1932

Abstract

A decade ago, the value of as a tool for plant molecular biologists was beginning to be appreciated. Scientists were using it to study plant-microbe and protein-protein interactions, and it was the species of choice with which to activate plasmid-encoded viruses, screen for gene functions with virus-induced gene silencing (VIGS), and transiently express genes by leaf agroinfiltration. However, little information about the species’ origin, diversity, genetics, and genomics was available, and biologists were asking the question of whether is a second fiddle or virtuoso. In this review, we look at the increased knowledge about the species and its applications over the past decade. Although may still be the sidekick to , it shines ever more brightly with realized and yet-to-be-exploited potential.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080417-050141
2018-08-25
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/phyto/56/1/annurev-phyto-080417-050141.html?itemId=/content/journals/10.1146/annurev-phyto-080417-050141&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Akhtar S, Briddon RW, Mansoor S 2011. Reactions of Nicotiana species to inoculation with monopartite and bipartite begomoviruses. Virol. J. 8:475
    [Google Scholar]
  2. 2.  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 244:333–37
    [Google Scholar]
  3. 3.  Anderson G, Wang R, Bandyopadhyay A, Goodin M 2012. The nucleocapsid protein of Potato yellow dwarf virus: protein interactions and nuclear import mediated by a non-canonical nuclear localization signal. Front. Plant Sci. 3:14
    [Google Scholar]
  4. 4.  Andreou D, Saetre P, Kahler AK, Werge T, Andreassen OA et al. 2011. Dystrobrevin-binding protein 1 gene (DTNBP1) variants associated with cerebrospinal fluid homovanillic acid and 5-hydroxyindoleacetic acid concentrations in healthy volunteers. Eur. Neuropsychopharm. 21:700–4
    [Google Scholar]
  5. 5.  Arntzen C 2015. Plant-made pharmaceuticals: from ‘edible vaccines’ to Ebola therapeutics. Plant Biotechnol. J. 13:1013–16
    [Google Scholar]
  6. 6.  Aslan S, Sun C, Leonova S, Dutta P, Dörmann P et al. 2014. Wax esters of different compositions produced via engineering of leaf chloroplast metabolism in Nicotiana benthamiana. Metab. . Eng 25:103–12
    [Google Scholar]
  7. 7.  Baksa I, Nagy T, Barta E, Havelda Z, Varallyay E et al. 2015. Identification of Nicotiana benthamiana microRNAs and their targets using high throughput sequencing and degradome analysis. BMC Genom 16:1025
    [Google Scholar]
  8. 8.  Bally J, Nakasugi K, Jia F, Jung H, Ho SYW et al. 2015. The extremophile Nicotiana benthamiana has traded viral defence for early vigour. Nat. Plants 1:15165
    [Google Scholar]
  9. 9.  Bandyopadhyay A, Kopperud K, Anderson G, Martin K, Goodin M 2010. An integrated protein localization and interaction map for Potato yellow dwarf virus, type species of the genus Nucleorhabdovirus. . Virology 402:61–71
    [Google Scholar]
  10. 10.  Baulcombe D 2004. RNA silencing in plants. Nature 431:356–63
    [Google Scholar]
  11. 11.  Baulcombe DC, Chapman S, Santa Cruz S 1995. Jellyfish green fluorescent protein as a reporter for virus infections. Plant J 7:1045–53
    [Google Scholar]
  12. 12.  Boivin EB, Lepage E, Matton DP, De Crescenzo G, Jolicoeur M 2010. Transient expression of antibodies in suspension plant cell suspension cultures is enhanced when co-transformed with the tomato bushy stunt virus p19 viral suppressor of gene silencing. Biotechnol. Prog. 26:1534–43
    [Google Scholar]
  13. 13.  Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB 2012. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol. Plant-Microbe Interact. 25:1523–30
    [Google Scholar]
  14. 14.  Bruun-Rasmussen M, Madsen CT, Jessing S, Albrechtsen M 2007. Stability of Barley stripe mosaic virus–induced gene silencing in barley. Mol. Plant-Microbe Interact. 20:1323–31
    [Google Scholar]
  15. 15.  Burbidge N 1960. The Australian species of Nicotiana L. (Solanaceae). Aust. J. Bot. 8:342–80
    [Google Scholar]
  16. 16.  Burch-Smith TM, Schiff M, Liu Y, Dinesh-Kumar SP 2006. Efficient virus-induced gene silencing in Arabidopsis. Plant Physiol 142:21–27
    [Google Scholar]
  17. 17.  Burstenbinder K, Moller B, Plotner R, Stamm G, Hause G et al. 2017. The IQD family of calmodulin-binding proteins links calcium signaling to microtubules, membrane subdomains, and the nucleus. Plant Physiol 173:1692–708
    [Google Scholar]
  18. 18.  Caputi L, Franke J, Farrow SC, Chung K, Payne RME et al. 2018. Missing enzymes in the biosynthesis of the anticancer drug vinblastine in Madagascar periwinkle. Science 360:1235–39
    [Google Scholar]
  19. 19.  Casper SJ, Holt CA 1996. Expression of the green fluorescent protein–encoding gene from a tobacco mosaic virus–based vector. Gene 173:69–73
    [Google Scholar]
  20. 20.  Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V et al. 2007. pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana–virus interactions. Mol. Plant-Microbe Interact. 20:740–50
    [Google Scholar]
  21. 21.  Chan H-T, Daniell H 2015. Plant-made oral vaccines against human infectious diseases—are we there yet?. Plant Biotechnol. J. 13:1056–70
    [Google Scholar]
  22. 22.  Chen Q 2016. Glycoengineering of plants yields glycoproteins with polysialylation and other defined N-glycoforms. PNAS 113:9404–6
    [Google Scholar]
  23. 23.  Clemente T 2006. Nicotiana (Nicotiana tobaccum, Nicotiana benthamiana). Agrobacterium Protocols K Wang 143–54 Totowa, NJ: Humana Press
    [Google Scholar]
  24. 24.  Cox KM, Sterling JD, Regan JT, Gasdaska JR, Frantz KK et al. 2006. Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat. Biotechnol. 24:1591–97
    [Google Scholar]
  25. 25.  Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR 2000. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. PNAS 97:3718–23
    [Google Scholar]
  26. 26.  Daniell H, Streatfield SJ, Rybicki EP 2015. Advances in molecular farming: key technologies, scaled up production and lead targets. Plant Biotechnol. J. 13:1011–12
    [Google Scholar]
  27. 27.  Delfosse VC, Casse MF, Agrofoglio YC, Kresic IB, Hopp HE et al. 2013. Agroinoculation of a full-length cDNA clone of cotton leafroll dwarf virus (CLRDV) results in systemic infection in cotton and the model plant Nicotiana benthamiana. . Virus Res 175:64–70
    [Google Scholar]
  28. 28.  Dietzgen RG, Martin KM, Anderson G, Goodin MM 2012. In planta localization and interactions of impatiens necrotic spot tospovirus proteins. J. Gen. Virol. 93:2490–95
    [Google Scholar]
  29. 29.  Dong Y, Burch-Smith TM, Liu Y, Mamillapalli P, Dinesh-Kumar SP 2007. A ligation-independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral development. Plant Physiol 145:1161–70
    [Google Scholar]
  30. 30.  Dugdale B, Kato M, Deo P, Plan M, Harrison M et al. 2018. Production of human vitronectin in Nicotiana benthamiana using the INPACT hyperexpression platform. Plant Biotechnol. J. 16:394–403
    [Google Scholar]
  31. 31.  Eamens A, Wang MB, Smith NA, Waterhouse PM 2008. RNA silencing in plants: yesterday, today, and tomorrow. Plant Physiol 147:456–68
    [Google Scholar]
  32. 32.  El Kasmi F, Chung EH, Anderson RG, Li J, Wan L et al. 2017. Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein. PNAS 114:E7385–94
    [Google Scholar]
  33. 33.  Feng ZG, Pang SF, Guo DJ, Yang YT, Liu B et al. 2014. Recombinant keratinocyte growth factor 1 in tobacco potentially promotes wound healing in diabetic rats. BioMed Res. Int. 2014:579632
    [Google Scholar]
  34. 34.  Fitzmaurice WP 2002. Interspecific Nicotiana hybrids and their progeny US Patent 6344597B1
    [Google Scholar]
  35. 35.  Floss DM, Sack M, Arcalis E, Stadlmann J, Quendler H et al. 2009. Influence of elastin-like peptide fusions on the quantity and quality of a tobacco-derived human immunodeficiency virus–neutralizing antibody. Plant Biotechnol. J. 7:899–913
    [Google Scholar]
  36. 36.  Fu DQ, Zhu BZ, Zhu HL, Jiang WB, Luo YB 2005. Virus-induced gene silencing in tomato fruit. Plant J 43:299–308
    [Google Scholar]
  37. 37.  Gao X, Wheeler T, Li Z, Kenerley CM, He P, Shan L 2011. Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J 66:293–305
    [Google Scholar]
  38. 38.  Ghareeb H, Laukamm S, Lipka V 2016. COLORFUL-Circuit: a platform for rapid multigene assembly, delivery, and expression in plants. Front. Plant Sci. 7:246
    [Google Scholar]
  39. 39.  Gleba Y, Klimyuk V, Marillonnet S 2007. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol. 18:134–41
    [Google Scholar]
  40. 40.  Gleba YY, Tuse D, Giritch A 2014. Plant viral vectors for delivery by Agrobacterium. Curr. Top. . Microbiol 375:155–92
    [Google Scholar]
  41. 41.  Glenn WS, Runguphan W, O'Connor SE 2013. Recent progress in the metabolic engineering of alkaloids in plant systems. Curr. Opin. Biotechnol. 24:2354–65
    [Google Scholar]
  42. 42.  Goodin MM 2018. Protein localization and interaction studies in plants: toward defining complete proteomes by visualization. Adv. Virus Res. 100:117–44
    [Google Scholar]
  43. 43.  Goodin M, Chakrabarty R, Yelton S 2008. Membrane and protein dynamics in virus-infected plant cells. Methods Mol. Biol. 451:377–93
    [Google Scholar]
  44. 44.  Goodin M, Yelton S, Ghosh D, Mathews S, Lesnaw J 2005. Live-cell imaging of rhabdovirus-induced morphological changes in plant nuclear membranes. Mol. Plant-Microbe Interact. 18:703–9
    [Google Scholar]
  45. 45.  Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO 2002. pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J 31:375–83
    [Google Scholar]
  46. 46.  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]
  47. 47.  Goodspeed TH 1947. On the evolution of the genus Nicotiana. . PNAS 33:158–71
    [Google Scholar]
  48. 48.  Griffiths N, Jaipargas EA, Wozny MR, Barton KA, Mathur N et al. 2016. Photo-convertible fluorescent proteins as tools for fresh insights on subcellular interactions in plants. J. Microsc. 263:148–57
    [Google Scholar]
  49. 49.  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]
  50. 50.  Gronlund M, Constantin G, Piednoir E, Kovacev J, Johansen IE, Lund OS 2008. Virus-induced gene silencing in Medicago truncatula and Lathyrus odorata. . Virus Res 135:345–49
    [Google Scholar]
  51. 51.  Hayward A, Padmanabhan M, Dinesh-Kumar SP 2011. Virus-induced gene silencing in Nicotiana benthamiana and other plant species. Methods Mol. Biol. 678:55–63
    [Google Scholar]
  52. 52.  Jefferson RA, Kavanagh TA, Bevan MW 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–7
    [Google Scholar]
  53. 53.  Jeong RD, Chandra-Shekara AC, Barman SR, Navarre D, Klessig DF et al. 2010. Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase. PNAS 107:13538–43
    [Google Scholar]
  54. 54.  Jia H, Shen Y 2013. Virus-induced gene silencing in strawberry fruit. Methods Mol. Biol. 975:211–18
    [Google Scholar]
  55. 55.  Jiang WZ, Zhou HB, Bi HH, Fromm M, Yang B, Weeks DP 2013. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41:e188
    [Google Scholar]
  56. 56.  Jobsri J, Allen A, Rajagopal D, Shipton M, Kanyuka K et al. 2015. Plant virus particles carrying tumour antigen activate TLR7 and induce high levels of protective antibody. PLOS ONE 10:e0118096
    [Google Scholar]
  57. 57.  Juvale PS, Hewezi T, Zhang C, Kandoth PK, Mitchum MG et al. 2012. Temporal and spatial Bean pod mottle virus–induced gene silencing in soybean. Mol. Plant Pathol. 13:1140–48
    [Google Scholar]
  58. 58.  Kalantidis K, Schumacher HT, Alexiadis T, Helm JM 2008. RNA silencing movement in plants. Biol. Cell 100:13–26
    [Google Scholar]
  59. 59.  Kanneganti TD, Bai X, Tsai CW, Win J, Meulia T et al. 2007. A functional genetic assay for nuclear trafficking in plants. Plant J 50:149–58
    [Google Scholar]
  60. 60.  Kapila J, De Rycke R, Van Montagu M, Angenon G 1997. An Agrobacterium‐mediated transient gene expression system for intact leaves. Plant Sci 122:101–8
    [Google Scholar]
  61. 61.  Kelly LJ, Leitch AR, Clarkson JJ, Knapp S, Chase MW 2013. Reconstructing the complex evolutionary origin of wild allopolyploid tobaccos (Nicotiana section suaveolentes). Evolution 67:80–94
    [Google Scholar]
  62. 62.  Kostoff D 1940. Relation degrees and phylesis of certain Nicotiana species determined by cytogenetic analysis. Genetica 22:215–30
    [Google Scholar]
  63. 63.  Kulzer S, Petersen W, Baser A, Mandel K, Przyborski JM 2013. Use of self-assembling GFP to determine protein topology and compartmentalisation in the Plasmodium falciparum-infected erythrocyte. Mol. Biochem. Parasitol. 187:87–90
    [Google Scholar]
  64. 64.  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]
  65. 65.  Ladiges PY, Marks CE, Nelson G 2011. Biogeography of Nicotiana section suaveolentes (Solanaceae) reveals geographical tracks in arid Australia. J. Biogeogr. 38:2066–77
    [Google Scholar]
  66. 66.  Laliberte JF, Zheng H 2014. Viral manipulation of plant host membranes. Annu. Rev. Virol. 1:237–59
    [Google Scholar]
  67. 67.  Lamm CE, Link K, Wagner S, Milbradt J, Marschall M, Sonnewald U 2016. Human cytomegalovirus nuclear egress proteins ectopically expressed in the heterologous environment of plant cells are strictly targeted to the nuclear envelope. Viruses 8:73
    [Google Scholar]
  68. 68.  Lamm CE, Scherer M, Reuter N, Amin B, Stamminger T, Sonnewald U 2016. Human promyelocytic leukemia protein is targeted to distinct subnuclear domains in plant nuclei and colocalizes with nucleolar constituents in a SUMO-dependent manner. FEBS Open Bio 6:1141–54
    [Google Scholar]
  69. 69.  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]
  70. 70.  Larrimore KE, Barcus M, Kannan L, Gao Y, Zhan CG et al. 2013. Plants as a source of butyrylcholinesterase variants designed for enhanced cocaine hydrolase activity. Chem.-Biol. Interact. 203:217–20
    [Google Scholar]
  71. 71.  Lee SS, Park HJ, Jung WY, Lee A, Yoon DH et al. 2015. OsCYP21–4, a novel Golgi-resident cyclophilin, increases oxidative stress tolerance in rice. Front. Plant Sci. 6:797
    [Google Scholar]
  72. 72.  Leiser RM, Zieglergraff V, Reutenauer A, Herrbach E, Lemaire O et al. 1992. Agroinfection as an alternative to insects for infecting plants with beet western yellows luteovirus. PNAS 89:9136–40
    [Google Scholar]
  73. 73.  Levy A, Zheng JY, Lazarowitz SG 2013. The tobamovirus Turnip vein clearing virus 30-kilodalton movement protein localizes to novel nuclear filaments to enhance virus infection. J. Virol. 87:6428–40
    [Google Scholar]
  74. 74.  Li J, Chen Q, Lin Y, Jiang T, Wu G, Hua H 2011. RNA interference in Nilaparvata lugens (Homoptera: Delphacidae) based on dsRNA ingestion. Pest Manag. Sci. 67:852–59
    [Google Scholar]
  75. 75.  Li J-F, 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]
  76. 76.  Lim HS, Lee MY, Moon JS, Moon JK, Yu YM et al. 2013. Actin cytoskeleton and Golgi involvement in Barley stripe mosaic virus movement and cell wall localization of triple gene block proteins. Plant Pathol. J. 29:17–30
    [Google Scholar]
  77. 77.  Liu Y, Nakayama N, Schiff M, Litt A, Irish VF, Dinesh-Kumar SP 2004. Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana. Plant Mol. Biol. 54:701–11
    [Google Scholar]
  78. 78.  Liu Y, Schiff M, Dinesh-Kumar SP 2002. Virus-induced gene silencing in tomato. Plant J 31:777–86
    [Google Scholar]
  79. 79.  Lyon GM, Mehta AK, Varkey JB, Brantly K, Plyler L et al. 2014. Clinical care of two patients with Ebola virus disease in the United States. N. Engl. J. Med. 371:252402–9
    [Google Scholar]
  80. 80.  Mamta M, Dutta TK, Tripathi MK 2015. Rumen fermentation pattern of Barbari kids at different physiological stages under semi-intensive system of production. Indian J. Anim. Sci. 85:64–66
    [Google Scholar]
  81. 81.  Mandal MK, Ahvari H, Schillberg S, Schiermeyer A 2016. Tackling unwanted proteolysis in plant production hosts used for molecular farming. Front. Plant Sci. 7:267
    [Google Scholar]
  82. 82.  Mandal MK, Fischer R, Schillberg S, Schiermeyer A 2014. Inhibition of protease activity by antisense RNA improves recombinant protein production in Nicotiana tabacum cv. Bright Yellow 2 (BY-2) suspension cells. Biotechnol. J. 9:1065–73
    [Google Scholar]
  83. 83.  Marillonnet S, Thoeringer C, Kandzia R, Klimyuk V, Gleba Y 2005. Systemic Agrobacterium tumefaciens–mediated transfection of viral replicons for efficient transient expression in plants. Nat. Biotechnol. 23:718–23
    [Google Scholar]
  84. 84.  Marks CE, Ladiges PY, Newbigin E 2011. Karyotypic variation in Nicotiana section Suaveolentes. Genet. Resour. Crop. Evol. 58:797–803
    [Google Scholar]
  85. 85.  Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R, Goodin MM 2009. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. . Plant J 59:150–62
    [Google Scholar]
  86. 86.  Martin KM, Dietzgen RG, Wang R, Goodin MM 2012. Lettuce necrotic yellows cytorhabdovirus protein localization and interaction map, and comparison with nucleorhabdoviruses. J. Gen. Virol. 93:906–14
    [Google Scholar]
  87. 87.  Mathur J, Radhamony R, Sinclair AM, Donoso A, Dunn N et al. 2010. mEosFP-based green-to-red photoconvertible subcellular probes for plants. Plant Physiol 154:1573–87
    [Google Scholar]
  88. 88.  Mehlhorn DG, Wallmeroth N, Berendzen KW, Grefen C 2018. 2in1 vectors improve in planta BiFC and FRET analyses. Methods Mol. Biol. 1691:139–58
    [Google Scholar]
  89. 89.  Meier I, Richards EJ, Evans DE 2017. Cell biology of the plant nucleus. Annu. Rev. Plant Biol. 68:139–72
    [Google Scholar]
  90. 90.  Mermigka G, Verret F, Kalantidis K 2016. RNA silencing movement in plants. J. Integr. Plant Biol. 58:328–42
    [Google Scholar]
  91. 91.  Mills-Lujan K, Andrews DL, Chou CW, Deom CM 2015. The roles of phosphorylation and SHAGGY-like protein kinases in geminivirus C4 protein induced hyperplasia. PLOS ONE 10:e0122356
    [Google Scholar]
  92. 92.  Min BE, Martin K, Wang R, Tafelmeyer P, Bridges M, Goodin M 2010. A host-factor interaction and localization map for a plant-adapted rhabdovirus implicates cytoplasm-tethered transcription activators in cell-to-cell movement. Mol. Plant-Microbe Interact. 23:1420–32
    [Google Scholar]
  93. 93.  Naim F, Nakasugi K, Crowhurst RN, Hilario E, Zwart AB et al. 2012. Advanced engineering of lipid metabolism in Nicotiana benthamiana using a draft genome and the V2 viral silencing-suppressor protein. PLOS ONE 7:e52717
    [Google Scholar]
  94. 94.  Nakasugi K, Crowhurst R, Bally J, Waterhouse P 2014. Combining transcriptome assemblies from multiple de novo assemblers in the allo-tetraploid plant Nicotiana benthamiana. . PLOS ONE 9:e91776
    [Google Scholar]
  95. 95.  Nakasugi K, Crowhurst RN, Bally J, Wood CC, Hellens RP, Waterhouse PM 2013. De novo transcriptome sequence assembly and analysis of RNA silencing genes of Nicotiana benthamiana. . PLOS ONE 8:e59534
    [Google Scholar]
  96. 96.  Nawaz-ul-Rehman MS, Prasanth KR, Xu K, Sasvari Z, Kovalev N et al. 2016. Viral replication protein inhibits cellular cofilin actin depolymerization factor to regulate the actin network and promote viral replicase assembly. PLOS Pathog 12:e1005440
    [Google Scholar]
  97. 97.  Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31:691–93
    [Google Scholar]
  98. 98.  Offenborn JN, Waadt R, Kudla J 2015. Visualization and translocation of ternary calcineurin-A/calcineurin-B/calmodulin-2 protein complexes by dual-color trimolecular fluorescence complementation. New Phytol 208:269–79
    [Google Scholar]
  99. 99.  Palacpac NQ, Yoshida S, Sakai H, Kimura Y, Fujiyama K et al. 1999. Stable expression of human β1,4-galactosyltransferase in plant cells modifies N-linked glycosylation patterns. PNAS 96:4692–97
    [Google Scholar]
  100. 100.  Palmer EK, Gleba Y, eds. 2014. Plant Viral Vectors New York: Springer
  101. 101.  Park E, Lee HY, Woo J, Choi D, Dinesh-Kumar SP 2017. Spatiotemporal monitoring of Pseudomonas syringae effectors via type III secretion using split fluorescent protein fragments. Plant Cell 29:1571–84
    [Google Scholar]
  102. 102.  Petre B, Saunders DG, Sklenar J, Lorrain C, Win J et al. 2015. Candidate effector proteins of the rust pathogen Melampsora larici-populina target diverse plant cell compartments. Mol. Plant-Microbe Interact. 28:689–700
    [Google Scholar]
  103. 103.  Petrie JR, Shrestha P, Liu Q, Mansour MP, Wood CC et al. 2010. Rapid expression of transgenes driven by seed-specific constructs in leaf tissue: DHA production. Plant Methods 6:8
    [Google Scholar]
  104. 104.  Peyret H, Lomonossoff GP 2015. When plant virology met Agrobacterium: the rise of the deconstructed clones. Plant Biotechnol. J. 13:1121–35
    [Google Scholar]
  105. 105.  Pflieger S, Blanchet S, Camborde L, Drugeon G, Rousseau A et al. 2008. Efficient virus-induced gene silencing in Arabidopsis using a ‘one-step’ TYMV-derived vector. Plant J 56:678–90
    [Google Scholar]
  106. 106.  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]
  107. 107.  Powell JD 2015. From pandemic preparedness to biofuel production: Tobacco finds its biotechnology niche in North America. Agriculture 5:901–17
    [Google Scholar]
  108. 108.  Ramalho TO, Figueira AR, Sotero AJ, Wang R, Geraldino Duarte PS et al. 2014. Characterization of Coffee ringspot virus-Lavras: a model for an emerging threat to coffee production and quality. Virology 464–65:385–96
    [Google Scholar]
  109. 109.  Ratcliff F, Martin-Hernandez AM, Baulcombe DC 2001. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J 25:237–45
    [Google Scholar]
  110. 110.  Reynolds KB, Taylor MC, Cullerne DP, Blanchard CL, Wood CC et al. 2017. A reconfigured Kennedy pathway which promotes efficient accumulation of medium-chain fatty acids in leaf oils. Plant Biotechnol. J. 15:111397–408
    [Google Scholar]
  111. 111.  Rioja C, Van Wees SC, Charlton KA, Pieterse CM, Lorenzo O, Garcia-Sanchez S 2013. Wide screening of phage-displayed libraries identifies immune targets in planta. PLOS ONE 8:e54654
    [Google Scholar]
  112. 112.  Ruiz MT, Voinnet O, Baulcombe DC 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:937–46
    [Google Scholar]
  113. 113.  Ruiz V, Mozgovoj MV, Dus Santos MJ, Wigdorovitz A 2015. Plant-produced viral bovine vaccines: What happened during the last 10 years?. Plant Biotechnol. J. 13:1071–77
    [Google Scholar]
  114. 114.  Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B 2017. Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J 92:787–95
    [Google Scholar]
  115. 115.  Scofield SR, Huang L, Brandt AS, Gill BS 2005. Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138:2165–73
    [Google Scholar]
  116. 116.  Scofield SR, Nelson RS 2009. Resources for virus-induced gene silencing in the grasses. Plant Physiol 149:152–57
    [Google Scholar]
  117. 117.  Shamloul M, Trusa J, Mett V, Yusibov V 2014. Optimization and utilization of Agrobacterium-mediated transient protein production in Nicotiana. J. Vis. . Exp 86:e51204
    [Google Scholar]
  118. 118.  Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–12
    [Google Scholar]
  119. 119.  Sourrouille C, Marquet-Blouin E, D'Aoust MA, Kiefer-Meyer MC, Seveno M et al. 2008. Down-regulated expression of plant-specific glycoepitopes in alfalfa. Plant Biotechnol. J. 6:702–21
    [Google Scholar]
  120. 120.  Stephan D, Maiss E 2006. Biological properties of Beet mild yellowing virus derived from a full-length cDNA clone. J. Gen. Virol. 87:445–49
    [Google Scholar]
  121. 121.  Strasser R, Altmann F, Mach L, Glossl J, Steinkellner H 2004. Generation of Arabidopsis thaliana plants with complex N-glycans lacking β1,2-linked xylose and core α1,3-linked fucose. FEBS Lett 561:132–36
    [Google Scholar]
  122. 122.  Strasser R, Stadlmann J, Schahs M, Stiegler G, Quendler H et al. 2008. Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol. J. 6:392–402
    [Google Scholar]
  123. 123.  Tzfira T, Tian GW, Lacroix B, Vyas S, Li J et al. 2005. pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol. Biol. 57:503–16
    [Google Scholar]
  124. 124.  Van Dijk P, Van Der Meer FA, Piron PGM 1987. Accessions of Australian Nicotiana species suitable as indicator hosts in the diagnosis of plant virus diseases. Neth. J. Plant Pathol. 93:73–85
    [Google Scholar]
  125. 125.  Van Kammen A 1997. Virus-induced gene silencing in infected and transgenic plants. Trends Plant Sci 2:409–11
    [Google Scholar]
  126. 126.  Velasquez AC, Chakravarthy S, Martin GB 2009. Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. J. Vis. Exp. 28:1292
    [Google Scholar]
  127. 127.  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]
  128. 128.  Wang JE, Li DW, Gong ZH, Zhang YL 2013. Optimization of virus-induced gene silencing in pepper (Capsicum annuum L.). Genet. Mol. Res. 12:2492–506
    [Google Scholar]
  129. 129.  Wang Q, Ma X, Qian S, Zhou X, Sun K et al. 2015. Rescue of a plant negative-strand RNA virus from cloned cDNA: insights into enveloped plant virus movement and morphogenesis. PLOS Pathog 11:e1005223
    [Google Scholar]
  130. 130.  Waterhouse PM, Helliwell CA 2003. Exploring plant genomes by RNA-induced gene silencing. Nat. Rev. Genet. 4:29–38
    [Google Scholar]
  131. 131.  Wei Y, Liu W, Hu W, Liu G, Wu C et al. 2017. Genome-wide analysis of autophagy-related genes in banana highlights MaATG8s in cell death and autophagy in immune response to Fusarium wilt. Plant Cell Rep 36:1237–50
    [Google Scholar]
  132. 132.  Wood CC, Petrie JR, Shrestha P, Mansour MP, Nichols PD et al. 2009. A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. Plant Biotechnol. J. 7:914–24
    [Google Scholar]
  133. 133.  Wylie SJ, Zhang C, Long V, Roossinck MJ, Koh SH et al. 2015. Differential responses to virus challenge of laboratory and wild accessions of Australian species of Nicotiana, and comparative analysis of RDR1 gene sequences. PLOS ONE 10:e0121787
    [Google Scholar]
  134. 134.  Xie W, Nielsen ME, Pedersen C, Thordal-Christensen H 2017. A split-GFP gateway cloning system for topology analyses of membrane proteins in plants. PLOS ONE 12:e0170118
    [Google Scholar]
  135. 135.  Xu K, Nagy PD 2016. Enrichment of phosphatidylethanolamine in viral replication compartments via co-opting the endosomal Rab5 small GTPase by a positive-strand RNA virus. PLOS Biol 14:e2000128
    [Google Scholar]
  136. 136.  Yang SJ, Carter SA, Cole AB, Cheng NH, Nelson RS 2004. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. . PNAS 101:6297–302
    [Google Scholar]
  137. 137.  Yin KQ, Tang Y, Zhao JP 2015. Genome-wide characterization of miRNAs involved in N gene-mediated immunity in response to tobacco mosaic virus in Nicotiana benthamiana. Evol. Bioinform. 11:Suppl. 11–11
    [Google Scholar]
  138. 138.  Ying XB, Dong L, Zhu H, Duan CG, Du QS et al. 2010. RNA-dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. . Plant Cell 22:1358–72
    [Google Scholar]
  139. 139.  Yoon JY, Choi SK, Palukaitis P, Gray SM 2011. Agrobacterium-mediated infection of whole plants by yellow dwarf viruses. Virus Res 160:428–34
    [Google Scholar]
  140. 140.  Zhai N, Jia H, Liu D, Liu S, Ma M et al. 2017. GhMAP3K65, a cotton Raf-like MAP3K gene, enhances susceptibility to pathogen infection and heat stress by negatively modulating growth and development in transgenic Nicotiana benthamiana. Int. J. Mol. Sci. 18:2462
    [Google Scholar]
  141. 141.  Zhang L, Ni H, Du X, Wang S, Ma XW et al. 2017. The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections. New Phytol 215:368–81
    [Google Scholar]
  142. 142.  Zhang XY, Dong SW, Xiang HY, Chen XR, Li DW et al. 2015. Development of three full-length infectious cDNA clones of distinct brassica yellows virus genotypes for agrobacterium-mediated inoculation. Virus Res 197:13–16
    [Google Scholar]
  143. 143.  Zhang Z, Thomma BP 2014. Virus-induced gene silencing and Agrobacterium tumefaciens–mediated transient expression in Nicotiana tabacum. Methods Mol. Biol. 1127:173–81
    [Google Scholar]
  144. 144.  Zhong G, Zhu Q, Li Y, Liu Y, Wang H 2017. Once for all: a novel robust system for co-expression of multiple chimeric fluorescent fusion proteins in plants. Front. Plant Sci. 8:1071
    [Google Scholar]
  145. 145.  Zhou T, Liu X, Fan Z 2018. Use of a virus gene silencing vector for maize functional genomics research. Methods Mol. Biol. 1676:141–50
    [Google Scholar]
  146. 146.  Zhu S, Jeong RD, Venugopal SC, Lapchyk L, Navarre D et al. 2011. SAG101 forms a ternary complex with EDS1 and PAD4 and is required for resistance signaling against turnip crinkle virus. PLOS Pathog 7:e1002318
    [Google Scholar]
  147. 147.  Zimin AV, Puiu D, Hall R, Kingan S, Clavijo BJ, Salzberg SL 2017. The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum. GigaSci 6:1–7
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-080417-050141
Loading
/content/journals/10.1146/annurev-phyto-080417-050141
Loading

Data & Media loading...

  • Article Type: Review Article
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