Skip to main content

Novel Technologies for Transgenic Management for Plant Virus Resistance

  • Chapter
  • First Online:
Genome Engineering for Crop Improvement

Abstract

Global food security is threatened by the rapidly growing human population, by plant pests and diseases, and by climate change. It is estimated that US$ 60 billion loss in crop yields (10–15% global crop yield reduction) each year is due to plant viral diseases. More importantly, viral agents are determined to be responsible for half of the emerging plant diseases worldwide. Plant virus control is accomplished mainly by chemical applications aiming at the vectors transmitting the virus to a new plant contributing to the epidemiology of the disease. The use of chemicals, in some cases, has a significant negative environmental impact and poses human risks, and thus other friendlier strategies of virus control need to be developed. Towards this direction RNA silencing (RNA interference, RNAi), a conserved endogenous pathway of all higher eukaryotes, is exploited as an antiviral method. The silencing inducer molecule is the double-stranded RNA (dsRNA) and the slicing of the target RNA is directed by specific virus-derived small interfering RNAs (vsiRNAs) in collaboration with host-encoded Argonaute enzymes. DsRNA- and artificial microRNA-mediated resistance has been exploited in transgenic plants to develop resistance against viruses. The current research efforts (computational and biochemical) focus on determining the more efficacious inducer of RNAi. In this respect, the contribution of the next-generation sequencing and bioinformatics analyses play a crucial role. The antiviral arsenal includes also the novel approach of genome editing for conferring the desired antiviral status in the host plant. This method involves less side-effects on the host gene expression as compared to RNAi related treatments. However, the DNA sequence to be modified (edited) needs to be determined in a laborious and time-consuming process prior to the actual modification. It is vital to determine the molecular/biochemical attributes in the specific plant-virus interaction that will shift the balance towards the resistance of the host to the invading virus.

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 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
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

  • Aaziz R, Tepfer M (1999) Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol 80:1339–1346

    Article  CAS  PubMed  Google Scholar 

  • Abel P, Nelson R, De B, Hoffmann N, Rogers S, Fraley R, Beachy R (1986) Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738–743

    Article  CAS  PubMed  Google Scholar 

  • Ai T, Zhang L, Gao Z, Zhu CX, Guo X (2011) Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol 13:304–316

    Article  CAS  PubMed  Google Scholar 

  • Alcaide-Loridan C, Jupin I (2012) Ubiquitin and plant viruses, let’s play together! Plant Physiol 160:72–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali Z, Ali S, Tashkandi M, Zaidi SSEA, Mahfouz MM (2016) CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci Rep. https://doi.org/10.1038/srep26912

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci 102:11928–11933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366

    Article  CAS  PubMed  Google Scholar 

  • Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Park H-S, Vazquez F, Robertson D, Meins F, Hohn T et al (2006) Four plant dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34:6233–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boonrod K, Galetzka D, Nagy PD, Conrad U, Krczal G (2004) Single-chain antibodies against a plant viral RNA-dependent RNA polymerase confer virus resistance. Nat Biotechnol 22:856–862

    Article  CAS  PubMed  Google Scholar 

  • Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollander J, Meins F, Kovalchuk I (2010) Transgenerational adaptation of arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS ONE 5:e9514

    Article  PubMed  PubMed Central  Google Scholar 

  • Brizard JP, Brugidou C, Carapito C, Delalande F, Van Dorsselaer A, Brugidou C (2006) Proteome analysis of plant-virus interactome: comprehensive data for virus multiplication inside their hosts. Mol Cell Proteomics 5:2279–2297

    Article  CAS  PubMed  Google Scholar 

  • Brocard M, Ruggieri A, Locker N (2017) m6A RNA methylation, a new hallmark in virus-host interactions. J Gen Virol 98:2207–2214

    Article  CAS  PubMed  Google Scholar 

  • Bruening G (2006) Resistance to infection. In: Loebenstein G, Carr JP (eds) Nature resistance mechanics plants to viruses. Springer, Netherlands Dordrecht, pp 211–240

    Chapter  Google Scholar 

  • Burgyán J, Havelda Z (2011) Viral suppressors of RNA silencing. Trends Plant Sci 16:265–272

    Article  PubMed  CAS  Google Scholar 

  • Callaway E (2018) CRISPR plants now subject to tough GM laws in European union. Nature 560:16

    Article  CAS  PubMed  Google Scholar 

  • Cao M, Du P, Wang X, Yu Y-Q, Qiu Y-H, Li W, Gal-On A, Zhou C, Li Y, Ding S-W (2014) Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis. Proc Natl Acad Sci USA 111:14613–14618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonell A (2019a) Design and high-throughput generation of artificial small RNA constructs for plants. Methods Mol Biol 247–260

    Google Scholar 

  • Carbonell A (2019) Secondary small interfering RNA-based silencing tools in plants: an update. Front Plant Sci 10:1–5

    Article  CAS  Google Scholar 

  • Carbonell A, Takeda A, Fahlgren N, Johnson SC, Cuperus JT, Carrington JC (2014) New generation of artificial microRNA and synthetic trans-acting small interfering RNA vectors for efficient gene silencing in Arabidopsis. Plant Physiol 165:15–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen K, Wang Y, Zhang R, Zhang H, Gao C (2019) CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol 70:667–697

    Article  CAS  PubMed  Google Scholar 

  • Christie M, Brosnan CA, Rothnagel JA, Carroll BJ (2011) RNA Decay and RNA silencing in plants: competition or collaboration? Front Plant Sci. https://doi.org/10.3389/fpls.2011.00099

    Article  PubMed  PubMed Central  Google Scholar 

  • Colas P, Cohen B, Jessen T, Grishina I, McCoy J, Brent R (1996) Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature 380:548–550

    Article  CAS  PubMed  Google Scholar 

  • Conti G, Zavallo D, Venturuzzi AL, Rodriguez MC, Crespi M, Asurmendi S (2017) TMV induces RNA decay pathways to modulate gene silencing and disease symptoms. Plant J 89:73–84

    Article  CAS  PubMed  Google Scholar 

  • Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103

    Article  PubMed  CAS  Google Scholar 

  • Csorba T, Pantaleo V, Burgyán J (2009) RNA silencing: an antiviral mechanism. Adv Virus Res 75:35–71

    Article  CAS  PubMed  Google Scholar 

  • De Felippes FF, Wang JW, Weigel D (2012) MIGS: MiRNA-induced gene silencing. Plant J 70:541–547

    Article  PubMed  CAS  Google Scholar 

  • de Ronde D, Butterbach P, Kormelink R (2014) Dominant resistance against plant viruses. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00307

    Article  PubMed  PubMed Central  Google Scholar 

  • de Felippes FF (2019) Gene regulation mediated by microRNA-triggered secondary small RNAs in plants. Plants 8:112

    Article  PubMed Central  CAS  Google Scholar 

  • Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc Natl Acad Sci USA 109:15942–15946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diezma-Navas L, Pérez-González A, Artaza H, Alonso L, Caro E, Llave C, Ruiz-Ferrer V (2019) Crosstalk between epigenetic silencing and infection by tobacco rattle virus in Arabidopsis. Mol Plant Pathol 20:1439–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding B, Wang G-L (2015) Chromatin versus pathogens: the function of epigenetics in plant immunity. Front Plant Sci 6:1–8

    Article  CAS  Google Scholar 

  • Ding S-W (2010) RNA-based antiviral immunity. Nat Rev Immunol 10:632–644

    Article  CAS  PubMed  Google Scholar 

  • Duan C-G, Fang Y-Y, Zhou B-J, Zhao J-H, Hou W-N, Zhu H, Ding S-W, Guo H-S (2012) Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the cucumber mosaic virus 2b protein. Plant Cell 24:259–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson D (2019) The evolving EU regulatory framework for precision breeding. Theor Appl Genet 132:569–573

    Article  PubMed  Google Scholar 

  • Espinas NA, Saze H, Saijo Y (2016) Epigenetic control of defense signaling and priming in plants. Front Plant Sci 7:1–7

    Article  Google Scholar 

  • Fahlgren N, Hill ST, Carrington JC, Carbonell A (2016) P-SAMS: a web site for plant artificial microRNA and synthetic trans-acting small interfering RNA design. Bioinformatics 32:157–158

    CAS  PubMed  Google Scholar 

  • Fischer R, Schumann D, Zimmermann S, Drossard J, Sack M, Schillberg S (1999) Expression and characterization of bispecific single-chain Fv fragments produced in transgenic plants. Eur J Biochem 262:810–816

    Article  CAS  PubMed  Google Scholar 

  • Fonseca JP, Mysore KS (2019) Genes involved in nonhost disease resistance as a key to engineer durable resistance in crops. Plant Sci 279:108–116

    Article  CAS  PubMed  Google Scholar 

  • Fraser RSS (1992) The genetics of plant-virus interactions: implications for plant breeding. Euphytica 63:175–185

    Article  Google Scholar 

  • Fraser RSS (1990) The genetics of resistance to plant viruses. Annu Rev Phytopathol 28:179–200

    Article  Google Scholar 

  • Gago-Zachert S, Schuck J, Weinholdt C, Knoblich M, Pantaleo V, Grosse I, Gursinsky T, Behrens SE (2019) Highly efficacious antiviral protection of plants by small interfering RNAs identified in vitro. Nucleic Acids Res 47:9343–9357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gal-On A, Shiboleth YM (2006) Cross-protection. In: Loebenstein G, Carr JP (eds) Nature resistance mechanics. Plants to viruses. Springer, Netherlands, Dordrecht, pp 261–288

    Chapter  Google Scholar 

  • García-Arenal F, Mcdonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93:941–952

    Article  PubMed  Google Scholar 

  • Garcia-Ruiz H (2018) Susceptibility genes to plant viruses. Viruses 10:484

    Article  PubMed Central  CAS  Google Scholar 

  • Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during turnip mosaic virus infection. Plant Cell 22:481–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia D, Garcia S, Voinnet O (2014) Nonsense-mediated decay serves as a general viral restriction mechanism in plants. Cell Host Microbe 16:391–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelinsky E, Hilbeck A (2018) European court of justice ruling regarding new genetic engineering methods scientifically justified: a commentary on the biased reporting about the recent ruling. Environ Sci Eur 30:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghoshal B, Sanfaçon H (2015) Symptom recovery in virus-infected plants: revisiting the role of RNA silencing mechanisms. Virology 479–480:167–179

    Article  PubMed  CAS  Google Scholar 

  • Gilliland A, Murphy AM, Carr JP (2006) Induced resistance mechanisms. Nat Resist Mech Plants Viruses 125–145

    Google Scholar 

  • Gottula J, Fuchs M (2009) Toward a quarter century of pathogen-derived resistance and practical approaches to plant virus disease control. Advance virus research. Elsevier pp 161–183

    Google Scholar 

  • Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, Proux F, Proux C, Vaucheret H, Mallory AC (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–3461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC (2013) Stepwise artificial evolution of a plant disease resistance gene. Proc Natl Acad Sci USA 110:21189–21194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashimoto M, Neriya Y, Yamaji Y, Namba S (2016) Recessive resistance to plant viruses: potential resistance genes beyond translation initiation factors. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01695

  • Hiatt A, Cafferkey R, Bowdish K (1989) Production of antibodies in transgenic plants. Nature 342:76–78

    Article  CAS  PubMed  Google Scholar 

  • Hunter WB, Glick E, Paldi N, Bextine BR (2012) Advances in RNA interference: dsRNA treatment in trees and grapevines for insect pest suppression. Southwest Entomol 37:85–87

    Article  Google Scholar 

  • Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32

    Article  CAS  PubMed  Google Scholar 

  • Kaldis A, Berbati M, Melita O, Reppa C, Holeva M, Otten P, Voloudakis A (2018) Exogenously applied dsRNA molecules deriving from the Zucchini yellow mosaic virus (ZYMV) genome move systemically and protect cucurbits against ZYMV. Mol Plant Pathol 19:883–895

    Article  CAS  PubMed  Google Scholar 

  • Kang B, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621

    Article  CAS  PubMed  Google Scholar 

  • Kim MJ, Huh SU, Ham B-K, Paek K-H (2008) A novel methyltransferase methylates cucumber mosaic virus 1a protein and promotes systemic spread. J Virol 82:4823–4833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konakalla NC, Kaldis A, Masarapu H, Voloudakis AE (2019) Topical application of double stranded RNA molecules deriving from Sesbania mosaic virus (SeMV) CP and MP genes protects Sesbania plants against SeMV. Eur J Plant Pathol 155:1345–1352

    Article  CAS  Google Scholar 

  • Kurreck J (2006) siRNA efficiency: structure or sequence-that is the question. J Biomed Biotechnol 2006:1–7

    Article  CAS  Google Scholar 

  • Kushwaha NK, Hafrén A, Hofius D (2019) Autophagy-virus interplay in plants: from antiviral recognition to proviral manipulation. Mol Plant Pathol 20:1211–1216

    Article  PubMed  PubMed Central  Google Scholar 

  • Langner T, Kamoun S, Belhaj K (2018) CRISPR crops: plant genome editing toward disease resistance. Annu Rev Phytopathol 56:479–512

    Article  CAS  PubMed  Google Scholar 

  • Lassner M (2001) Directed molecular evolution in plant improvement. Curr Opin Plant Biol 4:152–156

    Article  CAS  PubMed  Google Scholar 

  • Ledford H (2019) EU regulators face CRISPR crop condundrum. Nature 572:15

    Article  CAS  PubMed  Google Scholar 

  • Lee H-A, Lee H-Y, Seo E, Lee J, Kim S-B, Oh S, Choi E, Choi E, Lee SE, Choi D (2017) Current understandings of plant nonhost resistance. Mol Plant-Microbe Interact 30:5–15

    Article  CAS  PubMed  Google Scholar 

  • Li F, Ding S-W (2006) Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 60:503–531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Zhang C, Li Y, Wu G, Hou X, Zhou X, Wang A (2018) Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase. Nat Commun 9:1–17

    CAS  Google Scholar 

  • Liao Y-C, Pingli H, Senzhao C, Yao M-J, Zhang J-B, Liu J-L (2006) Plantibodies: a novel strategy to create pathogen-resistant plants. Biotechnol Genet Eng Rev 23:253–272

    Article  CAS  PubMed  Google Scholar 

  • Lindbo JA (2012) A historical overview of RNAi in plants. In: Watson JM, Wang M-B (eds) Humana press. Totowa, NJ, pp 1–16

    Google Scholar 

  • Loebenstein G (2009) Plant virus diseases: Economic aspect. In: Regenmortel MHV, Mahy BWJ (eds) Desk Encyc. Academic Press, Desk Encyclopedia of Plant and Fungal, pp 426–430

    Google Scholar 

  • Ma JK, Drake PMW, Christou P (2003) The production of recombinant pharmaceutical proteins in plants. Nat Rev Genet 4:794–805

    Article  CAS  PubMed  Google Scholar 

  • Machado JPB, Calil IP, Santos AA, Fontes EPB (2017) Translational control in plant antiviral immunity. Genet Mol Biol 40:292–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Pérez M, Aparicio F, López-Gresa MP, Bellés JM, Sánchez-Navarro JA, Pallás V (2017) Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc Natl Acad Sci USA 114:10755–10760

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Martínez F, Lafforgue G, Morelli MJ, González-Candelas F, Chua NH, Daròs JA, Elena SF (2012) Ultradeep sequencing analysis of population dynamics of virus escape mutants in RNAi-mediated resistant plants. Mol Biol Evol 29:3297–3307

    Article  PubMed  CAS  Google Scholar 

  • Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408

    Article  CAS  PubMed  Google Scholar 

  • Maule AJ, Caranta C, Boulton MI (2007) Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231

    Article  CAS  PubMed  Google Scholar 

  • Miozzi L, Gambino G, Burgyan J, Pantaleo V (2013) Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. Mol Plant Pathol 14:30–43

    Article  CAS  PubMed  Google Scholar 

  • Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GQ, Xu ZP (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat Plants. https://doi.org/10.1038/nplants.2016.207

  • Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442:1046–1049

    Article  CAS  PubMed  Google Scholar 

  • Namgial T, Kaldis A, Chakraborty S, Voloudakis A (2019) Topical application of double-stranded RNA molecules containing sequences of tomato leaf curl virus and cucumber mosaic virus confers protection against the cognate viruses. Physiol Mol Plant Pathol. https://doi.org/10.1016/j.pmpp.2019.101432

  • Nicaise V, Candresse T (2016) Plum pox virus capsid protein suppresses plant pathogen-associated molecular pattern (PAMP)-triggered immunity. Mol Plant Pathol 18:878–886

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niehl A, Heinlein M (2019) Perception of double-stranded RNA in plant antiviral immunity. Mol Plant Pathol 20:1203–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niehl A, Wyrsch I, Boller T, Heinlein M (2016) Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211:1008–1019

    Article  CAS  PubMed  Google Scholar 

  • Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD, Chua NH (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428

    Article  CAS  PubMed  Google Scholar 

  • Pavan S, Jacobsen E, Visser RGF, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1–12

    Article  PubMed  Google Scholar 

  • Pecinka A, Mittelsten Scheid O (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53:801–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pooggin M (2013) How can plant DNA viruses evade siRNA-directed DNA methylation and silencing? Int J Mol Sci 14:15233–15259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pyott DE, Sheehan E, Molnar A (2016) Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Pathol 17:1276–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ratcliff FG, MacFarlane SA, Baulcombe DC (1999) Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 11:1207–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes MI, Nash TE, Dallas MM, Ascencio-Ibanez JT, Hanley-Bowdoin L (2013) Peptide aptamers that bind to geminivirus replication proteins confer a resistance phenotype to tomato yellow leaf curl virus and tomato mottle virus infection in tomato. J Virol 87:9691–9706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Negrete EA, Carrillo-Tripp J, Rivera-Bustamante RF (2009) RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 83:1332–1340

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Negrete EA, Morales-Aguilar JJ, Domínguez-Duran G, Torres-Devora G, Camacho-Beltrán E, Leyva-López NE, Voloudakis AE, Bejarano ER, Méndez-Lozano J (2019) High-throughput sequencing reveals differential begomovirus species diversity in non-cultivated plants in northern-pacific Mexico. Viruses 11:594

    Article  PubMed Central  CAS  Google Scholar 

  • Romay G, Bragard C (2017) Antiviral defenses in plants through genome editing. Front Microbiol. https://doi.org/10.3389/fmicb.2017.00047

  • Rudolph C, Schreier PH, Uhrig JF (2003) Peptide-mediated broad-spectrum plant resistance to tospoviruses. Proc Natl Acad Sci USA 100:4429–4434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanfaçon H (2015) Plant translation factors and virus resistance. Viruses 7:3392–3419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanford JC, Johnston SA (1985) The concept of parasite-derived resistance-deriving resistance genes from the parasite’s own genome. J Theor Biol 113:395–405

    Article  Google Scholar 

  • Sato Y, Miyashita S, Ando S, Takahashi H (2017) Increased cytosine methylation at promoter of the NB-LRR class R gene RCY1 correlated with compromised resistance to cucumber mosaic virus in EMS-generated src mutants of Arabidopsis thaliana. Physiol Mol Plant Pathol 100:151–162

    Article  CAS  Google Scholar 

  • Schillberg S, Zimmermann S, Findlay K, Fischer R (2000) Plasma membrane display of anti-viral single chain Fv fragments confers resistance to tobacco mosaic virus. Mol Breed 6:317–326

    Article  CAS  Google Scholar 

  • Schmitt-Keichinger C (2019) Manipulating cellular factors to combat viruses: a case study from the plant eukaryotic translation initiation factors eIF4. Front Microbiol 10:1–8

    Article  Google Scholar 

  • Sekhwal MK, Li P, Lam I, Wang X, Cloutier S, You FM (2015) Disease resistance gene analogs (RGAs) in plants. Int J Mol Sci 16:19248–19290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senthil-Kumar M, Mysore KS (2011) Virus-induced gene silencing can persist for more than 2years and also be transmitted to progeny seedlings in Nicotiana benthamiana and tomato. Plant Biotechnol J 9:797–806

    Article  CAS  PubMed  Google Scholar 

  • Sera T (2017) Use of peptide aptamers, cationic peptides and artificial zinc finger proteins to generate resistance to plant viruses. Curr Opin Virol 26:120–124

    Article  CAS  PubMed  Google Scholar 

  • Shamandi N, Zytnicki M, Charbonnel C, Elvira-Matelot E, Bochnakian A, Comella P, Mallory AC, Lepère G, Sáez-Vásquez J, Vaucheret H (2015) Plants encode a general siRNA suppressor that is induced and suppressed by viruses. PLOS Biol 13:e1002326

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simón-Mateo C, García JA (2011) Antiviral strategies in plants based on RNA silencing. Biochim Biophys Acta Gene Regul Mech 1809:722–731

    Article  CAS  Google Scholar 

  • Singh A, Mohorianu I, Green D, Dalmay T, Dasgupta I, Mukherjee SK (2019) Artificially induced phased siRNAs promote virus resistance in transgenic plants. Virology 537:208–215

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Taneja J, Dasgupta I, Mukherjee SK (2015) Development of plants resistant to tomato geminiviruses using artificial trans-acting small interfering RNA. Mol Plant Pathol 16:724–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soosaar JLM, Burch-Smith TM, Dinesh-Kumar SP (2005) Mechanisms of plant resistance to viruses. Nat Rev Microbiol 3:789–798

    Article  CAS  PubMed  Google Scholar 

  • Tamilarasan S (2012) Engineering crop plants for nematode resistance through host-derived RNA interference. Cell Dev Biol https://doi.org/10.4172/2168-9296.1000114

  • Tavladoraki P, Benvenuto E, Trinca S, De Martinis D, Cattaneo A, Galeffi P (1993) Transgenic plants expressing a functional single-chain Fv antibody are specifically protected from virus attack. Nature 366:469–472

    Article  CAS  PubMed  Google Scholar 

  • Tepfer M, Jacquemond M, García-Arenal F (2015) A critical evaluation of whether recombination in virus-resistant transgenic plants will lead to the emergence of novel viral diseases. New Phytol 207:536–541

    Article  CAS  PubMed  Google Scholar 

  • Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465

    Article  CAS  PubMed  Google Scholar 

  • van Schie CCN, Takken FLW (2014) Susceptibility genes 101: how to be a good host. Annu Rev Phytopathol 52:551–581

    Article  PubMed  CAS  Google Scholar 

  • Vadlamudi T, Patil BL, Kaldis A, Sai Gopal DVR, Mishra R, Berbati M, Voloudakis A (2020) DsRNA-mediated protection against two isolates of papaya ringspot virus through topical application of dsRNA in papaya. J Virol Methods 275:113750

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H, Béclin C, Fagard M (2001) Post-transcriptional gene silencing in plants. J Cell Sci 114:3083–3091

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H, Fagard M (2001) Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet 17:29–35

    Article  CAS  PubMed  Google Scholar 

  • Voloudakis AE, Holeva MC, Sarin LP, Bamford DH, Vargas M, Poranen MM, Tenllado F (2015) Efficient double-stranded RNA production methods for utilization in plant virus control. Methods Molecular Biology. Springer, New York, United States, pp 255–274

    Google Scholar 

  • Van VuT, Roy Choudhury N, Mukherjee SK (2013) Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res 172:35–45

    Article  CAS  Google Scholar 

  • Wang A, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 13:795–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Yang X, Wang Y, Xie Y, Zhou X (2018) Tomato yellow leaf curl virus V2 interacts with host histone deacetylase 6 to suppress methylation-mediated transcriptional gene silencing in plants. J Virol 92:e00036-e118

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, Wang C, Xu W, Zou J, Qiu Y, Kong J, Yang Y, Zhang B, Zhu S (2018) Epigenetic changes in the regulation of Nicotiana tabacum response to cucumber mosaic virus infection and symptom recovery through single-base resolution methylomes. Viruses 10:402

    Article  PubMed Central  CAS  Google Scholar 

  • Wang C, Wang C, Zou J, Yang Y, Li Z, Zhu S (2019) Epigenetics in the plant–virus interaction. Plant Cell Rep 38:1031–1038

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Mei J, Ren G (2019) Plant microRNAs: Biogenesis, homeostasis, and degradation. Front Plant Sci 10:1–12

    Google Scholar 

  • Wang M-B, Masuta C, Smith NA, Shimura H (2012) RNA silencing and plant viral diseases. Mol Plant-Microbe Interact 25:1275–1285

    Article  CAS  PubMed  Google Scholar 

  • Wang X-B, Wu Q, Ito T, Cillo F, Li W-X, Chen X, Yu J-L, Ding S-W (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:484–489

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wu Y, Gong Q, Ismayil A, Yuan Y, Lian B, Jia Q, Han M, Deng H, Hong Y et al (2019) Geminiviral V2 protein suppresses transcriptional gene silencing through interaction with AGO4. J Virol 93:e01675-e1718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wassenegger M, Heimes S, Riedel L, Sänger HL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76:567–576

    Article  CAS  PubMed  Google Scholar 

  • Waterhouse PM, Wang M-B, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842

    Article  CAS  PubMed  Google Scholar 

  • Yang DL, Zhang G, Tang K, Li J, Yang L, Huang H, Zhang H, Zhu JK (2016) Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res 26:66–82

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Xu Z, Zhao W, Liu Q, Li Q, Lu L, Liu R, Zhang X, Cui F (2018) Rice stripe virus-derived siRNAs play different regulatory roles in rice and in the insect vector Laodelphax striatellus. BMC Plant Biol 18:1–13

    Article  CAS  Google Scholar 

  • Zaidi SS-A, Mansoor S (2017) Viral vectors for plant genome engineering. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00539

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaidi SS-A, Mukhtar MS, Mansoor S (2018) Genome editing: targeting susceptibility genes for plant disease resistance. Trends Biotechnol 36:898–906

    Article  CAS  PubMed  Google Scholar 

  • Zaidi SS-A, Tashkandi M, Mansoor S, Mahfouz MM (2016) Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01673

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Feng H, Lu X, Wang C, Yang W, Li F (2019) An asymmetric bulge enhances artificial micro RNA‐mediated virus resistance. Plant Biotechnol J pbi. 13250

    Google Scholar 

  • Zhang H, Lang Z, Zhu JK (2018) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19:489–506

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Xia R, Kuang H, Meyers BC (2016) The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Mol Biol Evol 33:2692–2705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann S, Schillberg S, Liao YC, Fisher R (1998) Intracellular expression of TMV-specific single-chain Fv fragments leads to improved virus resistance in Nicotiana tabacum. Mol Breed 4:369–379

    Article  CAS  Google Scholar 

  • Zorzatto C, Machado JPB, Lopes KVG, Nascimento KJT, Pereira WA, Brustolini OJB, Reis PAB, Calil IP, Deguchi M, Sachetto-Martins G et al (2015) NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature 520:679–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Members of the Voloudakis’ group at the Agricultural University of Athens, Greece are acknowledged for their research contributions and discussions.

Part of the data presented in this review have been obtained in the frame of the projects:

(a) ‘Pythagoras II’ funded by General Secretariat of Research and Technology of Greece.

(b) ‘sRNAvac’ funded by General Secretariat of Research and Technology of Greece.

(c) ‘COST FA0806′ funded by Cooperation in Science & Technology (COST), EU.

(d) ‘Erasmus Mundus Action BRAVE’ funded by Education, Audiovisual and Culture Executive Agency, EU.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andreas E. Voloudakis .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Voloudakis, A.E., Mukherjee, S.K., Roy, A. (2021). Novel Technologies for Transgenic Management for Plant Virus Resistance. In: Sarmah, B.K., Borah, B.K. (eds) Genome Engineering for Crop Improvement. Concepts and Strategies in Plant Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-63372-1_7

Download citation

Publish with us

Policies and ethics