1932

Abstract

Plant viruses were first implemented as heterologous gene expression vectors more than three decades ago. Since then, the methodology for their use has varied, but we propose it was the merging of technologies with virology tools, which occurred in three defined steps discussed here, that has driven viral vector applications to date. The first was the advent of molecular biology and reverse genetics, which enabled the cloning and manipulation of viral genomes to express genes of interest (vectors 1.0). The second stems from the discovery of RNA silencing and the development of high-throughput sequencing technologies that allowed the convenient and widespread use of virus-induced gene silencing (vectors 2.0). Here, we briefly review the events that led to these applications, but this treatise mainly concentrates on the emerging versatility of gene-editing tools, which has enabled the emergence of virus-delivered genetic queries for functional genomics and virology (vectors 3.0).

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2019-08-25
2024-06-17
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Literature Cited

  1. 1. 
    Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573
    [Google Scholar]
  2. 2. 
    Aguero J, Ruiz-Ruiz S, Del Carmen Vives M, Velazquez K, Navarro L et al. 2012. Development of viral vectors based on Citrus leaf blotch virus to express foreign proteins or analyze gene function in citrus plants. Mol. Plant Microbe 25:1326–37
    [Google Scholar]
  3. 3. 
    Ahlquist P, French R, Janda M, Loesch-Fries LS 1984. Multicomponent RNA plant virus infection derived from cloned viral cDNA. PNAS 81:7066–70
    [Google Scholar]
  4. 4. 
    Ali Z, Abul-Faraj A, Li L, Ghosh N, Piatek M et al. 2015. Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol. Plant 8:1288–91
    [Google Scholar]
  5. 5. 
    Ali Z, Abul-Faraj A, Piatek M, Mahfouz MM 2015. Activity and specificity of TRV-mediated gene editing in plants. Plant Signal Behav 10:e1044191
    [Google Scholar]
  6. 6. 
    Ali Z, Eid A, Ali S, Mahfouz MM 2018. Pea early-browning virus-mediated genome editing via the CRISPR/Cas9 system in Nicotiana benthamiana and Arabidopsis. Virus Res 244:333–7
    [Google Scholar]
  7. 7. 
    Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC et al. 1998. A viral suppressor of gene silencing in plants. PNAS 95:13079–84
    [Google Scholar]
  8. 8. 
    Balaji B, Cawly J, Angel C, Zhang Z, Palanichelvam K et al. 2007. Silencing of the N family of resistance genes in Nicotiana edwardsonii compromises the hypersensitive response to tombusviruses. Mol. Plant Microbe 20:1262–70
    [Google Scholar]
  9. 9. 
    Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF 2014. DNA replicons for plant genome engineering. Plant Cell 26:151–63
    [Google Scholar]
  10. 10. 
    Baulcombe DC. 1999. Fast forward genetics based on virus-induced gene silencing. Curr. Opin. Plant Biol. 2:109–13
    [Google Scholar]
  11. 11. 
    Bawden FC, Kassanis B. 1941. Some properties of tobacco etch viruses. Ann. Appl. Biol. 28:107–18
    [Google Scholar]
  12. 12. 
    Bedoya LC, Martínez F, Orzáez D, Daròs J-A 2012. Visual tracking of plant virus infection and movement using a reporter MYB transcription factor that activates anthocyanin biosynthesis. Plant Physiol 158:1130–38
    [Google Scholar]
  13. 13. 
    Berardi A, Evans DJ, Baldelli Bombelli F, Lomonossoff GP 2018. Stability of plant virus-based nanocarriers in gastrointestinal fluids. Nanoscale 10:1667–79
    [Google Scholar]
  14. 14. 
    Bevan M. 1984. Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12:8711–21
    [Google Scholar]
  15. 15. 
    Blanc S, Ammar ED, Garcia-Lampasona S, Dolja VV, Llave C et al. 1998. Mutations in the potyvirus helper component protein: effects on interactions with virions and aphid stylets. J. Gen. Virol. 79:3119–22
    [Google Scholar]
  16. 16. 
    Boettcher M, Tian R, Blau JA, Markegard E, Wagner RT et al. 2018. Dual gene activation and knockout screen reveals directional dependencies in genetic networks. Nat. Biotechnol. 36:170–78
    [Google Scholar]
  17. 17. 
    Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP 2004. Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–46
    [Google Scholar]
  18. 18. 
    Burstein D, Harrington LB, Strutt SC, Probst AJ, Anantharaman K et al. 2017. New CRISPR-Cas systems from uncultivated microbes. Nature 542:237–41
    [Google Scholar]
  19. 19. 
    Butler NM, Atkins PA, Voytas DF, Douches DS 2015. Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas system. PLOS ONE 10:e0144591
    [Google Scholar]
  20. 20. 
    Čermák T, Baltes NJ, Čegan R, Zhang Y, Voytas DF 2015. High-frequency, precise modification of the tomato genome. Genome Biol 16:232
    [Google Scholar]
  21. 21. 
    Chang HHY, Pannunzio NR, Adachi N, Lieber MR 2017. Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat. Rev. Mol. Cell Biol. 18:495–506
    [Google Scholar]
  22. 22. 
    Chapman S, Kavanagh T, Baulcombe D 1992. Potato virus X as a vector for gene expression in plants. Plant J 2:549–57
    [Google Scholar]
  23. 23. 
    Chiong K. 2018. Tobacco mosaic virus as a gene editing platform MS Thesis, Texas A&M Univ., College Station
    [Google Scholar]
  24. 24. 
    Cody WB. 2018. A viral-based toolbox for efficient gene editing in Nicotiana species PhD Diss., Texas A&M Univ., College Station
    [Google Scholar]
  25. 25. 
    Cody WB, Scholthof HB, Mirkov TE 2017. Multiplexed gene editing and protein overexpression using a Tobacco mosaic virus viral vector. Plant Physiol 175:23–35
    [Google Scholar]
  26. 26. 
    Cong L, Ran FA, Cox D, Lin S, Barretto R et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–23
    [Google Scholar]
  27. 27. 
    Dahan-Meir T, Filler-Hayut S, Melamed-Bessudo C, Bocobza S, Czosnek H et al. 2018. Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system. Plant J 95:5–16
    [Google Scholar]
  28. 28. 
    Dahlman JE, Abudayyeh OO, Joung J, Gootenberg JS, Zhang F, Konermann S 2015. Orthogonal gene knockout and activation with a catalytically active Cas9 nuclease. Nat. Biotechnol. 33:1159–61
    [Google Scholar]
  29. 29. 
    Dawson WO, Bar-Joseph M, Garnsey SM, Moreno P 2015. Citrus tristeza virus: making an ally from an enemy. Annu. Rev. Phytopathol. 53:137–55
    [Google Scholar]
  30. 30. 
    Dawson WO, Beck DL, Knorr DA, Grantham GL 1986. cDNA cloning of the complete genome of Tobacco mosaic virus and production of infectious transcripts. PNAS 83:1832–36
    [Google Scholar]
  31. 31. 
    Dolja VV, Koonin EV. 2013. The closterovirus-derived gene expression and RNA interference vectors as tools for research and plant biotechnology. Front. Microbiol. 4:83
    [Google Scholar]
  32. 32. 
    Dong C, Beetham P, Vincent K, Sharp P 2006. Oligonucleotide-directed gene repair in wheat using a transient plasmid gene repair assay system. Plant Cell Rep 25:457–65
    [Google Scholar]
  33. 33. 
    Esvelt K. 2016. Gene editing can drive science to openness. Nature 534:153
    [Google Scholar]
  34. 34. 
    Esvelt KM, Carlson JC, Liu DR 2011. A system for the continuous directed evolution of biomolecules. Nature 472:499–503
    [Google Scholar]
  35. 35. 
    Fiers W, Contreras R, Duerinck F, Haegeman G, Iserentant D et al. 1976. Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature 260:500
    [Google Scholar]
  36. 36. 
    Forment J, Gadea J, Huerta L, Abizanda L, Agusti J et al. 2005. Development of a citrus genome-wide EST collection and cDNA microarray as resources for genomic studies. Plant Mol. Biol. 57:375–91
    [Google Scholar]
  37. 37. 
    Franck A, Guilley H, Jonard G, Richards K, Hirth L 1980. Nucleotide sequence of Cauliflower mosaic virus DNA. Cell 21:285–94
    [Google Scholar]
  38. 38. 
    Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32:279–84
    [Google Scholar]
  39. 39. 
    Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TMA 1987. The 5'-leader sequence of Tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acid Res 15:3257–73
    [Google Scholar]
  40. 40. 
    Gao J, Wang G, Ma S, Xie X, Wu X et al. 2015. CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol. Biol 87:99–110
    [Google Scholar]
  41. 41. 
    Gao Y, Zhao Y. 2014. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol. 56:343–49
    [Google Scholar]
  42. 42. 
    Gaquerel E, Gulati J, Baldwin IT 2014. Revealing insect herbivory-induced phenolamide metabolism: from single genes to metabolic network plasticity analysis. Plant J 79:679–92
    [Google Scholar]
  43. 43. 
    Gardner RC, Howarth AJ, Hahn P, Brown-Luedi M, Shepherd RJ, Messing J 1981. The complete nucleotide sequence of an infectious clone of Cauliflower mosaic virus by M13mp7 shotgun sequencing. Nucleic Acid Res 9:2871–88
    [Google Scholar]
  44. 44. 
    Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV et al. 2017. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J 89:1251–62
    [Google Scholar]
  45. 45. 
    Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA et al. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–51
    [Google Scholar]
  46. 46. 
    Giritch A, Marillonnet S, Engler C, van Eldik G, Botterman J et al. 2006. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. PNAS 103:14701–6
    [Google Scholar]
  47. 47. 
    Gleba Y, Klimyuk V, Marillonnet S 2005. Magnifection: a new platform for expressing recombinant vaccines in plants. Vaccine 23:2042–48
    [Google Scholar]
  48. 48. 
    Gleba Y, Klimyuk V, Marillonnet S 2007. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol. 18:134–41
    [Google Scholar]
  49. 49. 
    Goelet P, Lomonossoff GP, Butler PJ, Akam ME, Gait MJ, Karn J 1982. Nucleotide sequence of Tobacco mosaic virus RNA. PNAS 79:5818–22
    [Google Scholar]
  50. 50. 
    Goodin MM, Zaitlin D, Naidu RA, Lommel SA 2008. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol. Plant-Microbe Interact. 21:1015–26
    [Google Scholar]
  51. 51. 
    Grimsley N, Hohn B, Hohn T, Walden R 1986. “Agroinfection,” an alternative route for viral infection of plants by using the Ti plasmid. PNAS 83:3282–86
    [Google Scholar]
  52. 52. 
    Hajeri S, Killiny N, El-Mohtar C, Dawson WO, Gowda S 2014. Citrus tristeza virus–based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). J. Biotechnol. 176:42–49
    [Google Scholar]
  53. 53. 
    Holmes FO. 1946. A comparison of the experimental host ranges of tobacco-etch and tobacco-mosaic viruses. Phytopathology 36:643–59
    [Google Scholar]
  54. 54. 
    Hsu PD, Lander ES, Zhang F 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–78
    [Google Scholar]
  55. 55. 
    Hull R. 2002. Matthews' Plant Virology London: Academic
    [Google Scholar]
  56. 56. 
    Hummel AW, Chauhan RD, Cermak T, Mutka AM, Vijayaraghavan A et al. 2018. Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnol. J. 16:1275–82
    [Google Scholar]
  57. 57. 
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–21
    [Google Scholar]
  58. 58. 
    Karvelis T, Gasiunas G, Miksys A, Barrangou R, Horvath P, Siksnys V 2013. crRNA and tracrRNA guide Cas9-mediated DNA interference in Streptococcus thermophilus. RNA Biol 10:841–51
    [Google Scholar]
  59. 59. 
    Kay R, Chan A, Daly M, McPherson J 1987. Duplication of CaMV 35S promoter sequences creates a strong enhancer for plant genes. Science 236:1299–302
    [Google Scholar]
  60. 60. 
    Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT et al. 2016. High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490
    [Google Scholar]
  61. 61. 
    Kleinstiver BP, Prew MS, Tsai SQ, Nguyen NT, Topkar VV et al. 2015. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat. Biotechnol. 33:1293–98
    [Google Scholar]
  62. 62. 
    Koonin EV, Makarova KS. 2018. Anti-CRISPRs on the march. Science 362:156–57
    [Google Scholar]
  63. 63. 
    Koonin EV, Makarova KS, Zhang F 2017. Diversity, classification and evolution of CRISPR/Cas systems. Curr. Opin. Microbiol. 37:67–78
    [Google Scholar]
  64. 64. 
    Kosicki M, Tomberg K, Bradle A 2018. Repair of double-strand breaks induced by CRISPR–Cas9 leads to large deletions and complex rearrangements. Nat. Biotechnol. 36:765–71
    [Google Scholar]
  65. 65. 
    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
    [Google Scholar]
  66. 66. 
    Lacomme C. 2015. Strategies for altering plant traits using virus-induced gene silencing technologies. Methods Mol. Biol. 1287:25–41
    [Google Scholar]
  67. 67. 
    Landsberger M, Gandon S, Meaden S, Rollie C, Chevallereau A et al. 2018. Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity. Cell 174:908–16.e12
    [Google Scholar]
  68. 68. 
    Lange M, Yellina AL, Orashakova S, Becker A 2013. Virus-induced gene silencing (VIGS) in plants: an overview of target species and the virus-derived vector systems. Methods Mol. Biol. 975:1–14
    [Google Scholar]
  69. 69. 
    Langner T, Kamoun S, Belhaj K 2018. CRISPR crops: plant genome editing toward disease resistance. Annu. Rev. Phytopathol. 56:479–512
    [Google Scholar]
  70. 70. 
    Li JF, Norville JE, Aach J, McCormack M, Zhang D et al. 2013. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31:688–91
    [Google Scholar]
  71. 71. 
    Lindbo JA. 2007. TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol 145:1232–40
    [Google Scholar]
  72. 72. 
    Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG 1993. Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5:1749–59
    [Google Scholar]
  73. 73. 
    Liu Y, Schiff M, Dinesh-Kumar SP 2002. Virus-induced gene silencing in tomato. Plant J 31:777–86
    [Google Scholar]
  74. 74. 
    Lloyd A, Plaisier CL, Carroll D, Drews GN 2005. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. PNAS 102:2232–37
    [Google Scholar]
  75. 75. 
    Majer E, Llorente B, Rodriguez-Concepcion M, Daros JA 2017. Rewiring carotenoid biosynthesis in plants using a viral vector. Sci. Rep. 7:41645
    [Google Scholar]
  76. 76. 
    Mali P, Yang L, Esvelt KM, Aach J, Guell M et al. 2013. RNA-guided human genome engineering via Cas9. Science 339:823–26
    [Google Scholar]
  77. 77. 
    Marnef A, Legube G. 2017. Organizing DNA repair in the nucleus: DSBs hit the road. Curr. Opin. Cell Biol. 46:1–8
    [Google Scholar]
  78. 78. 
    Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31:691–93
    [Google Scholar]
  79. 79. 
    Odokonyero D, Mendoza MR, Alvarado VY, Zhang J, Wang X, Scholthof HB 2015. Transgenic down-regulation of ARGONAUTE2 expression in Nicotiana benthamiana interferes with several layers of antiviral defenses. Virology 486:209–18
    [Google Scholar]
  80. 80. 
    Odokonyero D, Mendoza MR, Moffett P, Scholthof HB 2017. Tobacco rattle virus (TRV)-mediated silencing of Nicotiana benthamiana ARGONAUTES (NbAGOs) reveals new antiviral candidates and dominant effects of TRV-NbAGO1. Phytopathology 107:977–87
    [Google Scholar]
  81. 81. 
    Omarov RT, Scholthof HB. 2012. Biological chemistry of virus-encoded suppressors of RNA silencing: an overview. Antiviral Resistance in Plants: Methods and Protocols JM Watson, M-B Wang 39–56 New York: Humana Press
    [Google Scholar]
  82. 82. 
    Philips JG, Naim F, Lorenc MT, Dudley KJ, Hellens RP, Waterhouse PM 2017. The widely used Nicotiana benthamiana 16c line has an unusual T-DNA integration pattern including a transposon sequence. PLOS ONE 12:e0171311
    [Google Scholar]
  83. 83. 
    Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–89
    [Google Scholar]
  84. 84. 
    Reeves RG, Voeneky S, Caetano-Anolles D, Beck F, Boete C 2018. Agricultural research, or a new bioweapon system?. Science 362:35–37
    [Google Scholar]
  85. 85. 
    Restrepo MA, Freed DD, Carrington JC 1990. Nuclear transport of plant potyviral proteins. Plant Cell 2:987–98
    [Google Scholar]
  86. 86. 
    Ruiz MT, Voinnet O, Baulcombe DC 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:937–46
    [Google Scholar]
  87. 87. 
    Saunders K, Lomonossoff GP. 2017. In planta synthesis of designer-length Tobacco mosaic virus–based nano-rods that can be used to fabricate nano-wires. Front. Plant Sci. 8:1335
    [Google Scholar]
  88. 88. 
    Saxena P, Hsieh YC, Alvarado VY, Sainsbury F, Saunders K et al. 2011. Improved foreign gene expression in plants using a virus-encoded suppressor of RNA silencing modified to be developmentally harmless. Plant Biotechnol. J. 9:703–12
    [Google Scholar]
  89. 89. 
    Schiml S, Fauser F, Puchta H 2014. The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80:1139–50
    [Google Scholar]
  90. 90. 
    Scholthof HB. 2000. Plant virus gene vectors. Encyclopedia of Plant Pathology O Maloy, TD Murray 783–86 New York: Wiley
    [Google Scholar]
  91. 91. 
    Scholthof HB. 2005. Plant virus transport: motions of functional equivalence. Trends Plant Sci 10:376–82
    [Google Scholar]
  92. 92. 
    Scholthof HB. 2006. The Tombusvirus-encoded P19: from irrelevance to elegance. Nat. Rev. Microbiol. 4:405–11
    [Google Scholar]
  93. 93. 
    Scholthof HB. 2007. Heterologous expression of viral RNA interference suppressors: RISC management. Plant Physiol 145:1110–17
    [Google Scholar]
  94. 94. 
    Scholthof HB, Scholthof KB, Jackson AO 1996. Plant virus gene vectors for transient expression of foreign proteins in plants. Annu. Rev. Phytopathol. 34:299–323
    [Google Scholar]
  95. 95. 
    Scholthof K-BG. 2004. Tobacco mosaic virus: a model system for plant biology. Annu. Rev. Phytopathol. 42:13–34
    [Google Scholar]
  96. 96. 
    Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA et al. 2014. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87
    [Google Scholar]
  97. 97. 
    Shmakov S, Abudayyeh OO, Makarova KS, Wolf YI, Gootenberg JS et al. 2015. Discovery and functional characterization of diverse class 2 CRISPR/Cas systems. Mol. Cell 60:385–97
    [Google Scholar]
  98. 98. 
    Siegel A. 1985. Plant-virus-based vectors for gene transfer may be of considerable use despite a presumed high error frequency during RNA synthesis. Plant Mol. Biol. 4:327
    [Google Scholar]
  99. 99. 
    Stanley J, Markham PG, Callis RJ, Pinner MS 1986. The nucleotide sequence of an infectious clone of the geminivirus Beet curly top virus. EMBO J 5:1761–67
    [Google Scholar]
  100. 100. 
    Steele JFC, Peyret H, Saunders K, Castells-Graells R, Marsian J et al. 2017. Synthetic plant virology for nanobiotechnology and nanomedicine. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 9:e1447
    [Google Scholar]
  101. 101. 
    Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67
    [Google Scholar]
  102. 102. 
    Velázquez K, Agüero J, Vives MC, Aleza P, Pina JA et al. 2016. Precocious flowering of juvenile citrus induced by a viral vector based on Citrus leaf blotch virus: a new tool for genetics and breeding. Plant Biotechnol. J. 14:1976–85
    [Google Scholar]
  103. 103. 
    Wang A. 2015. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu. Rev. Phytopathol. 53:45–66
    [Google Scholar]
  104. 104. 
    Wang F, Wang M, Liu X, Xu Y, Zhu S et al. 2017. Identification of putative genes involved in limonoids biosynthesis in citrus by comparative transcriptomic analysis. Front. Plant Sci. 8:782
    [Google Scholar]
  105. 105. 
    Wang M, Lu Y, Botella JR, Mao Y, Hua K, Zhu JK 2017. Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Mol. Plant 10:1007–10
    [Google Scholar]
  106. 106. 
    Wang T, Wei JJ, Sabatini DM, Lander ES 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343:80–84
    [Google Scholar]
  107. 107. 
    Watters KE, Fellmann C, Bai HB, Ren SM, Doudna JA 2018. Systematic discovery of natural CRISPR-Cas12a inhibitors. Science 362:236–39
    [Google Scholar]
  108. 108. 
    Wright DA, Townsend JA, Winfrey RJ Jr, Irwin PA, Rajagopal J et al. 2005. High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44:693–705
    [Google Scholar]
  109. 109. 
    Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U et al. 2014. Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat. Biotechnol. 32:656–62
    [Google Scholar]
  110. 110. 
    Wu GA, Terol J, Ibanez V, López-García A, Pérez-Román E et al. 2018. Genomics of the origin and evolution of Citrus. Nature 554:311–16
    [Google Scholar]
  111. 111. 
    Xie K, Minkenberg B, Yang Y 2015. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. PNAS 112:3570–75
    [Google Scholar]
  112. 112. 
    Xie K, Yang Y. 2013. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant 6:1975–83
    [Google Scholar]
  113. 113. 
    Xu Q, Chen L-L, Ruan X, Chen D, Zhu A et al. 2013. The draft genome of sweet orange (Citrus sinensis). Nat. Genet. 45:59–66
    [Google Scholar]
  114. 114. 
    Yin K, Han T, Liu G, Chen T, Wang Y et al. 2015. A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Sci. Rep. 5:14926
    [Google Scholar]
  115. 115. 
    Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–71
    [Google Scholar]
  116. 116. 
    Zhou Y, Zhu S, Cai C, Yuan P, Li C et al. 2014. High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 509:487–91
    [Google Scholar]
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