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Annual Review of Virology

Volume 9, 2022

The Role of Viruses in Identifying and Analyzing RNA Silencing

Abstract

Adaptive antiviral immunity in plants is an RNA-based mechanism in which small RNAs derived from both strands of the viral RNA are guides for an Argonaute (AGO) nuclease. The primed AGO specifically targets and silences the viral RNA. In plants this system has diversified to involve mobile small interfering RNAs (siRNAs), an amplification system involving secondary siRNAs and targeting mechanisms involving DNA methylation. Most, if not all, plant viruses encode multifunctional proteins that are suppressors of RNA silencing that may also influence the innate immune system and fine-tune the virus-host interaction. Animal viruses similarly trigger RNA silencing, although it may be masked in differentiated cells by the interferon system and by the action of the virus-encoded suppressor proteins. There is huge potential for RNA silencing to combat viral disease in crops, farm animals, and people, although there are complications associated with the various strategies for siRNA delivery including transgenesis. Alternative approaches could include using breeding or small molecule treatment to enhance the inherent antiviral capacity of infected cells.

Keyword(s): adaptive immunity, DNA methylation, innate immunity, RNA mobility, RNA-dependent RNA polymerase, viral suppressors of RNA silencing
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2022-09-29
2024-05-12
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Literature Cited

  1. 1.
    Kutter C, Svoboda P. 2008. miRNA, siRNA, piRNA: knowns of the unknown. RNA Biol 5:4181–88
     [Crossref] [Google Scholar]
  2. 2.
    Borges F, Martienssen RA. 2015. The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 16:12727–41
     [Crossref] [Google Scholar]
  3. 3.
    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]
  4. 4.
    Baulcombe D. 2004. RNA silencing in plants. Nature 431:356–63
     [Crossref] [Google Scholar]
  5. 5.
    Vivier E, Malissen B. 2005. Innate and adaptive immunity: specificities and signaling hierarchies revisited. Nat. Immunol. 6:117–21
     [Crossref] [Google Scholar]
  6. 6.
    Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:7117323–29
     [Crossref] [Google Scholar]
  7. 7.
    Wingard SA. 1928. Hosts and symptoms of ring spot, a virus disease of plants. J. Agric. Res. 37:127–53
     [Google Scholar]
  8. 8.
    Ghoshal B, Sanfaçon H. 2015. Symptom recovery in virus-infected plants: revisiting the role of RNA silencing mechanisms. Virology 479–480:167–79
     [Crossref] [Google Scholar]
  9. 9.
    Sherwood JL. 1988. Mechanisms of cross protection between virus strains. Plant Resistance to Viruses D Evered, S Harnett 144–57 Chichester, UK: Wiley & Sons
     [Google Scholar]
  10. 10.
    Moore CJ, Sutherland PW, Forster RLS, Gardner RC, MacDiarmid RM. 2001. Dark green islands in plant virus infection are the result of posttranscriptional gene silencing. Mol. Plant-Microbe Interact. 14:8939–46
     [Crossref] [Google Scholar]
  11. 11.
    Sherwood JL, Fulton RW. 1982. The specific involvement of coat protein in tobacco mosaic virus cross protection. Virology 119:150–58
     [Crossref] [Google Scholar]
  12. 12.
    Sherwood JL. 1987. Demonstration of the specific involvement of coat protein in tobacco mosaic virus (TMV) cross protection using a TMV coat protein mutant. Phytopathology 118:358–62
     [Crossref] [Google Scholar]
  13. 13.
    Palukaitis P, Zaitlin M. 1984. A model to explain the “cross protection” phenomenon shown by plant viruses and viroids. Plant-Microbe Interact. 1:420–29
     [Google Scholar]
  14. 14.
    Sanford JC, Johnston SA. 1985. The concept of parasite-derived resistance: deriving resistance genes from the pathogen's own genome. J. Theor. Biol. 113:2395–405
     [Crossref] [Google Scholar]
  15. 15.
    Baulcombe DC. 1996. Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8:101833–44
     [Crossref] [Google Scholar]
  16. 16.
    Powell PA, Sanders PR, Tumer NE, Fraley RT, Beachy RN. 1990. Protection against tobacco mosaic virus infection in transgenic plants requires accumulation of coat protein rather than coat protein RNA sequences. Virology 175:531–38
     [Crossref] [Google Scholar]
  17. 17.
    Powell PA, Nelson RS, De B, Hoffmann N, Rogers SG et al. 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738–43
     [Crossref] [Google Scholar]
  18. 18.
    English JJ, Mueller E, Baulcombe DC. 1996. Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8:179–88
     [Crossref] [Google Scholar]
  19. 19.
    Napoli C, Lemieux C, Jorgensen RA. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–89
     [Crossref] [Google Scholar]
  20. 20.
    van der Krol AR, Mur LA, Beld M, Mol JNM, Stuitji AR. 1990. Flavonoid genes in petunia: Addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–99
     [Google Scholar]
  21. 21.
    Smith CJS, Watson CF, Ray J, Bird CR, Morris PC et al. 1988. Antisense RNA inhibition of polygalaturonase gene expression in transgenic tomatoes. Nature 334:724–26
     [Crossref] [Google Scholar]
  22. 22.
    Elkind Y, Edwards R, Mavandad M, Hedrick SA, Ribak O et al. 1990. Abnormal-plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. PNAS 87:9057–61
     [Crossref] [Google Scholar]
  23. 23.
    Timmons L, Fire A. 1998. Specific interference by ingested dsRNA. Nature 395:6705854
     [Crossref] [Google Scholar]
  24. 24.
    Hamilton AJ, Baulcombe DC. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:5441950–52
     [Crossref] [Google Scholar]
  25. 25.
    Ratcliff F, Harrison BD, Baulcombe DC. 1997. A similarity between viral defense and gene silencing in plants. Science 276:1558–60
     [Crossref] [Google Scholar]
  26. 26.
    Covey SN, Al-Kaff NS, Langara A, Turner DS. 1997. Plants combat infection by gene silencing. Nature 385:781–82
     [Crossref] [Google Scholar]
  27. 27.
    Chen X. 2009. Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25:21–44
     [Crossref] [Google Scholar]
  28. 28.
    Myles KM, Wiley MR, Morazzani EM, Adelman ZN. 2008. Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. PNAS 105:5019938–43
     [Crossref] [Google Scholar]
  29. 29.
    Molnár A, Csorba T, Lakatos L, Várallyay É, Lacomme C, Burgyán J. 2005. Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J. Virol. 79:127812–18
     [Crossref] [Google Scholar]
  30. 30.
    Harris CJ, Molnar A, Müller SY, Baulcombe DC. 2015. FDF-PAGE: a powerful technique revealing previously undetected small RNAs sequestered by complementary transcripts. Nucleic Acids Res 43:157590–99
     [Crossref] [Google Scholar]
  31. 31.
    Song X, Li Y, Cao X, Qi Y. 2019. MicroRNAs and their regulatory roles in plant-environment interactions. Annu. Rev. Plant Biol. 70:489–525
     [Crossref] [Google Scholar]
  32. 32.
    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]
  33. 33.
    Wang XB, Wu Q, Ito T, Cillo F, Li WX et al. 2010. RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. PNAS 107:1484–89
     [Crossref] [Google Scholar]
  34. 34.
    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]
  35. 35.
    Harvey JJW, Lewsey MG, Patel K, Westwood J, Heimstädt S et al. 2011. An antiviral defense role of AGO2 in plants. PLOS ONE 6:1e14639
     [Crossref] [Google Scholar]
  36. 36.
    Brosseau C, El Oirdi M, Adurogbangba A, Ma X, Moffett P. 2016. Antiviral defense involves AGO4 in an Arabidopsis–potexvirus interaction. Mol. Plant-Microbe Interact. 29:11878–88
     [Crossref] [Google Scholar]
  37. 37.
    Qu F, Ye X, Morris TJ. 2008. Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. PNAS 105:387–12
     [Crossref] [Google Scholar]
  38. 38.
    Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA et al. 2012. Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24:93613–29
     [Crossref] [Google Scholar]
  39. 39.
    Wang XB, 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]
  40. 40.
    Kreuze JF, Perez A, Untiveros M, Quispe D, Fuentes S et al. 2009. Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology 388:11–7
     [Crossref] [Google Scholar]
  41. 41.
    Wu Q, Luo Y, Lu R, Lau N, Lai EC et al. 2010. Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. PNAS 107:41606–11
     [Crossref] [Google Scholar]
  42. 42.
    Zheng Y, Gao S, Padmanabhan C, Li R, Galvez M et al. 2017. VirusDetect: an automated pipeline for efficient virus discovery using deep sequencing of small RNAs. Virology 500:130–38
     [Crossref] [Google Scholar]
  43. 43.
    Csorba T, Kontra L, Burgyán J. 2015. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103
     [Crossref] [Google Scholar]
  44. 44.
    Voinnet O, Baulcombe DC. 1997. Systemic signalling in gene silencing. Nature 389:553
     [Crossref] [Google Scholar]
  45. 45.
    Palauqui J-C, Elmayan T, Pollien J-M, Vaucheret H. 1997. Systemic acquired silencing: Transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–45
     [Crossref] [Google Scholar]
  46. 46.
    Jose AM, Hunter CP. 2007. Transport of sequence-specific RNA interference information between cells. Annu. Rev. Genet. 41:305–30
     [Crossref] [Google Scholar]
  47. 47.
    Melnyk CW, Molnar A, Baulcombe DC. 2011. Intercellular and systemic movement of RNA silencing signals. EMBO J 30:173553–63
     [Crossref] [Google Scholar]
  48. 48.
    Schwach F, Vaistij FE, Jones L, Baulcombe DC. 2005. An RNA-dependent RNA-polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–52
     [Crossref] [Google Scholar]
  49. 49.
    Havelda Z, Hornyik C, Crescenzi A, Burgyan J. 2003. In situ characterization of Cymbidium Ringspot Tombusvirus infection-induced posttranscriptional gene silencing in Nicotiana benthamiana. J. Virol. 77:106082–86
     [Crossref] [Google Scholar]
  50. 50.
    Kørner CJ, Pitzalis N, Peña EJ, Erhardt M, Vazquez F, Heinlein M. 2018. Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery. Nat. Plants 4:3157–64
     [Crossref] [Google Scholar]
  51. 51.
    Devers EA, Brosnan CA, Sarazin A, Albertini D, Amsler AC et al. 2020. Movement and differential consumption of short interfering RNA duplexes underlie mobile RNA interference. Nat. Plants 6:7789–99
     [Crossref] [Google Scholar]
  52. 52.
    D'Ario M, Griffiths-Jones S, Kim M. 2017. Small RNAs: big impact on plant development. Trends Plant Sci 22:121056–68
     [Crossref] [Google Scholar]
  53. 53.
    Chitwood DM, Guo M, Nogueira FTS, Timmermans MCP. 2007. Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex. Development 134:813–23
     [Crossref] [Google Scholar]
  54. 54.
    Pant BD, Buhtz A, Kehr J, Scheible WR. 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:5731–38
     [Crossref] [Google Scholar]
  55. 55.
    Voinnet O, Vain P, Angell S, Baulcombe DC. 1998. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95:2177–87
     [Crossref] [Google Scholar]
  56. 56.
    Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S et al. 2001. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107:4465–76
     [Crossref] [Google Scholar]
  57. 57.
    Liu Y, Teng C, Xia R, Meyers BC. 2020. PhasiRNAs in plants: their biogenesis, genic sources, and roles in stress responses, development, and reproduction. Plant Cell 32:103059–80
     [Crossref] [Google Scholar]
  58. 58.
    Chen H-M, Chen L-T, Patel K, Li Y-H, Baulcombe DC, Wu S-H. 2010. 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. PNAS 107:3415269–74
     [Crossref] [Google Scholar]
  59. 59.
    Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT et al. 2010. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17:8997–1003
     [Crossref] [Google Scholar]
  60. 60.
    Wang Z, Hardcastle TJ, Pastor AC, Yip WH, Tang S, Baulcombe DC. 2018. A novel DCL2-dependent miRNA pathway in tomato affects susceptibility to RNA viruses. Genes Dev 32:17–181155–60
     [Crossref] [Google Scholar]
  61. 61.
    Wang T, Deng Z, Zhang X, Wang H, Wang Y et al. 2018. Tomato DCL2b is required for the biosynthesis of 22-nt small RNAs, the resulting secondary siRNAs, and the host defense against ToMV. Hortic. Res. 5:62
     [Crossref] [Google Scholar]
  62. 62.
    Mlotshwa S, Pruss GJ, Peragine A, Endres MW, Li J et al. 2008. DICER-LIKE2 plays a primary role in transitive silencing of transgenes in Arabidopsis. PLOS ONE 3:3e1755
     [Crossref] [Google Scholar]
  63. 63.
    Iwakawa H, Lam AYW, Mine A, Fujita T, Kiyokawa K et al. 2021. Ribosome stalling caused by the Argonaute-microRNA-SGS3 complex regulates the production of secondary siRNAs in plants. Cell Rep 35:13109300
     [Crossref] [Google Scholar]
  64. 64.
    Parent JS, Bouteiller N, Elmayan T, Vaucheret H. 2015. Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing. Plant J 81:2223–32
     [Crossref] [Google Scholar]
  65. 65.
    Bouché N, Lauressergues D, Gasciolli V, Vaucheret H, Bouche N. 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]
  66. 66.
    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. 15:161494–1500
     [Crossref] [Google Scholar]
  67. 67.
    Wafula E, DePamphilis CW, Johnson NR, Shahid S, Phifer T et al. 2018. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553:768682–85
     [Crossref] [Google Scholar]
  68. 68.
    VanHoudt H, Ingelbrecht I, VanMontagu M, Depicker A. 1997. Post-transcriptional silencing of a neomycin phosphotransferase II transgene correlates with the accumulation of unproductive RNAs and with increased cytosine methylation of 3′ flanking regions. Plant J 12:2379–92
     [Crossref] [Google Scholar]
  69. 69.
    Jorgensen RA. 1994. Developmental significance of epigenetic impositions on the plant genome—a paragenetic function for chromosomes. Dev. Genet. 15:523–32
     [Crossref] [Google Scholar]
  70. 70.
    Wassenegger M, Heimes S, Riedel L, Sanger HL. 1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76:3567–76
     [Crossref] [Google Scholar]
  71. 71.
    Marí-Ordóñez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. 2013. Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 45:91029–39
     [Crossref] [Google Scholar]
  72. 72.
    Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:6394–408
     [Crossref] [Google Scholar]
  73. 73.
    McCue AD, Nuthikattu S, Reeder SH, Slotkin RK. 2012. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLOS Genet 8:2e1002474
     [Crossref] [Google Scholar]
  74. 74.
    Pontier D, Picart C, Roudier F, Garcia D, Lahmy S et al. 2012. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48:1121–32
     [Crossref] [Google Scholar]
  75. 75.
    McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK. 2014. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J 34:20–35
     [Crossref] [Google Scholar]
  76. 76.
    Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. 2009. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 41:5630–34
     [Crossref] [Google Scholar]
  77. 77.
    Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. 2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308:5718118–20
     [Crossref] [Google Scholar]
  78. 78.
    Onodera Y, Haag JR, Ream T, Nunes PC, Pontes O, Pikaard CS. 2005. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120:5613–22
     [Crossref] [Google Scholar]
  79. 79.
    Wierzbicki AT, Haag JR, Pikaard CS. 2008. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:4635–48
     [Crossref] [Google Scholar]
  80. 80.
    Johnson LM, Du J, Hale CJ, Bischof S, Feng S et al. 2014. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507:7490124–28
     [Crossref] [Google Scholar]
  81. 81.
    Liu ZW, Shao CR, Zhang CJ, Zhou JX, Zhang SW et al. 2014. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLOS Genet 10:1e1003948
     [Crossref] [Google Scholar]
  82. 82.
    Law JA, Du J, Hale CJ, Feng S, Krajewski K et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:7454385–89
     [Crossref] [Google Scholar]
  83. 83.
    Kumagai MH, Donson J, Della-Cioppa G, Harvey D, Hanley K, Grill LK. 1995. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. PNAS 92:1679–83
     [Crossref] [Google Scholar]
  84. 84.
    Ruiz MT, Voinnet O, Baulcombe DC. 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:6937–46
     [Crossref] [Google Scholar]
  85. 85.
    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]
  86. 86.
    Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. 2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr. Biol. 15:10968–73
     [Crossref] [Google Scholar]
  87. 87.
    Abrahamian P, Hammond RW, Hammond J. 2020. Plant virus-derived vectors: applications in agricultural and medical biotechnology. Annu. Rev. Virol. 7:513–35
     [Crossref] [Google Scholar]
  88. 88.
    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
     [Crossref] [Google Scholar]
  89. 89.
    Gouil Q, Baulcombe DC. 2016. DNA methylation signatures of the plant chromomethyltransferases. PLOS Genet 12:12e1006526
     [Crossref] [Google Scholar]
  90. 90.
    Smith NA, Eamens AL, Wang MB. 2011. Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLOS Pathog 7:5e1002022
     [Crossref] [Google Scholar]
  91. 91.
    Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J et al. 2011. A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLOS Pathog 7:5e1002021
     [Crossref] [Google Scholar]
  92. 92.
    Adkar-Purushothama CR, Brosseau C, Giguère T, Sano T, Moffett P, Perreaulta JP. 2015. Small RNA derived from the virulence modulating region of the Potato spindle tuber viroid silences callose synthase genes of tomato plants. Plant Cell 27:82178–94
     [Crossref] [Google Scholar]
  93. 93.
    Pitzalis N, Amari K, Graindorge S, Pflieger D, Donaire L et al. 2020. Turnip mosaic virus in oilseed rape activates networks of sRNA-mediated interactions between viral and host genomes. Commun. Biol. 3:702
     [Crossref] [Google Scholar]
  94. 94.
    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. 14:130–43
     [Crossref] [Google Scholar]
  95. 95.
    Qi X, Bao FS, Xie Z. 2009. Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis. PLOS ONE 4:3e4971
     [Crossref] [Google Scholar]
  96. 96.
    Yang Y, Liu T, Shen D, Wang J, Ling X et al. 2019. Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms. PLOS Pathog 15:1e1007534
     [Crossref] [Google Scholar]
  97. 97.
    Döring TF, Chittka L. 2007. Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod-Plant Interact 1:13–16
     [Crossref] [Google Scholar]
  98. 98.
    Pruss G, Ge X, Shi XM, Carrington JC, Vance VB. 1997. Plant viral synergism: The potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859–68
     [Crossref] [Google Scholar]
  99. 99.
    Xia Z, Zhao Z, Chen L, Li M, Zhou T et al. 2016. Synergistic infection of two viruses MCMV and SCMV increases the accumulations of both MCMV and MCMV-derived siRNAs in maize. Sci. Rep. 6:20520
     [Crossref] [Google Scholar]
  100. 100.
    Redinbaugh MG, Stewart LR. 2018. Maize lethal necrosis: an emerging, synergistic viral disease. Annu. Rev. Virol. 5:301–22
     [Crossref] [Google Scholar]
  101. 101.
    Mascia T, Gallitelli D. 2016. Synergies and antagonisms in virus interactions. Plant Sci 252:176–92
     [Crossref] [Google Scholar]
  102. 102.
    Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC et al. 1998. A viral suppressor of gene silencing in plants. PNAS 95:2213079–84
     [Crossref] [Google Scholar]
  103. 103.
    Kasschau KD, Carrington JC. 1998. A counterdefensive strategy of plant viruses: suppression of post-transcriptional gene silencing. Cell 95:4461–70
     [Crossref] [Google Scholar]
  104. 104.
    Valli A, Gallo A, Rodamilans B, Lopez-Moya JJ, Garcia JA. 2017. The HCPro from the Potyviridae family: an enviable multitasking Helper Component that every virus would like to have. Mol. Plant Pathol. 19:3744–63
     [Crossref] [Google Scholar]
  105. 105.
    Anandalakshmi R, Marathe R, Ge X, Herr JM, Mau C et al. 2000. A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290:5489142–44
     [Crossref] [Google Scholar]
  106. 106.
    Nakahara KS, Masuta C, Yamada S, Shimura H, Kashihara Y, Wada TS. 2012. Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. PNAS 109:2510113–18
     [Crossref] [Google Scholar]
  107. 107.
    Lucy AP, Guo HS, Li WX, Ding SW. 2000. Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J 19:71672–80
     [Crossref] [Google Scholar]
  108. 108.
    González I, Rakitina D, Semashko M, Taliansky M, Praveen S et al. 2012. RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA 18:4771–82
     [Crossref] [Google Scholar]
  109. 109.
    Chen HY, Yang J, Lin C, Yuan YA. 2008. Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO Rep 9:8754–60
     [Crossref] [Google Scholar]
  110. 110.
    Duan CG, Fang YY, Zhou BJ, Zhao JH, Hou WN 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]
  111. 111.
    Hamera S, Song X, Su L, Chen X, Fang R 2012. Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities. Plant J 69:1104–15
     [Crossref] [Google Scholar]
  112. 112.
    Zhang X, Yuan Y-R, Pei Y, Lin S-S, Tuschl T et al. 2006. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20:233255–68
     [Crossref] [Google Scholar]
  113. 113.
    Hamilton AJ, Voinnet O, Chappell L, Baulcombe DC. 2002. Two classes of short interfering RNA in RNA silencing. EMBO J 21:174671–79
     [Crossref] [Google Scholar]
  114. 114.
    Garnelo Gόmez B, Rosas-Díaz T, Shi C, Fan P, Zhang D et al. 2021. The viral silencing suppressor P19 interacts with the receptor-like kinases BAM1 and BAM2 and suppresses the cell-to-cell movement of RNA silencing independently of its ability to bind sRNA. New Phytol 229:41840–43
     [Crossref] [Google Scholar]
  115. 115.
    Rosas-Diaz T, Zhang D, Fan P, Wang L, Ding X et al. 2018. A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi. PNAS 115:61388–93
     [Crossref] [Google Scholar]
  116. 116.
    Michaeli S, Clavel M, Lechner E, Viotti C, Wu J et al. 2019. The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1. PNAS 116:4522872–83
     [Crossref] [Google Scholar]
  117. 117.
    Wang L, Ding Y, He L, Zhang G, Zhu JK, Lozano-Duran R. 2020. A virus-encoded protein suppresses methylation of the viral genome through its interaction with AGO4 in the Cajal body. eLife 9:e55542
     [Crossref] [Google Scholar]
  118. 118.
    Ji LH, Ding SW. 2001. The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol. Plant-Microbe Interact. 14:6715–24
     [Crossref] [Google Scholar]
  119. 119.
    Love AJ, Geri C, Laird J, Carr C, Yun BW et al. 2012. Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLOS ONE 7:10e47535
     [Crossref] [Google Scholar]
  120. 120.
    Hunter LJR, Westwood JH, Heath G, Macaulay K, Smith AG et al. 2013. Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLOS ONE 8:6e66530
     [Crossref] [Google Scholar]
  121. 121.
    Wang Y, Gong Q, Wu Y, Huang F, Ismayil A et al. 2021. A calmodulin-binding transcription factor links calcium signaling to antiviral RNAi defense in plants. Cell Host Microbe 29:91393–406
     [Crossref] [Google Scholar]
  122. 122.
    Malcuit I, Marano MR, Kavanagh TA, De Jong W, Forsyth A, Baulcombe DC. 1999. The 25-kDa movement protein of PVX elicits Nb-mediated hypersensitive cell death in potato. Mol. Plant-Microbe Interact. 12:6536–43
     [Crossref] [Google Scholar]
  123. 123.
    Voinnet O, Pinto YM, Baulcombe DC. 1999. Suppression of gene silencing: a general strategy used by diverse DNA and RNA of plants. PNAS 96:2414147–52
     [Crossref] [Google Scholar]
  124. 124.
    de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R. 2014. Analysis of Tomato spotted wilt virus NSs protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol. Plant Pathol. 15:2185–95
     [Crossref] [Google Scholar]
  125. 125.
    Ren T, Qu F, Morris TJ. 2000. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:101917–25
     [Crossref] [Google Scholar]
  126. 126.
    Shivaprasad PV, Chen H-M, Patel K, Bond DM, Santos BACM, Baulcombe DC. 2012. A microRNA superfamily regulates nucleotide binding site–leucine-rich repeats and other mRNAs. Plant Cell 24:3859–74
     [Crossref] [Google Scholar]
  127. 127.
    De Vries S, De Vries J, Rose LE. 2019. The elaboration of miRNA regulation and gene regulatory networks in plant–microbe interactions. Genes 10:4310
     [Crossref] [Google Scholar]
  128. 128.
    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. 33102692–705
  129. 129.
    Deng Y, Wang J, Tung J, Liu D, Zhou Y et al. 2018. A role for small RNA in regulating innate immunity during plant growth. PLOS Pathog. 14:1e1006756
     [Crossref] [Google Scholar]
  130. 130.
    Canto-Pastor A, Santos BAMC, Valli AA, Summers W, Schornack S, Baulcombe DC. 2019. Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato. PNAS 116:72755–60
     [Crossref] [Google Scholar]
  131. 131.
    Alizon S, Hurford A, Mideo N, Van Baalen M. 2009. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22:2245–59
     [Crossref] [Google Scholar]
  132. 132.
    Doumayrou J, Avellan A, Froissart R, Michalakis Y. 2013. An experimental test of the transmission-virulence trade-off hypothesis in a plant virus. Evolution 67:2477–86
     [Crossref] [Google Scholar]
  133. 133.
    González VM, Müller S, Baulcombe DC, Puigdomènech P. 2015. Evolution of NBS-LRR gene copies among dicot plants and its regulation by members of the miR482/2118 superfamily of miRNAs. Mol. Plant 8:2329–31
     [Crossref] [Google Scholar]
  134. 134.
    Félix MA, Ashe A, Piffaretti J, Wu G, Nuez I et al. 2011. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLOS Biol 9:1e1000586
     [Crossref] [Google Scholar]
  135. 135.
    Félix MA, Wang D. 2019. Natural viruses of Caenorhabditis nematodes. Annu. Rev. Genet. 53:313–26
     [Crossref] [Google Scholar]
  136. 136.
    Ashe A, Bélicard T, Le Pen J, Sarkies P, Frézal L et al. 2013. A deletion polymorphism in the Caenorhabditis elegans RIG-I homolog disables viral RNA dicing and antiviral immunity. eLife 2:e00994
     [Crossref] [Google Scholar]
  137. 137.
    Sijen T, Steiner FA, Thijssen KL, Plasterk RHA. 2007. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315:5809244–47
     [Crossref] [Google Scholar]
  138. 138.
    Ashe A, Sarkies P, Le Pen J, Tanguy M, Miska EA 2015. Antiviral RNA interference against Orsay virus is neither systemic nor transgenerational in Caenorhabditis elegans. J. Virol. 89:2312035–46
     [Crossref] [Google Scholar]
  139. 139.
    Bronkhorst AW, Van Rij RP. 2014. The long and short of antiviral defense: small RNA-based immunity in insects. Curr. Opin. Virol. 7:119–28
     [Crossref] [Google Scholar]
  140. 140.
    Ding SW, Han Q, Wang J, Li WX 2018. Antiviral RNA interference in mammals. Curr. Opin. Immunol. 54:109–14
     [Crossref] [Google Scholar]
  141. 141.
    Maillard PV, van der Veen AG, Poirier EZ, Reis e Sousa C. 2019. Slicing and dicing viruses: antiviral RNA interference in mammals. EMBO J 38:8e100941
     [Crossref] [Google Scholar]
  142. 142.
    Poirier EZ, Buck MD, Chakravarty P, Carvalho J, Frederico B et al. 2021. An isoform of Dicer protects mammalian stem cells against multiple RNA viruses. Science 373:6551231–36
     [Crossref] [Google Scholar]
  143. 143.
    Maillard PV, van der Veen AG, Deddouche-Grass S, Rogers NC, Merits A, Reis e Sousa C. 2016. Inactivation of the type I interferon pathway reveals long double-stranded RNA-mediated RNA interference in mammalian cells. EMBO J 35:232505–18
     [Crossref] [Google Scholar]
  144. 144.
    Han Q, Chen G, Wang J, Jee D, Li WX et al. 2020. Mechanism and function of antiviral RNA interference in mice. mBio 11:4e03278–19
     [Crossref] [Google Scholar]
  145. 145.
    Li Y, Basavappa M, Lu J, Dong S, Cronkite DA et al. 2016. Induction and suppression of antiviral RNA interference by influenza A virus in mammalian cells. Nat. Microbiol. 2:16250
     [Crossref] [Google Scholar]
  146. 146.
    Qiu Y, Xu YP, Wang M, Miao M, Zhou H et al. 2020. Flavivirus induces and antagonizes antiviral RNA interference in both mammals and mosquitoes. Sci. Adv. 6:6eaax7989
     [Crossref] [Google Scholar]
  147. 147.
    Zhang Y, Xu Y, Dai Y, Li Z, Wang J et al. 2021. Efficient Dicer processing of virus-derived double-stranded RNAs and its modulation by RIG-I-like receptor LGP2. PLOS Pathog 17:8e1009790
     [Crossref] [Google Scholar]
  148. 148.
    Kreuze JF, Valkonen JP. 2017. Utilization of engineered resistance to viruses in crops of the developing world, with emphasis on sub-Saharan Africa. Curr. Opin. Virol. 26:90–97
     [Crossref] [Google Scholar]
  149. 149.
    Hu W, Zheng H, Li Q, Wang Y, Liu X et al. 2021. shRNA transgenic swine display resistance to infection with the foot-and-mouth disease virus. Sci. Rep. 11:16377
     [Crossref] [Google Scholar]
  150. 150.
    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]
  151. 151.
    Palliser D, Chowdhury D, Wang Q-Y, Lee SJ, Bronson RT et al. 2006. An siRNA-based microbicide protects mice from lethal herpes simplex virus 2 infection. Nature 439:89–94
     [Crossref] [Google Scholar]
  152. 152.
    Zhang C, Wohlhueter R, Zhang H. 2016. Genetically modified foods: a critical review of their promise and problems. Food Sci. Hum. Wellness 5:3116–23
     [Crossref] [Google Scholar]
  153. 153.
    Murray JD, Maga EA. 2016. A new paradigm for regulating genetically engineered animals that are used as food. PNAS 113:133410–13
     [Crossref] [Google Scholar]
  154. 154.
    Chakraborty C, Sharma AR, Sharma G, Doss CGP, Lee SS. 2017. Therapeutic miRNA and siRNA: moving from bench to clinic as next generation medicine. Mol. Ther.-Nucleic Acids 8:132–43
     [Crossref] [Google Scholar]
  155. 155.
    Lafforgue G, Martinez F, Sardanyes J, de la Iglesia F, Niu Q-W et al. 2011. Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance. J. Virol. 85:199686–95
     [Crossref] [Google Scholar]
  156. 156.
    Brown JKM. 2015. Durable resistance of crops to disease: a Darwinian perspective. Annu. Rev. Phytopathol. 53:513–39
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-091919-064218
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The Role of Viruses in Identifying and Analyzing RNA Silencing
Annual Review of Virology 9, 353 (2022); https://doi.org/10.1146/annurev-virology-091919-064218
/content/journals/10.1146/annurev-virology-091919-064218
/content/journals/10.1146/annurev-virology-091919-064218
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