genomic studies of Prunus fruit trees and its induced resistance to Plum pox virus via silencing of a host factor gene. Plant Biotechnol. J. 15:3344–56
     [Google Scholar]
  31. 31.
    Dent M, Matoba N. 2020. Cancer biologics made in plants. Curr. Opin. Biotechnol. 61:82–88
     [Google Scholar]
  32. 32.
    Dinesh-Kumar SP, Anandalakshmi R, Marathe R, Schiff M, Liu Y. 2003. Virus-induced gene silencing. Methods Mol. Biol. 236:287–94
     [Google Scholar]
  33. 33.
    Domazakis E, Wouters D, Visser RGF, Kamoun S, Joosten MHAJ, Vleeshouwers VGAA. 2018. The ELR-SOBIR1 complex functions as a two-component receptor-like kinase to mount defense against Phytophthora infestans. Mol. Plant Microbe Interact 31:8795–802
     [Google Scholar]
  34. 34.
    Dommes AB, Gross T, Herbert DB, Kivivirta KI, Becker A. 2019. Virus-induced gene silencing: empowering genetics in non-model organisms. J. Exp. Bot. 70:3757–70This review summarizes vector systems and host plants and proposes general VIGS setup and reporting guidelines.
     [Google Scholar]
  35. 35.
    Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LCP et al. 2015. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat. Plants 1:415034
     [Google Scholar]
  36. 36.
    Dunoyer P, Himber C, Voinnet O. 2005. DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37:121356–60
     [Google Scholar]
  37. 37.
    Ellison EE, Nagalakshmi U, Gamo ME, Huang P-J, Dinesh-Kumar S, Voytas DF. 2020. Multiplexed heritable gene editing using RNA viruses and mobile single guide RNAs. Nat. Plants 6:6620–24Multiple mobile single guide RNAs are virally expressed in a Cas9-overexpressing plant line for multiplex VIGE.
     [Google Scholar]
  38. 38.
    Fang X, Qi Y. 2016. RNAi in plants: an Argonaute-centered view. Plant Cell 28:2272–85
     [Google Scholar]
  39. 39.
    Folimonova SY. 2013. Developing an understanding of cross-protection by Citrus tristeza virus. Front. Microbiol 4:76
     [Google Scholar]
  40. 40.
    Franco-Orozco B, Berepiki A, Ruiz O, Gamble L, Griffe LL et al. 2017. A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. New Phytol 214:41657–72
     [Google Scholar]
  41. 41.
    Fraser PD, Bramley P, Seymour GB. 2001. Effect of the Cnr mutation on carotenoid formation during tomato fruit ripening. Phytochemistry 58:175–79
     [Google Scholar]
  42. 42.
    Fukudome A, Fukuhara T. 2017. Plant dicer-like proteins: double-stranded RNA-cleaving enzymes for small RNA biogenesis. J. Plant Res. 130:133–44
     [Google Scholar]
  43. 43.
    Gao Y, Zhu N, Zhu X, Wu M, Jiang C-Z et al. 2019. Diversity and redundancy of the ripening regulatory networks revealed by the fruitENCODE and the new CRISPR/Cas9 CNR and NOR mutants. Horticulture Res 6:39
     [Google Scholar]
  44. 44.
    Geng S, Kong X, Song G, Jia M, Guan J et al. 2019. DNA methylation dynamics during the interaction of wheat progenitor Aegilops tauschii with the obligate biotrophic fungus Blumeria graminis f. sp. tritici. New Phytol 221:21023–35
     [Google Scholar]
  45. 45.
    Gleba Y, Klimyuk V, Marillonnet S. 2005. Magnifection—a new platform for expressing recombinant vaccines in plants. Vaccine 23:17–182042–48
     [Google Scholar]
  46. 46.
    Gleba Y, Marillonnet S, Klimyuk V 2004. Engineering viral expression vectors for plants: the ‘full virus’ and the ‘deconstructed virus’ strategies. Curr. Opin. Plant Biol. 7:2182–88
     [Google Scholar]
  47. 47.
    Gong Q, Yang Z, Chen E, Sun G, He S et al. 2018. A Phi-class glutathione S-transferase gene for Verticillium wilt resistance in Gossypium arboreum identified in a genome-wide association study. Plant Cell Physiol. 59:2275–89
     [Google Scholar]
  48. 48.
    Guo Z, Wang X-B, Wang Y, Li W-X, Gal-On A, Ding S-W. 2018. Identification of a new host factor required for antiviral RNAi and amplification of viral siRNAs. Plant Physiol. 176:21587–97
     [Google Scholar]
  49. 49.
    Hartl M, Merker H, Schmidt DD, Baldwin IT. 2008. Optimized virus-induced gene silencing in Solanum nigrum reveals the defensive function of leucine aminopeptidase against herbivores and the shortcomings of empty vector controls. New Phytol 179:2356–65
     [Google Scholar]
  50. 50.
    Havelda Z, Várallyay E, Válóczi A, Burgyán J. 2008. Plant virus infection-induced persistent host gene downregulation in systemically infected leaves. Plant J 55:2278–88
     [Google Scholar]
  51. 51.
    He B, Cai Q, Qiao L, Huang C-Y, Wang S et al. 2021. RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat. Plants 7:3342–52
     [Google Scholar]
  52. 52.
    Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:2912217–22
     [Google Scholar]
  53. 53.
    Hefferon K. 2014. Plant virus expression vector development: new perspectives. Biomed. Res. Int. 2014:785382
     [Google Scholar]
  54. 54.
    Hu J, Li S, Li Z, Li H, Song W et al. 2019. A barley stripe mosaic virus-based guide RNA delivery system for targeted mutagenesis in wheat and maize. Mol. Plant Pathol. 20:101463–74
     [Google Scholar]
  55. 55.
    Hull R. 2014. Replication of plant viruses. Plant Virology341–421 Amsterdam: Academic. , 5th ed..
     [Google Scholar]
  56. 56.
    Janga MR, Pandeya D, Campbell LM, Konganti K, Villafuerte ST et al. 2019. Genes regulating gland development in the cotton plant. Plant Biotechnol. J. 17:61142–53
     [Google Scholar]
  57. 57.
    Ji L, Chen X 2012. Regulation of small RNA stability: methylation and beyond. Cell Res. 22:4624–36
     [Google Scholar]
  58. 58.
    Jiang Y, Liu C, Yan D, Wen X, Liu Y et al. 2017. MdHB1 down-regulation activates anthocyanin biosynthesis in the white-fleshed apple cultivar ‘Granny Smith. ’. J. Exp. Bot. 68:51055–69
     [Google Scholar]
  59. 59.
    Jiang Z, Zhao Q, Bai R, Yu R, Diao P et al. 2021. Host sunflower-induced silencing of parasitism-related genes confers resistance to invading Orobanche cumana. Plant Physiol. 185:2424–40
     [Google Scholar]
  60. 60.
    Jozwiak A, Sonawane PD, Panda S, Garagounis C, Papadopoulou KK et al. 2020. Plant terpenoid metabolism co-opts a component of the cell wall biosynthesis machinery. Nat. Chem. Biol. 16:7740–48
     [Google Scholar]
  61. 61.
    Kant R, Dasgupta I. 2019. Gene silencing approaches through virus-based vectors: speeding up functional genomics in monocots. Plant Mol. Biol. 100:1–23–18
     [Google Scholar]
  62. 62.
    Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S et al. 2003. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4:5383–91
     [Google Scholar]
  63. 63.
    Klee HJ, Giovannoni JJ 2011. Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45:41–59
     [Google Scholar]
  64. 64.
    Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel K-H. 2013. Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. PNAS 110:4819324–29
     [Google Scholar]
  65. 65.
    Koch A, Wassenegger M 2021. Host-induced gene silencing—mechanisms and applications. New Phytol 321:54–59Comprehensive review of the mechanism of HIGS and its application in plant protection.
     [Google Scholar]
  66. 66.
    Kolliopoulou A, Kontogiannatos D, Swevers L 2020. The use of engineered plant viruses in a trans-kingdom silencing strategy against their insect vectors. Front. Plant Sci 11:917
     [Google Scholar]
  67. 67.
    Kumagai MH, Donson J, della-Cioppa G, Harvey D, Hanley K, Grill LK 1995. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. PNAS 92:51679–83
     [Google Scholar]
  68. 68.
    Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P. 2003. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. PNAS 100:2615764–69
     [Google Scholar]
  69. 69.
    Lai T, Wang X, Ye B, Jin M, Chen W et al. 2020. Molecular and functional characterization of the SBP-box transcription factor SPL-CNR in tomato fruit ripening and cell death. J. Exp. Bot. 71:102995–3011
     [Google Scholar]
  70. 70.
    Lawrence DM, Jackson AO. 2001. Requirements for cell-to-cell movement of Barley stripe mosaic virus in monocot and dicot hosts. Mol. Plant Pathol. 2:265–75
     [Google Scholar]
  71. 71.
    Lee W-S, Hammond-Kosack KE, Kanyuka K. 2012. Barley stripe mosaic virus-mediated tools for investigating gene function in cereal plants and their pathogens: virus-induced gene silencing, host-mediated gene silencing, and virus-mediated overexpression of heterologous protein. Plant Physiol. 160:2582–90
     [Google Scholar]
  72. 72.
    Lei J, Dai P, Li Y, Zhang W, Zhou G, Liu C, Liu X. 2021. Heritable gene editing using FT mobile guide RNAs and DNA viruses. Plant Methods 17:120
     [Google Scholar]
  73. 73.
    Li S, Liu L, Zhuang X, Yu Y, Liu X et al. 2013. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:3562–74
     [Google Scholar]
  74. 74.
    Liang D, White RG, Waterhouse PM. 2012. Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol. 159:3984–1000
     [Google Scholar]
  75. 75.
    Liebrand TWH, van den Berg GCM, Zhang Z, Smit P, Cordewener JHG et al. 2013. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. PNAS 110:2410010–15
     [Google Scholar]
  76. 76.
    Lin X, Armstrong M, Baker K, Wouters D, Visser RGF et al. 2020. RLP/K enrichment sequencing; a novel method to identify receptor-like protein (RLP) and receptor-like kinase (RLK) genes. New Phytol 227:41264–76
     [Google Scholar]
  77. 77.
    Lindbo JA. 2007. TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 145:41232–40
     [Google Scholar]
  78. 78.
    Liu L, Chen X. 2018. Intercellular and systemic trafficking of RNAs in plants. Nat. Plants 4:11869–78
     [Google Scholar]
  79. 79.
    Ma X, Nicole M-C, Meteignier L-V, Hong N, Wang G, Moffett P 2015. Different roles for RNA silencing and RNA processing components in virus recovery and virus-induced gene silencing in plants. J. Exp. Bot. 66:3919–32
     [Google Scholar]
  80. 80.
    Ma X, Zhang X, Liu H, Li Z. 2020. Highly efficient DNA-free plant genome editing using virally delivered CRISPR-Cas9. Nat. Plants 6:7773–79Novel RNA virus–based vector system to deliver the complete CRISPR-Cas9 cassette for VIGE.
     [Google Scholar]
  81. 81.
    MacDiarmid R. 2005. RNA silencing in productive virus infections. Annu. Rev. Phytopathol. 43:523–44
     [Google Scholar]
  82. 82.
    MacFarlane SA. 2010. Tobraviruses—plant pathogens and tools for biotechnology. Mol. Plant Pathol. 11:4577–83
     [Google Scholar]
  83. 83.
    Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol 13:11722–36
     [Google Scholar]
  84. 84.
    Mallory A, Vaucheret H 2010. Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:123879–89
     [Google Scholar]
  85. 85.
    Manning K, Tör M, Poole M, Hong Y, Thompson AJ et al. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38:8948–52
     [Google Scholar]
  86. 86.
    Mao Y, Yang X, Zhou Y, Zhang Z, Botella JR, Zhu J-K. 2018. Manipulating plant RNA-silencing pathways to improve the gene editing efficiency of CRISPR/Cas9 systems. Genome Biol. 19:1149
     [Google Scholar]
  87. 87.
    Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet 15:6394–408
     [Google Scholar]
  88. 88.
    Mei Y, Beernink BM, Ellison EE, Konečná E, Neelakandan AK, Voytas DF, Whitham SA. 2019. Protein expression and gene editing in monocots using foxtail mosaic virus vectors. Plant Direct 3:11e00181
     [Google Scholar]
  89. 89.
    Melnyk CW, Molnar A, Baulcombe DC. 2011. Intercellular and systemic movement of RNA silencing signals. EMBO J. 30:173553–63
     [Google Scholar]
  90. 90.
    Ming R, Zhang Y, Wang Y, Khan M, Dahro B, Liu J-H. 2021. The JA-responsive MYC2-BADH-like transcriptional regulatory module in Poncirus trifoliata contributes to cold tolerance by modulation of glycine betaine biosynthesis. New Phytol 229:52730–50
     [Google Scholar]
  91. 91.
    Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:4349–57
     [Google Scholar]
  92. 92.
    Muraya MM, Chu J, Zhao Y, Junker A, Klukas C, Reif JC, Altmann T. 2017. Genetic variation of growth dynamics in maize (Zea mays L.) revealed through automated non-invasive phenotyping. Plant J. 89:2366–80
     [Google Scholar]
  93. 93.
    Murphy F, He Q, Armstrong M, Giuliani LM, Boevink PC et al. 2018. The potato MAP3K StVIK is required for the Phytophthora infestans RXLR effector Pi17316 to promote disease. Plant Physiol. 177:1398–410
     [Google Scholar]
  94. 94.
    Oh Y, Kim H, Kim S-G. 2021. Virus-induced plant genome editing. Curr. Opin. Plant Biol. 60:101992
     [Google Scholar]
  95. 95.
    Panwar V, McCallum B, Bakkeren G. 2013. Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol. Biol. 81:6595–608
     [Google Scholar]
  96. 96.
    Parent J-S, Bouteiller N, Elmayan T, Vaucheret H 2015. Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing. Plant J 81:2223–32
     [Google Scholar]
  97. 97.
    Peart JR, Lu R, Sadanandom A, Malcuit I, Moffett P et al. 2002. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. PNAS 99:1610865–69
     [Google Scholar]
  98. 98.
    Pennell RI, Lamb C. 1997. Programmed cell death in plants. Plant Cell 9:71157–68
     [Google Scholar]
  99. 99.
    Pogue GP, Vojdani F, Palmer KE, Hiatt E, Hume S et al. 2010. Production of pharmaceutical-grade recombinant aprotinin and a monoclonal antibody product using plant-based transient expression systems. Plant Biotechnol. J. 8:5638–54
     [Google Scholar]
  100. 100.
    Pumplin N, Voinnet O. 2013. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat. Rev. Microbiol 11:11745–60
     [Google Scholar]
  101. 101.
    Qi T, Guo J, Peng H, Liu P, Kang Z, Guo J. 2019. Host-induced gene silencing: a powerful strategy to control diseases of wheat and barley. Int. J. Mol. Sci. 20:1206A comprehensive review of the most recent studies of HIGS.
     [Google Scholar]
  102. 102.
    Qin C, Li B, Fan Y, Zhang X, Yu Z et al. 2017. Roles of Dicer-like proteins 2 and 4 in intra- and intercellular antiviral silencing. Plant Physiol. 174:21067–81
     [Google Scholar]
  103. 103.
    Qin C, Shi N, Gu M, Zhang H, Li B et al. 2012. Involvement of RDR6 in short-range intercellular RNA silencing in Nicotiana benthamiana. Sci. Rep. 2:467
     [Google Scholar]
  104. 104.
    Raja P, Wolf JN, Bisaro DM. 2010. RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim. Biophys. Acta Gene Regul. Mech. 1799:3–4337–51
     [Google Scholar]
  105. 105.
    Sanan-Mishra N, Jailani AAK, Mandal B, Mukherjee SK 2021. Secondary siRNAs in plants: biosynthesis, various functions, and applications in virology. Front. Plant Sci 12:610283
     [Google Scholar]
  106. 106.
    Sarkies P, Miska EA. 2014. Small RNAs break out: the molecular cell biology of mobile small RNAs. Nat. Rev. Mol. Cell Biol 15:8525–35
     [Google Scholar]
  107. 107.
    Saunders K, Wege C, Veluthambi K, Jeske H, Stanley J 2001. The distinct disease phenotypes of the common and yellow vein strains of Tomato golden mosaic virus are determined by nucleotide differences in the 3′-terminal region of the gene encoding the movement protein. J. Gen. Virol. 82:Part 145–51
     [Google Scholar]
  108. 108.
    Schiml S, Fauser F, Puchta H. 2014. The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80:61139–50
     [Google Scholar]
  109. 109.
    Schuck J, Gursinsky T, Pantaleo V, Burgyán J, Behrens S-E. 2013. AGO/RISC-mediated antiviral RNA silencing in a plant in vitro system. Nucleic Acids Res. 41:95090–103
     [Google Scholar]
  110. 110.
    Senthil-Kumar M, Mysore KS. 2011. Virus-induced gene silencing can persist for more than 2 years and also be transmitted to progeny seedlings in Nicotiana benthamiana and tomato. Plant Biotechnol. J. 9:7797–806
     [Google Scholar]
  111. 111.
    Song Y, Thomma BPHJ. 2018. Host-induced gene silencing compromises Verticillium wilt in tomato and Arabidopsis. Mol. Plant Pathol. 19:177–89
     [Google Scholar]
  112. 112.
    Su J, Li L, Zhang C, Wang C, Gu L et al. 2018. Genome-wide association study identified genetic variations and candidate genes for plant architecture component traits in Chinese upland cotton. Theor. Appl. Genet. 131:61299–314
     [Google Scholar]
  113. 113.
    Sukegawa S, Saika H, Toki S. 2021. Plant genome editing: ever more precise and wide reaching. Plant J 106:1208–18
     [Google Scholar]
  114. 114.
    Syed NH, Kalyna M, Marquez Y, Barta A, Brown JWS. 2012. Alternative splicing in plants—coming of age. Trends Plant Sci. 17:10616–23
     [Google Scholar]
  115. 115.
    Taochy C, Gursanscky NR, Cao J, Fletcher SJ, Dressel U et al. 2017. A genetic screen for impaired systemic RNAi highlights the crucial role of DICER-LIKE 2. Plant Physiol. 175:31424–37
     [Google Scholar]
  116. 116.
    Thompson AJ, Tor M, Barry CS, Vrebalov J, Orfila C et al. 1999. Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol. 120:2383–90
     [Google Scholar]
  117. 117.
    Tusé D, Nandi S, McDonald KA, Buyel JF. 2020. The emergency response capacity of plant-based biopharmaceutical manufacturing—what it is and what it could be. Front. Plant Sci 11:594019
     [Google Scholar]
  118. 118.
    Veluthambi K, Sunitha S. 2021. Targets and mechanisms of geminivirus silencing suppressor protein AC2. Front. Microbiol 12:645419
     [Google Scholar]
  119. 119.
    Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D et al. 2002. A MADS-box gene necessary for fruit ripening at the tomato Ripening-inhibitor (Rin) locus. Science 296:5566343–46
     [Google Scholar]
  120. 120.
    Wang M, Gao S, Zeng W, Yang Y, Ma J, Wang Y 2020. Plant virology delivers diverse toolsets for biotechnology. Viruses 12:111338
     [Google Scholar]
  121. 121.
    Wang M, Lu Y, Botella JR, Mao Y, Hua K, Zhu J-K. 2017. Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 System. Mol. Plant 10:71007–10
     [Google Scholar]
  122. 122.
    Wang M, Thomas N, Jin H 2017. Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection. Curr. Opin. Plant Biol. 38:133–41
     [Google Scholar]
  123. 123.
    Wang P, Li G, Li G, Yuan S, Wang C et al. 2021. TaPHT1;9-4B and its transcriptional regulator TaMYB4-7D contribute to phosphate uptake and plant growth in bread wheat. New Phytol 231:1968–83
     [Google Scholar]
  124. 124.
    Wang R, Angenent GC, Seymour G, de Maagd RA. 2020. Revisiting the role of master regulators in tomato ripening. Trends Plant Sci. 25:3291–301
     [Google Scholar]
  125. 125.
    Wang Y, Ying J, Zhang Y, Xu L, Zhang W et al. 2020. Genome-wide identification and functional characterization of the cation proton antiporter (CPA) family related to salt stress response in radish (Raphanus sativus L.). Int. J. Mol. Sci. 21:218262
     [Google Scholar]
  126. 126.
    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. 100:3641–49
     [Google Scholar]
  127. 127.
    Weiberg A, Jin H. 2015. Small RNAs—the secret agents in the plant-pathogen interactions. Curr. Opin. Plant Biol. 26:87–94
     [Google Scholar]
  128. 128.
    Wright AV, Nuñez JK, Doudna JA. 2016. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164:1–229–44
     [Google Scholar]
  129. 129.
    Wu C-H, Belhaj K, Bozkurt TO, Birk MS, Kamoun S. 2016. Helper NLR proteins NRC2a/b and NRC3 but not NRC1 are required for Pto-mediated cell death and resistance in Nicotiana benthamiana. New Phytol 209:41344–52
     [Google Scholar]
  130. 130.
    Wu H, Li B, Iwakawa H-O, Pan Y, Tang X et al. 2020. Plant 22-nt siRNAs mediate translational repression and stress adaptation. Nature 581:780689–93
     [Google Scholar]
  131. 131.
    Wu H, Tian Y, Wan Q, Fang L, Guan X et al. 2018. Genetics and evolution of MIXTA genes regulating cotton lint fiber development. New Phytol 217:2883–95VIGS was used to unravel gene functions involved in regulating a unique and agronomically important trait.
     [Google Scholar]
  132. 132.
    Wu C, Jia L, Goggin F 2011. The reliability of virus-induced gene silencing experiments using tobacco rattle virus in tomato is influenced by the size of the vector control. Mol. Plant Pathol. 12:3299–305
     [Google Scholar]
  133. 133.
    Yan H, Shi S, Ma N, Cao X, Zhang H et al. 2018. Graft-accelerated virus-induced gene silencing facilitates functional genomics in rose flowers. J. Integr. Plant Biol. 60:134–44
     [Google Scholar]
  134. 134.
    Yang Z, Ebright YW, Yu B, Chen X 2006. HEN1 recognizes 21–24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res. 34:2667–75
     [Google Scholar]
  135. 135.
    Yao M, Chen W, Kong J, Zhang X, Shi N et al. 2020. METHYLTRANSFERASE1 and ripening modulate vivipary during tomato fruit development. Plant Physiol. 183:41883–97
     [Google Scholar]
  136. 136.
    Yokotani N, Nakano R, Imanishi S, Nagata M, Inaba A, Kubo Y. 2009. Ripening-associated ethylene biosynthesis in tomato fruit is autocatalytically and developmentally regulated. J. Exp. Bot. 60:123433–42
     [Google Scholar]
  137. 137.
    Yuan C, Li C, Yan L, Jackson AO, Liu Z et al. 2011. A high throughput Barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLOS ONE 6:10e26468
     [Google Scholar]
  138. 138.
    Zhai R, Wang Z, Zhang S, Meng G, Song L et al. 2016. Two MYB transcription factors regulate flavonoid biosynthesis in pear fruit (Pyrus bretschneideri Rehd.). J. Exp. Bot. 67:51275–84
     [Google Scholar]
  139. 139.
    Zhang C, Wu Z, Li Y, Wu J 2015. Biogenesis, function, and applications of virus-derived small RNAs in plants. Front. Microbiol 6:1237
     [Google Scholar]
  140. 140.
    Zhang X, Kang L, Zhang Q, Meng Q, Pan Y et al. 2020. An RNAi suppressor activates in planta virus-mediated gene editing. Funct. Integr. Genom. 20:4471–77
     [Google Scholar]
  141. 141.
    Zhang X, Lai T, Zhang P, Zhang X, Yuan C et al. 2019. Mini review: Revisiting mobile RNA silencing in plants. Plant Sci 278:113–17
     [Google Scholar]
  142. 142.
    Zhou T, Zhang H, Lai T, Qin C, Shi N et al. 2012. Virus-induced gene complementation reveals a transcription factor network in modulation of tomato fruit ripening. Sci. Rep. 2:836
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-102820-020542
Loading
VIGS Goes Viral: How VIGS Transforms Our Understanding of Plant Science
Annual Review of Plant Biology 73, 703 (2022); https://doi.org/10.1146/annurev-arplant-102820-020542
/content/journals/10.1146/annurev-arplant-102820-020542
/content/journals/10.1146/annurev-arplant-102820-020542
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error