Rescue of a Plant Negative-Strand RNA Virus from Cloned cDNA: Insights into Enveloped Plant Virus Movement and Morphogenesis

PLoS Pathogens

Volumn 11, Issue 10, 2015, Pages

  Wang, Qiang ^a   Ma, Xiaonan ^a   Qian, ShaSha ^a   Zhou, Xin ^a   Sun, Kai ^a   Chen, Xiaolan ^a   Zhou, Xueping ^a,b   Jackson, Andrew O ^c   Li, Zhenghe ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CORE PROTEIN; GREEN FLUORESCENT PROTEIN; PHOSPHOPROTEIN; RNA POLYMERASE; VIRUS GLYCOPROTEIN; VIRUS NUCLEOPROTEIN; PLANT RNA;

AGROBACTERIUM TUMEFACIENS; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENE DELETION; GENE SILENCING; INOCULATION; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT DISEASE; PROTEIN EXPRESSION; RESTRICTION SITE; REVERSE GENETICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SONCHUS YELLOW NET RHABDOVIRUS INFECTION; VIRUS INFECTION; VIRUS MORPHOGENESIS; VIRUS NUCLEOCAPSID; VIRUS RECOMBINANT; VIRUS TRANSCRIPTION; WESTERN BLOTTING; GENETICS; IMMUNOBLOTTING; ISOLATION AND PURIFICATION; PLANT VIRUS; PROCEDURES; RHABDOVIRIDAE; RHABDOVIRUS INFECTION; SONCHUS; VIROLOGY;

DNA, COMPLEMENTARY; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; PLANT DISEASES; PLANT VIRUSES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHABDOVIRIDAE; RHABDOVIRIDAE INFECTIONS; RNA, PLANT; SONCHUS;

EID: 84946011323     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005223     Document Type: Article

References (61)

1. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. London, UK: Elsevier Academic Press; 2011.
2. Mann KS, Dietzgen RG, Plant rhabdoviruses: new insights and research needs in the interplay of negative-strand RNA viruses with plant and insect hosts. Arch Virol. 2014; 159: 1889–1900. doi: 10.1007/s00705-014-2029-z 24610553
3. Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL, Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res. 2011; 162: 184–202. doi: 10.1016/j.virusres.2011.09.028 21963660
4. Ammar el D, Tsai CW, Whitfield AE, Redinbaugh MG, Hogenhout SA, Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Annu Rev Entomol. 2009; 54: 447–468. doi: 10.1146/annurev.ento.54.110807.090454 18793103
5. Falk BW, Tsai JH, Biology and molecular biology of viruses in the genus Tenuivirus. Annu Rev Phytopathol. 1998; 36: 139–163. 15012496
6. Whitfield AE, Ullman DE, German TL, Tospovirus-thrips interactions. Annu Rev Phytopathol. 2005; 43: 459–489. 16078892
7. Jackson AO, Dietzgen RG, Goodin MM, Bragg JN, Deng M, Biology of plant rhabdoviruses. Annu Rev Phytopathol. 2005; 43: 623–660. 16078897
8. Kawaoka Y, Biology of Negative Strand RNA Viruses: The Power of Reverse Genetics, Vol. 283, 1st ed. Springer-Verlag Berlin Heidelberg; 2004.
9. Walker PJ, Dietzgen RG, Joubert DA, Blasdell KR, Rhabdovirus accessory genes. Virus Res. 2011; 162: 110–125. doi: 10.1016/j.virusres.2011.09.004 21933691
10. Lawson ND, Stillman EA, Whitt MA, Rose JK, Recombinant vesicular stomatitis viruses from DNA. Proc Natl Acad Sci U S A. 1995; 92: 4477–4481. 7753828
11. Schnell MJ, Mebatsion T, Conzelmann KK, Infectious rabies viruses from cloned cDNA. EMBO J. 1994; 13: 4195–4203. 7925265
12. Whelan SP, Ball LA, Barr JN, Wertz GT, Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc Natl Acad Sci U S A. 1995; 92: 8388–8392. 7667300
13. Roberts A, Rose JK, Recovery of negative-strand RNA viruses from plasmid DNAs: a positive approach revitalizes a negative field. Virology. 1998; 247: 1–6. 9683565
14. Rose JK, Positive strands to the rescue again: a segmented negative-strand RNA virus derived from cloned cDNAs. Proc Natl Acad Sci U S A. 1996; 93: 14998–15000. 8986751
15. Schneider U, Schwemmle M, Staeheli P, Genome trimming: a unique strategy for replication control employed by Borna disease virus. Proc Natl Acad Sci U S A. 2005; 102: 3441–3446. 15728364
16. Volchkov VE, Volchkova VA, Muhlberger E, Kolesnikova LV, Weik M, Dolnik O, et al. Recovery of infectious Ebola virus from complementary DNA: RNA editing of the GP gene and viral cytotoxicity. Science. 2001; 291, 1965–1969. 11239157
17. Flatz L, Bergthaler A, de la Torre JC, Pinschewer DD, Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc Natl Acad Sci U S A. 2006; 103: 4663–4668. 16537369
18. Conzelmann KK, Reverse genetics of mononegavirales. Curr Top Microbiol Immunol. 2004; 283: 1–41. 15298166
19. Neumann G, Kawaoka Y, Reverse genetics systems for the generation of segmented negative-sense RNA viruses entirely from cloned cDNA. Curr Top Microbiol Immunol. 2004; 283: 43–60. 15298167
20. Walpita P, Flick R, Reverse genetics of negative-stranded RNA viruses: a global perspective. FEMS Microbiol Lett. 2005; 244: 9–18. 15727815
21. Stobart CC, Moore ML, RNA virus reverse genetics and vaccine design. Viruses. 2014; 6: 2531–2550. doi: 10.3390/v6072531 24967693
22. Pfaller CK, Cattaneo R, Schnell MJ, Reverse genetics of Mononegavirales: How they work, new vaccines, and new cancer therapeutics. Virology. 2015; 479-480C: 331–344.
23. Falzarano D, Groseth A, Hoenen T, Development and application of reporter-expressing mononegaviruses: current challenges and perspectives. Antiviral Res. 2014; 103: 78–87. doi: 10.1016/j.antiviral.2014.01.003 24462694
24. Scholthof KB, Hillman BI, Modrell B, Heaton LA, Jackson AO, Characterization and detection of sc4: a sixth gene encoded by sonchus yellow net virus. Virology. 1994; 204: 279–288. 8091658
25. van Beek NAM, Lohuis D, Dijkstra J, Peters D, Morphogenesis of Sonchus yellow net virus in cowpea protoplasts. J Ultrastruct Res. 1985; 90: 294–303.
26. Ganesan U, Bragg JN, Deng M, Marr S, Lee MY, Qian S, et al. Construction of a Sonchus Yellow Net Virus minireplicon: a step toward reverse genetic analysis of plant negative-strand RNA viruses. J Virol. 2013; 87: 10598–10611. doi: 10.1128/JVI.01397-13 23885070
27. Ding SW, RNA-based antiviral immunity. Nat Rev Immunol. 2010; 10: 632–644. doi: 10.1038/nri2824 20706278
28. Gleba Y, Klimyuk V, Marillonnet S, Viral vectors for the expression of proteins in plants. Curr Opin Biotechnol. 2007; 18: 134–141. 17368018
29. Lindbo JA, TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 2007; 145: 1232–1240. 17720752
30. Whelan SP, Barr JN, Wertz GW, Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol. 2004; 283: 61–119. 15298168
31. Wertz GW, Perepelitsa VP, Ball LA, Gene rearrangement attenuates expression and lethality of a nonsegmented negative strand RNA virus. Proc Natl Acad Sci U S A. 1998; 95: 3501–3506. 9520395
32. Black LM, Vector cell monolayers and plant viruses. Adv Virus Res. 1979; 25: 191–271. 393097
33. Ma Y, Wu W, Chen H, Liu Q, Jia D, Mao Q, et al. An insect cell line derived from the small brown planthopper supports replication of rice stripe virus, a tenuivirus. J Gen Virol. 2013; 94: 1421–1425. doi: 10.1099/vir.0.050104-0 23468422
34. Johansen LK, Carrington JC, Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 2001; 126: 930–938. 11457942
35. Voinnet O, Rivas S, Mestre P, Baulcombe D, An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 2003; 33: 949–956. 12609035
36. Chiba M, Reed JC, Prokhnevsky AI, Chapman EJ, Mawassi M, Koonin EV, et al. Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. Virology. 2006; 346: 7–14. 16300814
37. Ambrós S, El-Mohtar C, Ruiz-Ruiz S, Peña L, Guerri J, Dawson WO, et al. Agroinoculation of Citrus tristeza virus causes systemic infection and symptoms in the presumed nonhost Nicotiana benthamiana. Mol Plant Microbe Interact. 2011; 24: 1119–1131. doi: 10.1094/MPMI-05-11-0110 21899435
38. Kasschau KD, Carrington JC, Long-distance movement and replication maintenance functions correlate with silencing suppression activity of potyviral HC-Pro. Virology. 2001; 285: 71–81. 11414807
39. Qu F, Morris TJ, Efficient infection of Nicotiana benthamiana by Tomato bushy stunt virus is facilitated by the coat protein and maintained by p19 through suppression of gene silencing. Mol Plant Microbe Interact. 2002; 15: 193–202. 11952121
40. Lucas WJ, Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology. 2006; 344: 169–184. 16364748
41. Ueki S, Citovsky V, To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Mol Plant. 2011; 4: 782–793. doi: 10.1093/mp/ssr060 21746703
42. Huang YW, Geng YF, Ying XB, Chen XY, Fang RX, Identification of a movement protein of rice yellow stunt rhabdovirus. J Virol. 2005; 79: 2108–2114. 15681413
43. Martin KM, Dietzgen RG, Wang R, Goodin MM, Lettuce necrotic yellows cytorhabdovirus protein localization and interaction map, and comparison with nucleorhabdoviruses. J Gen Virol. 2012; 93: 906–914. doi: 10.1099/vir.0.038034-0 22190014
44. Melcher U, The '30K' superfamily of viral movement proteins. J Gen Virol. 2000; 81: 257–266. 10640565
45. Goodin MM, Chakrabarty R, Yelton S, Martin K, Clark A, Brooks R, Membrane and protein dynamics in live plant nuclei infected with Sonchus yellow net virus, a plant-adapted rhabdovirus. J Gen Virol. 2007; 88: 1810–1820. 17485543
46. Min BE, Martin K, Wang R, Tafelmeyer P, Bridges M, Goodin M, 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. 2010; 23: 1420–1432. doi: 10.1094/MPMI-04-10-0097 20923350
47. Soellick T, Uhrig JF, Bucher GL, Kellmann JW, Schreier PH, The movement protein NSm of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proc Natl Acad Sci U S A. 2000; 97: 2373–2378. 10688879
48. Leastro MO, Pallás V, Resende RO, Sánchez-Navarro JA, The movement proteins (NSm) of distinct tospoviruses peripherally associate with cellular membranes and interact with homologous and heterologous NSm and nucleocapsid proteins. Virology. 2015; 478: 39–49. 25705793
49. Tripathi D, Raikhy G, Pappu HR, Movement and nucleocapsid proteins coded by two tospovirus species interact through multiple binding regions in mixed infections. Virology. 2015; 478: 137–147. doi: 10.1016/j.virol.2015.01.009 25666522
50. Lyles DS, Assembly and budding of negative-strand RNA viruses. Adv Virus Res. 2013; 85: 57–90. doi: 10.1016/B978-0-12-408116-1.00003-3 23439024
51. Liljeroos L, Butcher SJ, Matrix proteins as centralized organizers of negative-sense RNA virions. Front Biosci. 2013; 18: 696–715.
52. Schmitt AP, Lamb RA, Escaping from the cell: assembly and budding of negative-strand RNA viruses. Curr Top Microbiol Immunol. 2004; 283: 145–196. 15298170
53. Goldberg KB, Modrell B, Hillman BI, Heaton LA, Choi TJ, Jackson AO, Structure of the glycoprotein gene of sonchus yellow net virus, a plant rhabdovirus. Virology. 1991; 185: 32–38. 1926779
54. Sin SH, McNulty BC, Kennedy GG, Moyer JW, Viral genetic determinants for thrips transmission of Tomato spotted wilt virus. Proc Natl Acad Sci U S A. 2005; 102: 5168–5173. 15753307
55. Gomme EA, Wanjalla CN, Wirblich C, Schnell MJ, Rabies virus as a research tool and viral vaccine vector. Adv Virus Res. 2011; 79: 139–164. doi: 10.1016/B978-0-12-387040-7.00009-3 21601047
56. Shen Y, Zhao X, Yao M, Li C, Miriam K, Zhang X, et al. A versatile complementation assay for cell-to-cell and long distance movements by cucumber mosaic virus based agro-infiltration. Virus Res. 2014; 190: 25–33. doi: 10.1016/j.virusres.2014.06.013 25014544
57. Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO, pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J. 2002; 31: 375–383. 12164816
58. Jackson AO, Wagner JD, Procedures for plant rhabdovirus purification, polyribosome isolation, and replicase extraction. Methods Mol Biol. 1998; 81: 77–97. 9760495
59. Jackson AO, Christie SR, Purification and some physicochemical properties of sonchus yellow net virus. Virology. 1977; 77: 344–355. 841865
60. Jones RW, Jackson AO, Replication of sonchus yellow net virus in infected protoplasts. Virology. 1990; 179: 815–820. 2238470
61. Kong L, Wu J, Lu L, Xu Y, Zhou X, Interaction between Rice stripe virus disease-specific protein and host PsbP enhances virus symptoms. Mol Plant. 2014; 7: 691–708. doi: 10.1093/mp/sst158 24214893