1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Virology
  4. Volume 9, 2022
  5. Article

Annual Review of Virology

Volume 9, 2022

RNA-Based Vaccination of Plants for Control of Viruses

Abstract

Plant viruses cause nearly half of the emerging plant diseases worldwide, contributing to 10–15% of crop yield losses. Control of plant viral diseases is mainly accomplished by extensive chemical applications targeting the vectors (i.e., insects, nematodes, fungi) transmitting these viruses. However, these chemicals have a significant negative effect on human health and the environment. RNA interference is an endogenous, cellular, sequence-specific RNA degradation mechanism in eukaryotes induced by double-stranded RNA molecules that has been exploited as an antiviral strategy through transgenesis. Because genetically modified crop plants are not accepted for cultivation in several countries globally, there is an urgent demand for alternative strategies. This has boosted research on exogenous application of the RNA-based biopesticides that are shown to exhibit significant protective effect against viral infections. Such environment-friendly and efficacious antiviral agents for crop protection will contribute to global food security, without adverse effects on human health.

Keyword(s): amiRNAs, antiviral plant resistance, dsRNA, epigenetics, RNAi, siRNA, tasiRNAs
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-091919-073708
2022-09-29
2024-04-29
Loading full text...

Full text loading...

/deliver/fulltext/virology/9/1/annurev-virology-091919-073708.html?itemId=/content/journals/10.1146/annurev-virology-091919-073708&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A 2019. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3:3430–39
     [Crossref] [Google Scholar]
  2. 2.
    Eur. Comm 2019. The European Green Deal. Eur. Comm. 53:924
     [Google Scholar]
  3. 3.
    Patil BL. 2021. Plant viral diseases: economic implications. Encyclopedia of Virology D Bamford, M Zuckerman 81–97 Amsterdam: Elsevier. , 4th ed..
     [Google Scholar]
  4. 4.
    Patil BL, Fauquet CM. 2021. Ecology of plant viruses, with special reference to Geminiviruses. Studies in Viral Ecology CJ Hurst 183–229 Hoboken, NJ: Wiley
     [Google Scholar]
  5. 5.
    Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D. 2000. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit. Rev. Biochem. Mol. Biol. 35:2105–40
     [Google Scholar]
  6. 6.
    Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. 2013. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat. Rev. Microbiol. 11:11777–88
     [Crossref] [Google Scholar]
  7. 7.
    Jones RA. 2004. Using epidemiological information to develop effective integrated virus disease management strategies. Virus Res 100:15–30
     [Crossref] [Google Scholar]
  8. 8.
    Van Den Bosch F, Jeger MJ, Gilligan CA. 2007. Disease control and its selection for damaging plant virus strains in vegetatively propagated staple food crops; a theoretical assessment. Proc. R. Soc. B 274:160611–18
     [Crossref] [Google Scholar]
  9. 9.
    Wang QC, Valkonen JPT. 2009. Cryotherapy of shoot tips: novel pathogen eradication method. Trends Plant Sci 14:119–22
     [Crossref] [Google Scholar]
  10. 10.
    Saeed ST, Samad A. 2017. Emerging threats of begomoviruses to the cultivation of medicinal and aromatic crops and their management strategies. VirusDisease 28:11–17
     [Crossref] [Google Scholar]
  11. 11.
    Konam J, Namaliu Y, Daniel R, Guest D. 2011. Integrated Pest and Disease Management for Sustainable Cocoa Production: A Training Manual for Farmers and Extension Workers Canberra, Aust.: ACIAR
  12. 12.
    Cillo F, Palukaitis P. 2014. Transgenic resistance. Adv. Virus Res. 90:35–146
     [Crossref] [Google Scholar]
  13. 13.
    Patil B. 2018. Genetic engineering for virus resistance in plants: principles and methods. Genes, Genetics and Transgenics for Virus Resistance in Plants101–16 Norfolk, UK: Caister
     [Google Scholar]
  14. 14.
    Sanford JC, Johnston SA. 1985. The concept of parasite-derived resistance—deriving resistance genes from the parasite's own genome. J. Theor. Biol. 113:2395–405
     [Crossref] [Google Scholar]
  15. 15.
    Abel P, Nelson R, De B, Hoffmann N, Rogers S et al. 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:4751738–43
     [Crossref] [Google Scholar]
  16. 16.
    Beachy RN, Loesch-Fries S, Turner NE. 1990. Coat protein-mediated resistance against virus infection. Annu. Rev. Phytopathol. 28:451–74
     [Crossref] [Google Scholar]
  17. 17.
    Tricoll DM, Carney KJ, Russell PF, McMaster JR, Groff DW et al. 1995. Field evaluation of transgenic squash containing single or multiple virus coat protein gene constructs for resistance to cucumber mosaic virus, watermelon mosaic virus 2 and zucchini yellow mosaic virus. Nat. Biotechnol. 13:121458–65
     [Crossref] [Google Scholar]
  18. 18.
    Scorza R, Callahan A, Dardick C, Ravelonandro M, Polak J et al. 2013. Genetic engineering of Plum pox virus resistance: “HoneySweet” plum—from concept to product. Plant Cell Tissue Organ Cult 115:11–12
     [Crossref] [Google Scholar]
  19. 19.
    Pooggin MM. 2017. RNAi-mediated resistance to viruses: a critical assessment of methodologies. Curr. Opin. Virol. 26:28–35
     [Crossref] [Google Scholar]
  20. 20.
    Hsu PD, Lander ES, Zhang F. 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:61262–78
     [Crossref] [Google Scholar]
  21. 21.
    Puchta H, Dujon B, Hohn B. 1996. Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. PNAS 93:105055–60
     [Crossref] [Google Scholar]
  22. 22.
    Cong L, Ran FA, Cox D, Lin S, Barretto R et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:6121819–23
     [Crossref] [Google Scholar]
  23. 23.
    Baulcombe D. 2004. RNA silencing in plants. Nature 431:7006356–63
     [Crossref] [Google Scholar]
  24. 24.
    Csorba T, Pantaleo V, Burgyán J. 2009. RNA silencing: an antiviral mechanism. Adv. Virus Res. 75:35–71
     [Crossref] [Google Scholar]
  25. 25.
    Mlotshwa S, Pruss GJ, Vance V. 2008. Small RNAs in viral infection and host defense. Trends Plant Sci 13:7375–82
     [Crossref] [Google Scholar]
  26. 26.
    Lindbo JA. 2012. A historical overview of RNAi in plants. Antiviral Resistance in Plants JM Watson, M-B Wang 1–16 Totowa, NJ: Humana
     [Google Scholar]
  27. 27.
    Vaucheret H, Béclin C, Fagard M. 2001. Post-transcriptional gene silencing in plants. J. Cell Sci. 114:173083–91
     [Crossref] [Google Scholar]
  28. 28.
    Lindbo JA, Dougherty WG. 2005. Plant pathology and RNAi: a brief history. Annu. Rev. Phytopathol. 43:191–204
     [Crossref] [Google Scholar]
  29. 29.
    Szittya G, Silhavy D, Molnár A, Havelda Z, Lovas Á et al. 2003. Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:3633–40
     [Crossref] [Google Scholar]
  30. 30.
    Patil BL, Fauquet CM. 2015. Light intensity and temperature affect systemic spread of silencing signal in transient agroinfiltration studies. Mol. Plant Pathol. 16:5484–94
     [Crossref] [Google Scholar]
  31. 31.
    Patil BL, Fauquet CM. 2015. Studies on differential behavior of cassava mosaic geminivirus DNA components, symptom recovery patterns, and their siRNA profiles. Virus Genes 50:3474–86
     [Crossref] [Google Scholar]
  32. 32.
    Tenllado F, Llave C, Díaz-Ruíz JR. 2004. RNA interference as a new biotechnological tool for the control of virus diseases in plants. Virus Res 102:185–96
     [Crossref] [Google Scholar]
  33. 33.
    Waterhouse PM, Fusaro AF. 2006. Viruses face a double defense by plant small RNAs. Science 313:578354–55
     [Crossref] [Google Scholar]
  34. 34.
    Klas FE, Fuchs M, Gonsalves D. 2006. Comparative spatial spread overtime of Zucchini Yellow Mosaic Virus (ZYMV) and Watermelon Mosaic Virus (WMV) in fields of transgenic squash expressing the coat protein genes of ZYMV and WMV, and in fields of nontransgenic squash. Transgenic Res 15:5527–41
     [Crossref] [Google Scholar]
  35. 35.
    Thomas PE, Lawson EC, Zalewski JC, Reed GL, Kaniewski WK. 2000. Extreme resistance to Potato leafroll virus in potato cv. Russet Burbank mediated by the viral replicase gene. Virus Res 71:1–249–62
     [Crossref] [Google Scholar]
  36. 36.
    Hily JM, Scorza R, Malinowski T, Zawadzka B, Ravelonandro M. 2004. Stability of gene silencing-based resistance to Plum pox virus in transgenic plum (Prunus domestica L.) under field conditions. Transgenic Res 13:5427–36
     [Crossref] [Google Scholar]
  37. 37.
    Kundu JK, Briard P, Hily JM, Ravelonandro M, Scorza R. 2008. Role of the 25–26 nt siRNA in the resistance of transgenic Prunus domestica graft inoculated with plum pox virus. Virus Genes 36:1215–20
     [Crossref] [Google Scholar]
  38. 38.
    Krubphachaya P, Juříček M, Kertbundit S. 2007. Induction of RNA-mediated resistance to papaya ringspot virus type W. J. Biochem. Mol. Biol. 40:3404–11
     [Google Scholar]
  39. 39.
    Patil BL, Ogwok E, Wagaba H, Mohammed IU, Yadav JS et al. 2011. RNAi-mediated resistance to diverse isolates belonging to two virus species involved in Cassava brown streak disease. Mol. Plant Pathol. 12:131–41
     [Crossref] [Google Scholar]
  40. 40.
    Patil BL, Bagewadi B, Yadav JS, Fauquet CM. 2016. Mapping and identification of cassava mosaic geminivirus DNA-A and DNA-B genome sequences for efficient siRNA expression and RNAi based virus resistance by transient agro-infiltration studies. Virus Res 213:109–15
     [Crossref] [Google Scholar]
  41. 41.
    Yadav JS, Ogwok E, Wagaba H, Patil BL, Bagewadi B et al. 2011. RNAi-mediated resistance to Cassava brown streak Uganda virus in transgenic cassava. Mol. Plant Pathol. 12:7677–87
     [Crossref] [Google Scholar]
  42. 42.
    Pooggin M, Shivaprasad PV, Veluthambi K, Hohn T. 2003. RNAi targeting of DNA virus in plants. Nat. Biotechnol. 21:2131–32
     [Crossref] [Google Scholar]
  43. 43.
    Kumar S, Tanti B, Patil BL, Mukherjee SK, Sahoo L. 2017. RNAi-derived transgenic resistance to Mungbean yellow mosaic India virus in cowpea. PLOS ONE 12:10e0186786
     [Crossref] [Google Scholar]
  44. 44.
    Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–11
     [Crossref] [Google Scholar]
  45. 45.
    Ratcliff F, Harrison BD, Baulcombe DC. 1997. A similarity between viral defense and gene silencing in plants. Science 276:53181558–60
     [Crossref] [Google Scholar]
  46. 46.
    Baulcombe D. 2002. Viral suppression of systemic silencing. Trends Microbiol 10:7306–8
     [Crossref] [Google Scholar]
  47. 47.
    Kim VN. 2005. Small RNAs: classification, biogenesis, and function. Mol. Cells 19:11–15
     [Crossref] [Google Scholar]
  48. 48.
    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
     [Crossref] [Google Scholar]
  49. 49.
    Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O. 2006. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:578368–71
     [Crossref] [Google Scholar]
  50. 50.
    Gasciolli V, Mallory AC, Bartel DP, Vaucheret H. 2005. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15:161494–500
     [Crossref] [Google Scholar]
  51. 51.
    Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N et al. 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 22:2481–96
     [Crossref] [Google Scholar]
  52. 52.
    Wang X-B, Jovel J, Udomporn P, Wang Y, Wu Q et al. 2011. The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative Argonautes in Arabidopsis thaliana. Plant Cell 23:41625–38
     [Crossref] [Google Scholar]
  53. 53.
    Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD et al. 2004. Genetic and functional diversification of small RNA pathways in plants. PLOS Biol 2:5E104
     [Crossref] [Google Scholar]
  54. 54.
    Diaz-Pendon JA, Li F, Li W-X, Ding S-W. 2007. Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19:62053–63
     [Crossref] [Google Scholar]
  55. 55.
    Rosa C, Kuo YW, Wuriyanghan H, Falk BW. 2018. RNA interference mechanisms and applications in plant pathology. Annu. Rev. Phytopathol. 56:581–610
     [Crossref] [Google Scholar]
  56. 56.
    Zhang S, Liu Y, Yu B 2015. New insights into pri-miRNA processing and accumulation in plants. Wiley Interdiscip. Rev. RNA 6:5533–45
     [Crossref] [Google Scholar]
  57. 57.
    Jaubert M, Bhattacharjee S, Mello AFS, Perry KL, Moffett P. 2011. ARGONAUTE2 mediates RNA-silencing antiviral defenses against Potato virus X in Arabidopsis. Plant Physiol 156:31556–64
     [Crossref] [Google Scholar]
  58. 58.
    Raja P, Sanville BC, Buchmann RC, Bisaro DM. 2008. Viral genome methylation as an epigenetic defense against geminiviruses. J. Virol. 82:188997–9007
     [Crossref] [Google Scholar]
  59. 59.
    Zilberman D, Cao X, Jacobsen SE. 2003. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:5607716–19
     [Crossref] [Google Scholar]
  60. 60.
    Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S et al. 2014. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157:51050–60
     [Crossref] [Google Scholar]
  61. 61.
    Salaman RN, Smith KM, MacClement WD, Bawden FC, Bernal JD et al. 1938. A discussion on new aspects of virus disease. Proc. R. Soc. B 125:291–310
     [Google Scholar]
  62. 62.
    Ziebell H, Carr JP. 2010. Cross-protection: a century of mystery. Adv. Virus Res. 76:10211–64
     [Crossref] [Google Scholar]
  63. 63.
    Gal-On A, Shiboleth YM. 2006. Cross-protection. Natural Resistance Mechanisms of Plants to Viruses G Loebenstein, JP Carr 261–88 Dordrecht, Neth.: Springer Netherlands
     [Google Scholar]
  64. 64.
    Pechinger K, Chooi KM, MacDiarmid RM, Harper SJ, Ziebell H. 2019. A new era for mild strain cross-protection. Viruses 11:7670
     [Crossref] [Google Scholar]
  65. 65.
    Ziebell H, MacDiarmid R. 2017. Prospects for engineering and improvement of cross-protective virus strains. Curr. Opin. Virol. 26:8–14
     [Crossref] [Google Scholar]
  66. 66.
    Folimonova SY. 2013. Developing an understanding of cross-protection by Citrus tristeza virus. Front. Microbiol. 4:76
     [Crossref] [Google Scholar]
  67. 67.
    Muller GW, Rezende JAM 2006. Preimmunization: applications and perspectives in virus disease control. Diseases of Fruits and Vegetables, Vol. I SAMH Naqvi 361–95 Dordrecht, Neth.: Kluwer
     [Google Scholar]
  68. 68.
    Jones RAC, Koenig R, Lesemann DE. 1980. Pepino mosaic virus, a new potexvirus from pepino (Solanum muricatum). Ann. Appl. Biol. 94:161–68
     [Crossref] [Google Scholar]
  69. 69.
    Sherwood JL, Fulton RW. 1982. The specific involvement of coat protein in tobacco mosaic virus cross protection. Virology 119:1150–58
     [Crossref] [Google Scholar]
  70. 70.
    Folimonova SY, Robertson CJ, Shilts T, Folimonov AS, Hilf ME et al. 2010. Infection with strains of Citrus tristeza virus does not exclude superinfection by other strains of the virus. J. Virol. 84:31314–25
     [Crossref] [Google Scholar]
  71. 71.
    Folimonova SY. 2012. Superinfection exclusion is an active virus-controlled function that requires a specific viral protein. J. Virol. 86:105554–61
     [Crossref] [Google Scholar]
  72. 72.
    Bergua M, Zwart MP, El-Mohtar C, Shilts T, Elena SF, Folimonova SY. 2014. A viral protein mediates superinfection exclusion at the whole-organism level but is not required for exclusion at the cellular level. J. Virol. 88:1911327–38
     [Crossref] [Google Scholar]
  73. 73.
    Sun Y-D, Folimonova SY. 2019. The p33 protein of Citrus tristeza virus affects viral pathogenicity by modulating a host immune response. New Phytol 221:42039–53
     [Crossref] [Google Scholar]
  74. 74.
    Duan C-G, Fang Y-Y, Zhou B-J, Zhao J-H, Hou W-N et al. 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 24:1259–74
     [Crossref] [Google Scholar]
  75. 75.
    Smith NA, Singh SP, Wang M-B, Stoutjesdijk PA, Green AG, Waterhouse PM. 2000. Total silencing by intron-spliced hairpin RNAs. Nature 407:6802319–20
     [Crossref] [Google Scholar]
  76. 76.
    Waterhouse PM, Helliwell CA. 2003. Exploring plant genomes by RNA-induced gene silencing. Nat. Rev. Genet. 4:129–38
     [Crossref] [Google Scholar]
  77. 77.
    Béclin C, Boutet S, Waterhouse P, Vaucheret H. 2002. A branched pathway for transgene-induced RNA silencing in plants. Curr. Biol. 12:8684–88
     [Crossref] [Google Scholar]
  78. 78.
    Waterhouse PM, Graham MW, Wang M-B. 1998. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. PNAS 95:2313959–64
     [Crossref] [Google Scholar]
  79. 79.
    Wesley SV, Helliwell CA, Smith NA, Wang M, Rouse DT et al. 2001. Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27:6581–90
     [Crossref] [Google Scholar]
  80. 80.
    Dietzgen RG, Mitter N. 2006. Transgenic gene silencing strategies for virus control. Australas. Plant Pathol. 35:6605–18
     [Crossref] [Google Scholar]
  81. 81.
    Bucher E, Lohuis D, van Poppel PMJA, Geerts-Dimitriadou C, Goldbach R, Prins M. 2006. Multiple virus resistance at a high frequency using a single transgene construct. J. Gen. Virol. 87:123697–701
     [Crossref] [Google Scholar]
  82. 82.
    Birch RG, Shen B, Sawyer BJB, Huttner E, Tucker WQJ, Betzner AS. 2010. Evaluation and application of a luciferase fusion system for rapid in vivo analysis of RNAi targets and constructs in plants. Plant Biotechnol. J. 8:4465–75
     [Crossref] [Google Scholar]
  83. 83.
    Kalantidis K, Psaradakis S, Tabler M, Tsagris M. 2002. The occurrence of CMV-specific short RNAs in transgenic tobacco expressing virus-derived double-stranded RNA is indicative of resistance to the virus. Mol. Plant-Microbe Interact. 15:8826–33
     [Crossref] [Google Scholar]
  84. 84.
    Wang MB, Waterhouse PM. 2002. Application of gene silencing in plants. Curr. Opin. Plant Biol. 5:2146–50
     [Crossref] [Google Scholar]
  85. 85.
    Tenllado F, Díaz-Ruíz JR. 2001. Double-stranded RNA-mediated interference with plant virus infection. J. Virol. 75:2412288–97
     [Crossref] [Google Scholar]
  86. 86.
    Peach C, Velten J. 1991. Transgene expression variability (position effect) of CAT and GUS reporter genes driven by linked divergent T-DNA promoters. Plant Mol. Biol. 17:149–60
     [Crossref] [Google Scholar]
  87. 87.
    Vargas M, Martínez-García B, Díaz-Ruíz JR, Tenllado F. 2008. Transient expression of homologous hairpin RNA interferes with PVY transmission by aphids. Virol. J. 5:142
     [Crossref] [Google Scholar]
  88. 88.
    Voloudakis AE, Holeva MC, Sarin LP, Bamford DH, Vargas M et al. 2015. Efficient double-stranded RNA production methods for utilization in plant virus control. Methods Mol. Biol. 1236:255–74
     [Crossref] [Google Scholar]
  89. 89.
    Maxwell B, Boyes D, Tang J, Rodrigues T, Desai S et al. 2018. Enabling the RNA revolution, cell-free dsRNA production and control of Colorado potato beetle Poster GreenLight Biosciences Medford, MA: http://www.globalengage.co.uk/pgc/docs/PosterMaxwell.pdf
  90. 90.
    Taning CNT, Mezzetti B, Kleter G, Smagghe G, Baraldi E. 2021. Does RNAi-based technology fit within EU sustainability goals?. Trends Biotechnol 39:7644–47
     [Crossref] [Google Scholar]
  91. 91.
    Koch A, Höfle L, Werner BT, Imani J, Schmidt A et al. 2019. SIGS vs HIGS: a study on the efficacy of two dsRNA delivery strategies to silence Fusarium FgCYP51 genes in infected host and non-host plants. Mol. Plant Pathol. 20:121636–44
     [Crossref] [Google Scholar]
  92. 92.
    Dalakouras A, Wassenegger M, McMillan JN, Cardoza V, Maegele I et al. 2016. Induction of silencing in plants by high-pressure spraying of in vitro-synthesized small RNAs. Front. Plant Sci. 7:1327
     [Crossref] [Google Scholar]
  93. 93.
    Hendrix B, Hoffer P, Sanders R, Schwartz S, Zheng W et al. 2021. Systemic GFP silencing is associated with high transgene expression in Nicotiana benthamiana. PLOS ONE 16:3e0245422
     [Crossref] [Google Scholar]
  94. 94.
    Zhu KY, Palli SR. 2020. Mechanisms, applications, and challenges of insect RNA interference. Annu. Rev. Entomol. 65:293–311
     [Crossref] [Google Scholar]
  95. 95.
    Gebremichael DE, Haile ZM, Negrini F, Sabbadini S, Capriotti L et al. 2021. RNA interference strategies for future management of plant pathogenic fungi: prospects and challenges. Plants 10:4650
     [Crossref] [Google Scholar]
  96. 96.
    Reis RS, Hart-Smith G, Eamens AL, Wilkins MR, Waterhouse PM. 2015. Gene regulation by translational inhibition is determined by Dicer partnering proteins. Nat. Plants 1:314027
     [Crossref] [Google Scholar]
  97. 97.
    Wang J, Mei J, Ren G. 2019. Plant microRNAs: biogenesis, homeostasis, and degradation. Front. Plant Sci. 10:360
     [Crossref] [Google Scholar]
  98. 98.
    Shweta, Akhter Y, Khan JA. 2018. Genome wide identification of cotton (Gossypium hirsutum)-encoded microRNA targets against Cotton leaf curl Burewala virus. Gene 638:60–65
     [Crossref] [Google Scholar]
  99. 99.
    Akmal M, Baig MS, Khan JA. 2017. Suppression of cotton leaf curl disease symptoms in Gossypium hirsutum through over expression of host-encoded miRNAs. J. Biotechnol. 263:21–29
     [Crossref] [Google Scholar]
  100. 100.
    Wang H, Jiao X, Kong X, Hamera S, Wu Y et al. 2016. A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol 170:42365–77
     [Crossref] [Google Scholar]
  101. 101.
    Cao M, Du P, Wang X, Yu Y-Q, Qiu Y-H et al. 2014. Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis. PNAS 111:4014613–18
     [Crossref] [Google Scholar]
  102. 102.
    Deng P, Muhammad S, Cao M, Wu L. 2018. Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol. J. 16:5965–75
     [Crossref] [Google Scholar]
  103. 103.
    Zhao M, Cai C, Zhai J, Lin F, Li L et al. 2015. Coordination of microRNAs, phasiRNAs, and NB-LRR genes in response to a plant pathogen: insights from analyses of a set of soybean Rps gene near-isogenic lines. Plant Genome 8:1plantgenome2014.09.0044
     [Crossref] [Google Scholar]
  104. 104.
    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 32:1157–58
     [Crossref] [Google Scholar]
  105. 105.
    Gago-Zachert S, Schuck J, Weinholdt C, Knoblich M, Pantaleo V et al. 2019. Highly efficacious antiviral protection of plants by small interfering RNAs identified in vitro. Nucleic Acids Res 47:179343–57
     [Crossref] [Google Scholar]
  106. 106.
    Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH et al. 2009. RNAi in budding yeast. Science 326:5952544–50
     [Crossref] [Google Scholar]
  107. 107.
    Pantaleo V, Rubino L, Russo M. 2003. Replication of Carnation Italian ringspot virus defective interfering RNA in Saccharomyces cerevisiae. J. Virol. 77:32116–23
     [Crossref] [Google Scholar]
  108. 108.
    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 13:2304–16
     [Crossref] [Google Scholar]
  109. 109.
    Ali I, Amin I, Briddon RW, Mansoor S. 2013. Artificial microRNA-mediated resistance against the monopartite begomovirus Cotton leaf curl Burewala virus. Virol. J. 10:231
     [Crossref] [Google Scholar]
  110. 110.
    Duan C-G, Wang C-H, Fang R-X, Guo H-S. 2008. Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J. Virol. 82:2211084–95
     [Crossref] [Google Scholar]
  111. 111.
    Mitter N, Zhai Y, Bai AX, Chua K, Eid S et al. 2016. Evaluation and identification of candidate genes for artificial microRNA-mediated resistance to tomato spotted wilt virus. Virus Res 211:151–58
     [Crossref] [Google Scholar]
  112. 112.
    Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW et al. 2006. Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat. Biotechnol. 24:111420–28
     [Crossref] [Google Scholar]
  113. 113.
    Van Vu T, Choudhury NR, Mukherjee SK. 2013. Transgenic tomato plants expressing artificial micro-RNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res 172:1–235–45
     [Google Scholar]
  114. 114.
    Wagaba H, Patil BL, Mukasa S, Alicai T, Fauquet CM, Taylor NJ. 2016. Artificial microRNA-derived resistance to Cassava brown streak disease. J. Virol. Methods 231:38–43
     [Crossref] [Google Scholar]
  115. 115.
    Liu P, Zhang X, Zhang F, Xu M, Ye Z et al. 2021. A virus-derived siRNA activates plant immunity by interfering with ROS scavenging. Mol. Plant 14:71088–103
     [Crossref] [Google Scholar]
  116. 116.
    Carbonell A, Lisón P, Daròs JA. 2019. Multi-targeting of viral RNAs with synthetic trans-acting small interfering RNAs enhances plant antiviral resistance. Plant J 100:4720–37
     [Crossref] [Google Scholar]
  117. 117.
    Singh A, Mohorianu I, Green D, Dalmay T, Dasgupta I, Mukherjee SK. 2019. Artificially induced phased siRNAs promote virus resistance in transgenic plants. Virology 537:208–15
     [Crossref] [Google Scholar]
  118. 118.
    Chen L, Cheng X, Cai J, Zhan L, Wu X et al. 2016. Multiple virus resistance using artificial trans-acting siRNAs. J. Virol. Methods 228:16–20
     [Crossref] [Google Scholar]
  119. 119.
    Liu Q, Li Y, Xu K, Li D, Hu H et al. 2020. Clay nanosheet-mediated delivery of recombinant plasmids expressing artificial miRNAs via leaf spray to prevent infection by plant DNA viruses. Hortic. Res. 7:1179
     [Crossref] [Google Scholar]
  120. 120.
    Golestanipour A, Nikkhah M, Aalami A, Hosseinkhani S. 2018. Gene delivery to tobacco root cells with single-walled carbon nanotubes and cell-penetrating fusogenic peptides. Mol. Biotechnol. 60:12863–78
     [Crossref] [Google Scholar]
  121. 121.
    Betti F, Ladera-Carmona MJ, Weits DA, Ferri G, Iacopino S et al. 2021. Exogenous miRNAs induce post-transcriptional gene silencing in plants. Nat. Plants 7:101379–88
     [Crossref] [Google Scholar]
  122. 122.
    Senthil-Kumar M, Mysore KS. 2011. Caveat of RNAi in plants: the off-target effect. Methods Mol. Biol. 744:13–25
     [Crossref] [Google Scholar]
  123. 123.
    Demirer GS, Zhang H, Goh NS, Pinals RL, Chang R, Landry MP 2020. Carbon nanocarriers deliver siRNA to intact plant cells for efficient gene knockdown. Sci. Adv. 6:26eaqz0495
     [Crossref] [Google Scholar]
  124. 124.
    Wassenegger M, Heimes S, Riedel L, Sänger HL. 1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76:3567–76
     [Crossref] [Google Scholar]
  125. 125.
    Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:6394–408
     [Crossref] [Google Scholar]
  126. 126.
    Zhang H, Lang Z, Zhu JK. 2018. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19:8489–506
     [Crossref] [Google Scholar]
  127. 127.
    Wang C, Wang C, Zou J, Yang Y, Li Z, Zhu S. 2019. Epigenetics in the plant-virus interaction. Plant Cell Rep 38:91031–38
     [Crossref] [Google Scholar]
  128. 128.
    Diezma-Navas L, Pérez-González A, Artaza H, Alonso L, Caro E et al. 2019. Crosstalk between epigenetic silencing and infection by tobacco rattle virus in Arabidopsis. Mol. Plant Pathol. 20:101439–52
     [Crossref] [Google Scholar]
  129. 129.
    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. 100:151–62
     [Crossref] [Google Scholar]
  130. 130.
    Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN et al. 2015. Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nat. Plants 1:1015145
     [Crossref] [Google Scholar]
  131. 131.
    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. 83:31332–40
     [Crossref] [Google Scholar]
  132. 132.
    Wang M-B, Masuta C, Smith NA, Shimura H. 2012. RNA silencing and plant viral diseases. Mol. Plant-Microbe Interact. 25:101275–85
     [Crossref] [Google Scholar]
  133. 133.
    Pooggin M. 2013. How can plant DNA viruses evade siRNA-directed DNA methylation and silencing?. Int. J. Mol. Sci. 14:815233–59
     [Crossref] [Google Scholar]
  134. 134.
    Brocard M, Ruggieri A, Locker N. 2017. m6A RNA methylation, a new hallmark in virus-host interactions. J. Gen. Virol. 98:92207–14
     [Crossref] [Google Scholar]
  135. 135.
    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. PNAS 114:4010755–60
     [Crossref] [Google Scholar]
  136. 136.
    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. 82:104823–33
     [Crossref] [Google Scholar]
  137. 137.
    Ding B, Wang G-L. 2015. Chromatin versus pathogens: the function of epigenetics in plant immunity. Front. Plant Sci. 6:675
     [Google Scholar]
  138. 138.
    Wang C, Wang C, Xu W, Zou J, Qiu Y et al. 2018. Epigenetic changes in the regulation of Nicotiana tabacum response to Cucumber mosaic virus infection and symptom recovery through single-base resolution methylomes. Viruses 10:8402
     [Crossref] [Google Scholar]
  139. 139.
    Espinas NA, Saze H, Saijo Y. 2016. Epigenetic control of defense signaling and priming in plants. Front. Plant Sci. 7:1201
     [Google Scholar]
  140. 140.
    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. 92:18e00036–18
     [Crossref] [Google Scholar]
  141. 141.
    Wang Y, Wu Y, Gong Q, Ismayil A, Yuan Y et al. 2019. Geminiviral V2 protein suppresses transcriptional gene silencing through interaction with AGO4. J. Virol. 93:6e01675–18
     [Google Scholar]
  142. 142.
    Thieme M, Bucher E. 2018. Transposable elements as tool for crop improvement. Adv. Bot. Res. 88:165–202
     [Crossref] [Google Scholar]
  143. 143.
    Kanazawa A, Inaba JI, Kasai M, Shimura H, Masuta C. 2011. RNA-mediated epigenetic modifications of an endogenous gene targeted by a viral vector: a potent gene silencing system to produce a plant that does not carry a transgene but has altered traits. Plant Signal. Behav. 6:81090–93
     [Crossref] [Google Scholar]
  144. 144.
    Otagaki S, Arai M, Takahashi A, Goto K, Hong JS et al. 2006. Rapid induction of transcriptional and post-transcriptional gene silencing using a novel Cucumber mosaic virus vector. Plant Biotechnol 23:3259–65
     [Crossref] [Google Scholar]
  145. 145.
    Dalmay T, Hamilton A, Mueller E, Baulcombe DC. 2000. Potato virus X amplicons in Arabidopsis mediate genetic and epigenetic gene silencing. Plant Cell 12:3369–79
     [Crossref] [Google Scholar]
  146. 146.
    Jones L, Ratcliff F, Baulcombe DC. 2001. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr. Biol. 11:10747–57
     [Crossref] [Google Scholar]
  147. 147.
    Mochizuki T, Ohki ST. 2004. Shoot meristem tissue of tobacco inoculated with Cucumber mosaic virus is infected with the virus and subsequently recovers from infection by RNA silencing. J. Gen. Plant Pathol. 70:6363–66
     [Crossref] [Google Scholar]
  148. 148.
    Pramanik D, Shelake RM, Kim MJ, Kim J-Y. 2021. CRISPR-mediated engineering across the central dogma in plant biology for basic research and crop improvement. Mol. Plant 14:1127–50
     [Crossref] [Google Scholar]
  149. 149.
    Langner T, Kamoun S, Belhaj K. 2018. CRISPR crops: plant genome editing toward disease resistance. Annu. Rev. Phytopathol. 56:479–512
     [Crossref] [Google Scholar]
  150. 150.
    Gallego-Bartolomé J. 2020. DNA methylation in plants: mechanisms and tools for targeted manipulation. New Phytol 227:138–44
     [Crossref] [Google Scholar]
  151. 151.
    Schwab F, Zhai G, Kern M, Turner A, Schnoor JL, Wiesner MR. 2016. Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in plants—critical review. Nanotoxicology 10:3257–78
     [Crossref] [Google Scholar]
  152. 152.
    Sanzari I, Leone A, Ambrosone A 2019. Nanotechnology in plant science: to make a long story short. Front. Bioeng. Biotechnol. 7:120
     [Crossref] [Google Scholar]
  153. 153.
    Carpita NC, Gibeaut DM. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:11–30
     [Crossref] [Google Scholar]
  154. 154.
    Thakur M, Pandey S, Mewada A, Patil V, Khade M et al. 2014. Antibiotic conjugated fluorescent carbon dots as a theranostic agent for controlled drug release, bioimaging, and enhanced antimicrobial activity. J. Drug Deliv. 2014:1–9
     [Crossref] [Google Scholar]
  155. 155.
    Schwartz SH, Hendrix B, Hoffer P, Sanders RA, Zheng W. 2020. Carbon dots for efficient small interfering RNA delivery and gene silencing in plants. Plant Physiol 184:2647–57
     [Crossref] [Google Scholar]
  156. 156.
    Zhang H, Cao Y, Xu D, Goh NS, Demirer GS et al. 2021. Gold-nanocluster-mediated delivery of siRNA to intact plant cells for efficient gene knockdown. Nano Lett 21:5859–66
     [Crossref] [Google Scholar]
  157. 157.
    Numata K, Ohtani M, Yoshizumi T, Demura T, Kodama Y. 2014. Local gene silencing in plants via synthetic dsRNA and carrier peptide. Plant Biotechnol. J. 12:81027–34
     [Crossref] [Google Scholar]
  158. 158.
    Kozielski KL, Tzeng SY, Green JJ. 2013. Bioengineered nanoparticles for siRNA delivery. WIREs Nanomed. Nanobiotechnol. 5:5449–68
     [Crossref] [Google Scholar]
  159. 159.
    Zhang H, Demirer GS, Zhang H, Ye T, Goh NS et al. 2019. DNA nanostructures coordinate gene silencing in mature plants. PNAS 116:157543–48
     [Crossref] [Google Scholar]
  160. 160.
    Mitter N, Worrall EA, Robinson KE, Li P, Jain RG et al. 2017. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 3:216207
     [Crossref] [Google Scholar]
  161. 161.
    Worrall EA, Bravo-Cazar A, Nilon AT, Fletcher SJ, Robinson KE et al. 2019. Exogenous application of RNAi-inducing double-stranded RNA inhibits aphid-mediated transmission of a plant virus. Front. Plant Sci. 10:265
     [Crossref] [Google Scholar]
  162. 162.
    Avital A, Muzika NS, Persky Z, Bar G, Michaeli Y et al. 2021. Foliar delivery of siRNA particles for treating viral infections in agricultural grapevines. Adv. Funct. Mater. 31:442101003
     [Crossref] [Google Scholar]
  163. 163.
    Zhang P, Li S, Chen M. 2020. Characterization and function of circular RNAs in plants. Front. Mol. Biosci. 7:91
     [Crossref] [Google Scholar]
  164. 164.
    Dietz-Pfeilstetter A, Mendelsohn M, Gathmann A, Klinkenbuß D. 2021. Considerations and regulatory approaches in the USA and in the EU for dsRNA-based externally applied pesticides for plant protection. Front. Plant Sci. 12:682387
     [Crossref] [Google Scholar]
  165. 165.
    Org. Econ. Coop. Dev. 2020. Considerations for the environmental risk assessment of the application of sprayed or externally applied ds-RNA-based pesticides Series 104 Org. Econ. Coop. Dev. Paris: https://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2020)26&doclanguage=en
  166. 166.
    Christiaens O, Dzhambazova T, Kostov K, Arpaia S, Joga MR et al. 2018. Literature review of baseline information on RNAi to support the environmental risk assessment of RNAi-based GM plants. EFSA Support. Publ. 15:51424E
     [Google Scholar]
  167. 167.
    Parker KM, Barragán Borrero V, Van Leeuwen DM, Lever MA, Mateescu B, Sander M 2019. Environmental fate of RNA interference pesticides: adsorption and degradation of double-stranded RNA molecules in agricultural soils. Environ. Sci. Technol. 53:63027–36
     [Crossref] [Google Scholar]
  168. 168.
    Bachman P, Fischer J, Song Z, Urbanczyk-Wochniak E, Watson G. 2020. Environmental fate and dissipation of applied dsRNA in soil, aquatic systems, and plants. Front. Plant Sci. 11:21
     [Crossref] [Google Scholar]
  169. 169.
    Konakalla NC, Kaldis A, Berbati M, Masarapu H, Voloudakis AE. 2016. Exogenous application of double-stranded RNA molecules from TMV p126 and CP genes confers resistance against TMV in tobacco. Planta 244:4961–69
     [Crossref] [Google Scholar]
  170. 170.
    Yin G, Sun Z, Liu N, Zhang L, Song Y et al. 2009. Production of double-stranded RNA for interference with TMV infection utilizing a bacterial prokaryotic expression system. Appl. Microbiol. Biotechnol. 84:2323–33
     [Crossref] [Google Scholar]
  171. 171.
    Sun ZN, Yin GH, Song YZ, An HL, Zhu CX, Wen FJ. 2010. Bacterially expressed double-stranded RNAs against hot-spot sequences of tobacco mosaic virus or potato virus Y genome have different ability to protect tobacco from viral infection. Appl. Biochem. Biotechnol. 162:71901–14
     [Crossref] [Google Scholar]
  172. 172.
    Rego-Machado CM, Nakasu EYT, Silva JMF, Lucinda N, Nagata T, Inoue-Nagata AK. 2020. siRNA biogenesis and advances in topically applied dsRNA for controlling virus infections in tomato plants. Sci. Rep. 10:122277
     [Crossref] [Google Scholar]
  173. 173.
    Tenllado F, Martínez-García B, Vargas M, Díaz-Ruíz JR. 2003. Crude extracts of bacterially expressed dsRNA can be used to protect plants against virus infections. BMC Biotechnol 3:3
     [Crossref] [Google Scholar]
  174. 174.
    Necira K, Makki M, Sanz-García E, Canto T, Djilani-Khouadja F, Tenllado F. 2021. Topical application of Escherichia coli-encapsulated dsRNA induces resistance in Nicotiana benthamiana to potato viruses and involves RDR6 and combined activities of DCL2 and DCL4. Plants 10:4644
     [Crossref] [Google Scholar]
  175. 175.
    Gan D, Zhang J, Jiang H, Jiang T, Zhu S, Cheng B. 2010. Bacterially expressed dsRNA protects maize against SCMV infection. Plant Cell Rep 29:111261–68
     [Crossref] [Google Scholar]
  176. 176.
    Vadlamudi T, Patil BL, Kaldis A Sai Gopal DVR , Mishra R et al. 2020. dsRNA-mediated protection against two isolates of Papaya ringspot virus through topical application of dsRNA in papaya. J. Virol. Methods 275:113750
     [Crossref] [Google Scholar]
  177. 177.
    Shen W, Yang G, Chen Y, Yan P, Tuo D et al. 2014. Resistance of non-transgenic papaya plants to papaya ringspot virus (PRSV) mediated by intron-containing hairpin dsRNAs expressed in bacteria. Acta Virol 58:3261–66
     [Crossref] [Google Scholar]
  178. 178.
    Kaldis A, Berbati M, Melita O, Reppa C, Holeva M et al. 2018. Exogenously applied dsRNA molecules deriving from the Zucchini yellow mosaic virus (ZYMV) genome move systemically and protect cucurbits against ZYMV. Mol. Plant Pathol. 19:4883–95
     [Crossref] [Google Scholar]
  179. 179.
    Holeva MC, Sklavounos A, Rajeswaran R, Pooggin MM, Voloudakis AE. 2021. Topical application of double-stranded RNA targeting 2b and CP genes of Cucumber mosaic virus protects plants against local and systemic viral infection. Plants 10:5963
     [Crossref] [Google Scholar]
  180. 180.
    Borah M, Berbati M, Reppa C, Holeva M, Nath PD, Voloudakis A. 2018. RNA-based vaccination of Bhut Jolokia pepper (Capsicum chinense Jacq.) against cucumber mosaic virus. VirusDisease 29:2207–11
     [Crossref] [Google Scholar]
  181. 181.
    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. 108:101432
     [Crossref] [Google Scholar]
  182. 182.
    Lau SE, Mazumdar P, Hee TW, Song ALA, Othman RY, Harikrishna JA. 2014. Crude extracts of bacterially-expressed dsRNA protect orchid plants against Cymbidium mosaic virus during transplantation from in vitro culture. J. Hortic. Sci. Biotechnol. 89:5569–76
     [Crossref] [Google Scholar]
  183. 183.
    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. 155:41345–52
     [Crossref] [Google Scholar]
  184. 184.
    Tabein S, Jansen M, Noris E, Vaira AM, Marian D et al. 2020. The induction of an effective dsRNA-mediated resistance against tomato spotted wilt virus by exogenous application of double-stranded RNA largely depends on the selection of the viral RNA target region. Front. Plant Sci. 11:533338
     [Crossref] [Google Scholar]
  185. 185.
    Konakalla NC, Bag S, Deraniyagala AS, Culbreath AK, Pappu HR. 2021. Induction of plant resistance in tobacco (Nicotiana tabacum) against tomato spotted wilt orthotospovirus through foliar application of dsRNA. Viruses 13:4662
     [Crossref] [Google Scholar]
  186. 186.
    Patil BL, Raghu R, Dangwal M, Byregowda M, Voloudakis A. 2021. Exogenous dsRNA-mediated field protection against Pigeonpea sterility mosaic emaravirus. J. Plant Biochem. Biotechnol. 30:2400–5
     [Crossref] [Google Scholar]
  187. 187.
    Melita O, Kaldis A, Berbati M, Reppa C, Holeva M et al. 2021. Topical application of double-stranded RNA molecules deriving from Tomato yellow leaf curl virus reduces cognate virus infection in tomato. Biol. Plant 65:100–10
     [Crossref] [Google Scholar]
  188. 188.
    Carbonell A, Martínez de Alba ÁE, Flores R, Gago S. 2008. Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology 371:144–53
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-091919-073708
Loading
RNA-Based Vaccination of Plants for Control of Viruses
Annual Review of Virology 9, 521 (2022); https://doi.org/10.1146/annurev-virology-091919-073708
/content/journals/10.1146/annurev-virology-091919-073708
/content/journals/10.1146/annurev-virology-091919-073708
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