Twenty years ago, breakthroughs for reverse genetics analyses of negative-strand RNA (NSR) viruses were achieved by devising conditions for generation of infectious viruses in susceptible cells. Recombinant strategies have subsequently been engineered for members of all vertebrate NSR virus families, and research arising from these advances has profoundly increased understanding of infection cycles, pathogenesis, and complexities of host interactions of animal NSR viruses. These strategies also permitted development of many applications, including attenuated vaccines and delivery vehicles for therapeutic and biotechnology proteins. However, for a variety of reasons, it was difficult to devise procedures for reverse genetics analyses of plant NSR viruses. In this review, we discuss advances that have circumvented these problems and resulted in construction of a recombinant system for Sonchus yellow net nucleorhabdovirus. We also discuss possible extensions to other plant NSR viruses as well as the applications that may emanate from recombinant analyses of these pathogens.


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Literature Cited

  1. Albertini AA, Baquero E, Ferlin A, Gaudin Y. 1.  2012. Molecular and cellular aspects of rhabdovirus entry. Viruses 4:117–39 [Google Scholar]
  2. Ammar el-D, Tsai CW, Whitfield AE, Redinbaugh MG, Hogenhout SA. 2.  2009. Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Annu. Rev. Entomol. 54:447–68 [Google Scholar]
  3. Ammayappan A, Kurath G, Thompson TM, Vakharia VN. 3.  2011. A reverse genetics system for the Great Lakes strain of viral hemorrhagic septicemia virus: the NV gene is required for pathogenicity. Mar. Biotechnol. 13:672–83 [Google Scholar]
  4. Ammayappan A, Lapatra SE, Vakharia VN. 4.  2010. A vaccinia-virus-free reverse genetics system for infectious hematopoietic necrosis virus. J. Virol. Methods 167:132–39 [Google Scholar]
  5. An HY, Kim GN, Wu K, Kang CY. 5.  2013. Genetically modified VSV(NJ) vector is capable of accommodating a large foreign gene insert and allows high level gene expression. Virus Res. 171:168–77 [Google Scholar]
  6. Anderson G, Wang R, Bandyopadhyay A, Goodin M. 6.  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]
  7. Andino R, Domingo E. 7.  2015. Viral quasispecies. Virology 479–480:46–51 [Google Scholar]
  8. Baltimore D, Huang AS, Stampfer M. 8.  1970. Ribonucleic acid synthesis of vesicular stomatitis virus. II. An RNA polymerase in the virion. PNAS 66:572–76 [Google Scholar]
  9. Banerjee AK. 9.  2008. Response to “Non-segmented negative-strand RNA virus RNA synthesis in vivo.”. Virology 371:231–33 [Google Scholar]
  10. Billecocq A, Gauliard N, Le May N, Elliott RM, Flick R, Bouloy M. 10.  2008. RNA polymerase I–mediated expression of viral RNA for the rescue of infectious virulent and avirulent Rift Valley fever viruses. Virology 378:377–84 [Google Scholar]
  11. Black LM. 11.  1969. Insect tissue cultures as tools in plant virus research. Annu. Rev. Phytopathol. 7:73–100 [Google Scholar]
  12. Black LM. 12.  1979. Vector cell monolayers and plant viruses. Adv. Virus Res. 25:191–271 [Google Scholar]
  13. Blakqori G, Kochs G, Haller O, Weber F. 13.  2003. Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J. Gen. Virol. 84:1207–14 [Google Scholar]
  14. Blakqori G, Weber F. 14.  2005. Efficient cDNA-based rescue of La Crosse bunyaviruses expressing or lacking the nonstructural protein NSS. J. Virol. 79:10420–28 [Google Scholar]
  15. Bridgen A. 15.  2012. Reverse Genetics of RNA Viruses: Applications and Perspectives Chichester, UK: Wiley [Google Scholar]
  16. Bridgen A, Elliott RM. 16.  1996. Rescue of a segmented negative-strand RNA virus entirely from cloned complementary DNAs. PNAS 93:15400–4 [Google Scholar]
  17. Burgyan J, Havelda Z. 17.  2011. Viral suppressors of RNA silencing. Trends Plant Sci. 16:265–72 [Google Scholar]
  18. Chen L, Zhang S, Banerjee AK, Chen M. 18.  2013. N-terminal phosphorylation of phosphoprotein of vesicular stomatitis virus is required for preventing nucleoprotein from binding to cellular RNAs and for functional template formation. J. Virol. 87:3177–86 [Google Scholar]
  19. Chiba M, Reed JC, Prokhnevsky AI, Chapman EJ, Mawassi M. 19.  et al. 2006. Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. Virology 346:7–14 [Google Scholar]
  20. Cho WK, Lian S, Kim SM, Park SH, Kim KH. 20.  2013. Current insights into research on Rice stripe virus. Plant Pathol. J. 29:223–33 [Google Scholar]
  21. Collins PL, Hill MG, Camargo E, Grosfeld H, Chanock RM, Murphy BR. 21.  1995. Production of infectious human respiratory syncytial virus from cloned cDNA confirms an essential role for the transcription elongation factor from the 5′ proximal open reading frame of the M2 mRNA in gene expression and provides a capability for vaccine development. PNAS 92:11563–67 [Google Scholar]
  22. Conzelmann KK. 22.  2004. Reverse genetics of mononegavirales. Curr. Top. Microbiol. Immunol. 283:1–41 [Google Scholar]
  23. Cornu TI, de la Torre JC. 23.  2001. RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J. Virol. 75:9415–26 [Google Scholar]
  24. Curran J, Kolakofsky D. 24.  2008. Nonsegmented negative-strand RNA virus RNA synthesis in vivo. Virology 371:227–30 [Google Scholar]
  25. Dafny-Yelin M, Tzfira T. 25.  2007. Delivery of multiple transgenes to plant cells. Plant Physiol. 145:1118–28 [Google Scholar]
  26. de la Torre JC. 26.  2006. Reverse-genetic approaches to the study of Borna disease virus. Nat. Rev. Microbiol. 4:777–83 [Google Scholar]
  27. Deng M, Bragg JN, Ruzin S, Schichnes D, King D. 27.  et al. 2007. Role of the Sonchus yellow net virus N protein in formation of nuclear viroplasms. J. Virol. 81:5362–74 [Google Scholar]
  28. Dietzgen RG, Kuhn JH, Clawson AN, Freitas-Astua J, Goodin MM. 28.  et al. 2014. Dichorhavirus: a proposed new genus for Brevipalpus mite–transmitted, nuclear, bacilliform, bipartite, negative-strand RNA plant viruses. Arch. Virol. 159:607–19 [Google Scholar]
  29. Dietzgen RG, Kuzmin IV. 29.  2012. Taxonomy of rhabdoviruses. Rhabdoviruses: Molecular Taxonomy, Evolution, Genomics, Ecology, Host-Vector Interactions, Cytopathology and Control RG Dietzgen, IV Kuzmin 13–22 Norfolk, UK: UK Caister Acad. [Google Scholar]
  30. Ding SW. 30.  2010. RNA-based antiviral immunity. Nat. Rev. Immunol. 10:632–44 [Google Scholar]
  31. Doelling JH, Pikaard CS. 31.  1996. Species-specificity of rRNA gene transcription in plants manifested as a switch in RNA polymerase specificity. Nucleic Acids Res. 24:4725–32 [Google Scholar]
  32. Dunn EF, Pritlove DC, Jin H, Elliott RM. 32.  1995. Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology 211:133–43 [Google Scholar]
  33. Easton AJ, Pringle CR. 33.  2012. Order - Mononegavirales. Virus Taxonomy AMQ King, MJ Adams, EB Carstens, EJ Lefkowitz 653–57 San Diego, CA: Elsevier [Google Scholar]
  34. Elderfield RA, Hartgroves LCS, Barclay WS. 34.  2012. Using reverse genetics to improve influenza vaccines. See Ref. 15 224–49
  35. Elliott RM. 35.  2012. Bunyavirus reverse genetics and applications to studying interactions with host cells. See Ref. 15 200–23
  36. Emonet SE, Urata S, de la Torre JC. 36.  2011. Arenavirus reverse genetics: new approaches for the investigation of arenavirus biology and development of antiviral strategies. Virology 411:416–25 [Google Scholar]
  37. Engelhardt OG. 37.  2013. Many ways to make an influenza virus: review of influenza virus reverse genetics methods. Influ. Other Respir. Viruses 7:249–56 [Google Scholar]
  38. Falk BW, Tsai JH. 38.  1998. Biology and molecular biology of viruses in the genus Tenuivirus. Annu. Rev. Phytopathol. 36:139–63 [Google Scholar]
  39. Finke S, Conzelmann KK. 39.  2005. Recombinant rhabdoviruses: vectors for vaccine development and gene therapy. Curr. Top. Microbiol. Immunol. 292:165–200 [Google Scholar]
  40. Fodor E, Devenish L, Engelhardt OG, Palese P, Brownlee GG, Garcia-Sastre A. 40.  1999. Rescue of influenza A virus from recombinant DNA. J. Virol. 73:9679–82 [Google Scholar]
  41. Fooks AR, Banyard AC, Horton DL, Johnson N, McElhinney LM, Jackson AC. 41.  2014. Current status of rabies and prospects for elimination. Lancet 384:1389–99 [Google Scholar]
  42. Ganesan U, Bragg JN, Deng M, Marr S, Lee MY. 42.  et al. 2013. Construction of a Sonchus yellow net virus minireplicon: a step toward reverse genetic analysis of plant negative-strand RNA viruses. J. Virol. 87:10598–611 [Google Scholar]
  43. Gao Q, Park MS, Palese P. 43.  2008. Expression of transgenes from Newcastle disease virus with a segmented genome. J. Virol. 82:2692–98 [Google Scholar]
  44. Garbutt M, Liebscher R, Wahl-Jensen V, Jones S, Moller P. 44.  et al. 2004. Properties of replication-competent vesicular stomatitis virus vectors expressing glycoproteins of filoviruses and arenaviruses. J. Virol. 78:5458–65 [Google Scholar]
  45. Garcin D, Pelet T, Calain P, Roux L, Curran J, Kolakofsky D. 45.  1995. A highly recombinogenic system for the recovery of infectious Sendai paramyxovirus from cDNA: generation of a novel copy-back nondefective interfering virus. EMBO J. 14:6087–94 [Google Scholar]
  46. Gates B. 46.  2015. The next epidemic: lessons from Ebola. N. Engl. J. Med. 372:1381–84 [Google Scholar]
  47. Ghanem A, Conzelmann K-K. 47.  2012. Reverse genetics of rhabdoviruses. See Ref. 15 113–49
  48. Ghanem A, Kern A, Conzelmann KK. 48.  2012. Significantly improved rescue of rabies virus from cDNA plasmids. Eur. J. Cell Biol. 91:10–16 [Google Scholar]
  49. Gleba Y, Klimyuk V, Marillonnet S. 49.  2007. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol. 18:134–41 [Google Scholar]
  50. Goldberg KB, Modrell B, Hillman BI, Heaton LA, Choi TJ, Jackson AO. 50.  1991. Structure of the glycoprotein gene of Sonchus yellow net virus, a plant rhabdovirus. Virology 185:32–38 [Google Scholar]
  51. Goodin MM, Chakrabarty R, Yelton S, Martin K, Clark A, Brooks R. 51.  2007. Membrane and protein dynamics in live plant nuclei infected with Sonchus yellow net virus, a plant-adapted rhabdovirus. J. Gen. Virol. 88:1810–20 [Google Scholar]
  52. Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO. 52.  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]
  53. Habjan M, Penski N, Spiegel M, Weber F. 53.  2008. T7 RNA polymerase-dependent and -independent systems for cDNA-based rescue of Rift Valley fever virus. J. Gen. Virol. 89:2157–66 [Google Scholar]
  54. Himmelbach A, Zierold U, Hensel G, Riechen J, Douchkov D. 54.  et al. 2007. A set of modular binary vectors for transformation of cereals. Plant Physiol. 145:1192–200 [Google Scholar]
  55. Hoffmann E, Mahmood K, Yang CF, Webster RG, Greenberg HB, Kemble G. 55.  2002. Rescue of influenza B virus from eight plasmids. PNAS 99:11411–16 [Google Scholar]
  56. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 56.  2000. A DNA transfection system for generation of influenza A virus from eight plasmids. PNAS 97:6108–13 [Google Scholar]
  57. Hogenhout SA, Ammar el-D, Whitfield AE, Redinbaugh MG. 57.  2008. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46:327–59 [Google Scholar]
  58. Huang Y, Tang Q, Nadin-Davis SA, Zhang S, Hooper CD. 58.  et al. 2010. Development of a reverse genetics system for a human rabies virus vaccine strain employed in China. Virus Res. 149:28–35 [Google Scholar]
  59. Huang YW, Geng YF, Ying XB, Chen XY, Fang RX. 59.  2005. Identification of a movement protein of rice yellow stunt rhabdovirus. J. Virol. 79:2108–14 [Google Scholar]
  60. Inoue K, Shoji Y, Kurane I, Iijima T, Sakai T, Morimoto K. 60.  2003. An improved method for recovering rabies virus from cloned cDNA. J. Virol. Methods 107:229–36 [Google Scholar]
  61. Jackson AO. 61.  1978. Partial characterization of the structural proteins of Sonchus yellow net virus. Virology 87:172–81 [Google Scholar]
  62. Jackson AO, Dietzgen RG, Goodin MM, Bragg JN, Deng M. 62.  2005. Biology of plant rhabdoviruses. Annu. Rev. Phytopathol. 43:623–60 [Google Scholar]
  63. Jackson AO, Francki RIB, Zuidema D. 63.  1987. Biology, structure and replication of plant rhabdoviruses. The Rhabdoviruses RR Wagner 427–508 New York: Plenum [Google Scholar]
  64. Jayakar HR, Jeetendra E, Whitt MA. 64.  2004. Rhabdovirus assembly and budding. Virus Res. 106:117–32 [Google Scholar]
  65. Jones RW, Jackson AO. 65.  1990. Replication of Sonchus yellow net virus in infected protoplasts. Virology 179:815–20 [Google Scholar]
  66. Jordan I, Lipkin WI. 66.  2001. Borna disease virus. Rev. Med. Virol. 11:37–57 [Google Scholar]
  67. Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL. 67.  2011. Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res. 162:184–202 [Google Scholar]
  68. Lafforgue G, Tromas N, Elena SF, Zwart MP. 68.  2012. Dynamics of the establishment of systemic potyvirus infection: independent yet cumulative action of primary infection sites. J. Virol. 86:12912–22 [Google Scholar]
  69. Lawson ND, Stillman EA, Whitt MA, Rose JK. 69.  1995. Recombinant vesicular stomatitis viruses from DNA. PNAS 92:4477–81 [Google Scholar]
  70. Lindbo JA. 70.  2007. TRBO: a high-efficiency Tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 145:1232–40 [Google Scholar]
  71. Lowen AC, Noonan C, McLees A, Elliott RM. 71.  2004. Efficient bunyavirus rescue from cloned cDNA. Virology 330:493–500 [Google Scholar]
  72. Ma Y, Wu W, Chen H, Liu Q, Jia D. 72.  et al. 2013. An insect cell line derived from the small brown planthopper supports replication of rice stripe virus, a tenuivirus. J. Gen. Virol. 94:1421–25 [Google Scholar]
  73. Mann KS, Dietzgen RG. 73.  2014. Plant rhabdoviruses: new insights and research needs in the interplay of negative-strand RNA viruses with plant and insect hosts. Arch. Virol. 159:1889–900 [Google Scholar]
  74. Martin A, Staeheli P, Schneider U. 74.  2006. RNA polymerase II–controlled expression of antigenomic RNA enhances the rescue efficacies of two different members of the Mononegavirales independently of the site of viral genome replication. J. Virol. 80:5708–15 [Google Scholar]
  75. Martins CR, Johnson JA, Lawrence DM, Choi TJ, Pisi AM. 75.  et al. 1998. Sonchus yellow net rhabdovirus nuclear viroplasms contain polymerase-associated proteins. J. Virol. 72:5669–79 [Google Scholar]
  76. McGettigan JP, Naper K, Orenstein J, Koser M, McKenna PM, Schnell MJ. 76.  2003. Functional human immunodeficiency virus type 1 (HIV-1) Gag-Pol or HIV-1 Gag-Pol and env expressed from a single rhabdovirus-based vaccine vector genome. J. Virol. 77:10889–99 [Google Scholar]
  77. Melcher U. 77.  2000. The “30K” superfamily of viral movement proteins. J. Gen. Virol. 81:257–66 [Google Scholar]
  78. Min BE, Martin K, Wang R, Tafelmeyer P, Bridges M, Goodin M. 78.  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]
  79. Mondal A, Victor KG, Pudupakam RS, Lyons CE, Wertz GW. 79.  2014. Newly identified phosphorylation site in the vesicular stomatitis virus P protein is required for viral RNA synthesis. J. Virol. 88:1461–72 [Google Scholar]
  80. Morin B, Kranzusch PJ, Rahmeh AA, Whelan SP. 80.  2013. The polymerase of negative-stranded RNA viruses. Curr. Opin. Virol. 3:103–10 [Google Scholar]
  81. Neumann G, Fujii K, Kino Y, Kawaoka Y. 81.  2005. An improved reverse genetics system for influenza A virus generation and its implications for vaccine production. PNAS 102:16825–29 [Google Scholar]
  82. Neumann G, Kawaoka Y. 82.  2004. Reverse genetics systems for the generation of segmented negative-sense RNA viruses entirely from cloned cDNA. Curr. Top. Microbiol. Immunol. 283:43–60 [Google Scholar]
  83. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H. 83.  et al. 1999. Generation of influenza A viruses entirely from cloned cDNAs. PNAS 96:9345–50 [Google Scholar]
  84. Neumann G, Whitt MA, Kawaoka Y. 84.  2002. A decade after the generation of a negative-sense RNA virus from cloned cDNA: What have we learned?. J. Gen. Virol. 83:2635–62 [Google Scholar]
  85. Nguyen HT, Leelavathi S, Reddy VS. 85.  2004. Bacteriophage T7 RNA polymerase-directed, inducible and tissue-specific over-expression of foreign genes in transgenic plants. Plant Biotechnol. J. 2:301–10 [Google Scholar]
  86. Noton SL, Fearns R. 86.  2015. Initiation and regulation of paramyxovirus transcription and replication. Virology 479–480:545–54 [Google Scholar]
  87. Ogawa Y, Sugiura K, Kato K, Tohya Y, Akashi H. 87.  2007. Rescue of Akabane virus (family Bunyaviridae) entirely from cloned cDNAs by using RNA polymerase I. J. Gen. Virol. 88:3385–90 [Google Scholar]
  88. Ogino T, Banerjee AK. 88.  2011. An unconventional pathway of mRNA cap formation by vesiculoviruses. Virus Res. 162:100–9 [Google Scholar]
  89. Orbanz J, Finke S. 89.  2010. Generation of recombinant European bat lyssavirus type 1 and inter-genotypic compatibility of lyssavirus genotype 1 and 5 antigenome promoters. Arch. Virol. 155:1631–41 [Google Scholar]
  90. Osterholm MT, Moore KA, Kelley NS, Brosseau LM, Wong G. 90.  et al. 2015. Transmission of Ebola viruses: what we know and what we do not know. mBio 6:e00137 [Google Scholar]
  91. Pattnaik AK, Ball LA, LeGrone A, Wertz GW. 91.  1995. The termini of VSV DI particle RNAs are sufficient to signal RNA encapsidation, replication, and budding to generate infectious particles. Virology 206:760–64 [Google Scholar]
  92. Pattnaik AK, Ball LA, LeGrone AW, Wertz GW. 92.  1992. Infectious defective interfering particles of VSV from transcripts of a cDNA clone. Cell 69:1011–20 [Google Scholar]
  93. Pattnaik AK, Wertz GW. 93.  1990. Replication and amplification of defective interfering particle RNAs of vesicular stomatitis virus in cells expressing viral proteins from vectors containing cloned cDNAs. J. Virol. 64:2948–57 [Google Scholar]
  94. Pattnaik AK, Wertz GW. 94.  1991. Cells that express all five proteins of vesicular stomatitis virus from cloned cDNAs support replication, assembly, and budding of defective interfering particles. PNAS 88:1379–83 [Google Scholar]
  95. Pekosz A, He B, Lamb RA. 95.  1999. Reverse genetics of negative-strand RNA viruses: closing the circle. PNAS 96:8804–6 [Google Scholar]
  96. Pfaller CK, Cattaneo R, Schnell MJ. 96.  2015. Reverse genetics of Mononegavirales: how they work, new vaccines, and new cancer therapeutics. Virology 479–480C:331–44 [Google Scholar]
  97. Quan B, Seo HS, Blobel G, Ren Y. 97.  2014. Vesiculoviral matrix (M) protein occupies nucleic acid binding site at nucleoporin pair (Rae1·Nup98). PNAS 111:9127–32 [Google Scholar]
  98. Radecke F, Spielhofer P, Schneider H, Kaelin K, Huber M. 98.  et al. 1995. Rescue of measles viruses from cloned DNA. EMBO J. 14:5773–84 [Google Scholar]
  99. Rahmeh AA, Morin B, Schenk AD, Liang B, Heinrich BS. 99.  et al. 2012. Critical phosphoprotein elements that regulate polymerase architecture and function in vesicular stomatitis virus. PNAS 109:14628–33 [Google Scholar]
  100. Ramirez BC. 100.  2008. Tenuivirus. Desk Encyclopedia of Plant and Fungal Virology B Mahy, M van Regenmortel 320–23 Oxford, UK: Elsevier [Google Scholar]
  101. Roberts A, Buonocore L, Price R, Forman J, Rose JK. 101.  1999. Attenuated vesicular stomatitis viruses as vaccine vectors. J. Virol. 73:3723–32 [Google Scholar]
  102. Roberts A, Rose JK. 102.  1998. Recovery of negative-strand RNA viruses from plasmid DNAs: a positive approach revitalizes a negative field. Virology 247:1–6 [Google Scholar]
  103. Roberts A, Rose JK. 103.  1999. Redesign and genetic dissection of the rhabdoviruses. Adv. Virus Res. 53:301–19 [Google Scholar]
  104. Rodrigo G, Zwart MP, Elena SF. 104.  2014. Onset of virus systemic infection in plants is determined by speed of cell-to-cell movement and number of primary infection foci. J. R. Soc. Interface 11:20140555 [Google Scholar]
  105. Schnell MJ, Mebatsion T, Conzelmann KK. 105.  1994. Infectious rabies viruses from cloned cDNA. EMBO J. 13:4195–203 [Google Scholar]
  106. Schnell MJ, Tan GS, Dietzschold B. 106.  2005. The application of reverse genetics technology in the study of rabies virus (RV) pathogenesis and for the development of novel RV vaccines. J. Neurovirol. 11:76–81 [Google Scholar]
  107. Scholthof HB, Scholthof KB, Jackson AO. 107.  1996. Plant virus gene vectors for transient expression of foreign proteins in plants. Annu. Rev. Phytopathol. 34:299–323 [Google Scholar]
  108. Shaw M, Palese P. 108.  2013. Orthomyxoviruses. Fields Virology D Knipe, P Howley 1151–85 Philadelphia, PA: Lippincott [Google Scholar]
  109. Sin SH, McNulty BC, Kennedy GG, Moyer JW. 109.  2005. Viral genetic determinants for thrips transmission of Tomato spotted wilt virus. PNAS 102:5168–73 [Google Scholar]
  110. Soh TK, Whelan SP. 110.  2015. Tracking the fate of genetically distinct vesicular stomatitis virus matrix proteins highlights the role for late domains in assembly. J. Virol. 89:11750–60 [Google Scholar]
  111. Sun F, Yuan X, Zhou T, Fan Y, Zhou Y. 111.  2011. Arabidopsis is susceptible to Rice stripe virus infections. J. Phytopathol. 159:767–72 [Google Scholar]
  112. Sylvester ES, Richardson J. 112.  1992. Aphid-borne rhabdoviruses: relationships with their vectors. Advances in Disease Vector Research KF Harris 313–41 New York: Springer [Google Scholar]
  113. Tzfira T, Kozlovsky SV, Citovsky V. 113.  2007. Advanced expression vector systems: new weapons for plant research and biotechnology. Plant Physiol. 145:1087–89 [Google Scholar]
  114. Ueki S, Magori S, Lacroix B, Citovsky V. 114.  2013. Transient gene expression in epidermal cells of plant leaves by biolistic DNA delivery. Methods Mol. Biol. 940:17–26 [Google Scholar]
  115. Urwin P, Yi L, Martin H, Atkinson H, Gilmartin PM. 115.  2000. Functional characterization of the EMCV IRES in plants. Plant J. 24:583–89 [Google Scholar]
  116. Wagner JD, Choi TJ, Jackson AO. 116.  1996. Extraction of nuclei from Sonchus yellow net rhabdovirus-infected plants yields a polymerase that synthesizes viral mRNAs and polyadenylated plus-strand leader RNA. J. Virol. 70:468–77 [Google Scholar]
  117. Wagner JD, Jackson AO. 117.  1997. Characterization of the components and activity of Sonchus yellow net rhabdovirus polymerase. J. Virol. 71:2371–82 [Google Scholar]
  118. Walker PJ, Dietzgen RG, Joubert DA, Blasdell KR. 118.  2011. Rhabdovirus accessory genes. Virus Res. 162:110–25 [Google Scholar]
  119. Walpita P, Flick R. 119.  2005. Reverse genetics of negative-stranded RNA viruses: a global perspective. FEMS Microbiol. Lett. 244:9–18 [Google Scholar]
  120. Wang Q, Ma X, Qian S, Zhou X, Sun K. 120.  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]
  121. Whelan SP. 121.  2008. Response to “Non-segmented negative-strand RNA virus RNA synthesis in vivo.”. Virology 371:234–37 [Google Scholar]
  122. Whelan SP, Ball LA, Barr JN, Wertz GT. 122.  1995. Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. PNAS 92:8388–92 [Google Scholar]
  123. Whelan SP, Barr JN, Wertz GW. 123.  2004. Transcription and replication of nonsegmented negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:61–119 [Google Scholar]
  124. Whelan SP, Wertz GW. 124.  1999. The 5′ terminal trailer region of vesicular stomatitis virus contains a position-dependent cis-acting signal for assembly of RNA into infectious particles. J. Virol. 73:307–15 [Google Scholar]
  125. Whitfield AE, Ullman DE, German TL. 125.  2005. Tospovirus-thrips interactions. Annu. Rev. Phytopathol. 43:459–89 [Google Scholar]
  126. Xiong R, Wu J, Zhou Y, Zhou X. 126.  2008. Identification of a movement protein of the Tenuivirus rice stripe virus. J. Virol. 82:12304–11 [Google Scholar]
  127. Xu Y, Zhou X. 127.  2012. Role of rice stripe virus NSvc4 in cell-to-cell movement and symptom development in Nicotiana benthamiana. Front. Plant Sci. 3:269 [Google Scholar]
  128. Zhang C, Pei X, Wang Z, Jia S, Guo S. 128.  et al. 2012. The Rice stripe virus pc4 functions in movement and foliar necrosis expression in Nicotiana benthamiana. Virology 425:113–21 [Google Scholar]

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