Encapsidation of Host RNAs by Cucumber Necrosis Virus Coat Protein during both Agroinfiltration and Infection

Journal of Virology

Volumn 89, Issue 21, 2015, Pages 10748-10761

  Ghoshal, Kankana ^a   Theilmann, Jane ^b   Reade, Ron ^b   Maghodia, Ajay ^b   Rochon, D ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; MESSENGER RNA; RIBOSOME RNA; RNA; PLANT RNA; RETROPOSON;

AGRICULTURAL INOCULATION; AGROINFILTRATION; ARTICLE; BINDING AFFINITY; BINDING SITE; CHLOROPLAST; CONTROLLED STUDY; CUCUMBER NECROSIS VIRUS; CYTOPLASM; ENCAPSIDATION; GENE EXPRESSION; HORIZONTAL GENE TRANSFER; HOST CELL; MITOCHONDRION; NEXT GENERATION SEQUENCING; NONHUMAN; OPEN READING FRAME; PLANT VIRUS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; RETROPOSON; RNA SEQUENCE; RNA SYNTHESIS; VIRAL PHENOMENA AND FUNCTIONS; VIRUS INFECTION; VIRUS LIKE AGENT; COP-COATED VESICLE; CUCUMBER; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TOMBUSVIRUS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRION; VIROLOGY; WESTERN BLOTTING;

BASE SEQUENCE; BINDING SITES; BLOTTING, NORTHERN; BLOTTING, WESTERN; CHLOROPLASTS; COP-COATED VESICLES; CUCUMIS SATIVUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EVOLUTION, MOLECULAR; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; RETROELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, PLANT; SEQUENCE ANALYSIS, RNA; TOMBUSVIRUS; VIRION;

EID: 84945208006     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01466-15     Document Type: Article

References (62)

1. Annamalai P, Rao AL. 2007. In vivo packaging of brome mosaic virus RNA3, but not RNAs 1 and 2, is dependent on a cis-acting 3= tRNA-like structure. J Virol 81:173-181. http://dx.doi.org/10.1128/JVI.01500-06.
2. Basnayake VR, Sit TL, Lommel SA. 2009. The red clover necrotic mosaic virus origin of assembly is delimited to the RNA-2 trans-activator. Virology 384:169-178. http://dx.doi.org/10.1016/j.virol.2008.11.005.
3. Bink HH, Schirawski J, Haenni AL, Pleij CW. 2003. The 5=-proximal hairpin of turnip yellow mosaic virus RNA: its role in translation and encapsidation. J Virol 77:7452-7458. http://dx.doi.org/10.1128/JVI.77.13 .7452-7458.2003.
4. Borodavka A, Tuma R, Stockley PG. 2012. Evidence that viral RNAs have evolved for efficient, two-stage packaging. Proc Natl Acad Sci U S A 109: 15769-15774. http://dx.doi.org/10.1073/pnas.1204357109.
5. Choi YG, Rao AL. 2003. Packaging of brome mosaic virus RNA3 is mediated through a bipartite signal. J Virol 77:9750-9757. http://dx.doi .org/10.1128/JVI.77.18.9750-9757.2003.
6. Damayanti TA, Tsukaguchi S, Mise K, Okuno T. 2003. cis-Acting elements required for efficient packaging of brome mosaic virus RNA3 in barley protoplasts. J Virol 77:9979-9986. http://dx.doi.org/10.1128/JVI .77.18.9979-9986.2003.
7. Frolova E, Frolov I, Schlesinger S. 1997. Packaging signals in alphaviruses. J Virol 71:248-258.
8. Hemmer O, Dunoyer P, Richards K, Fritsch C. 2003. Mapping of viral RNA sequences required for assembly of peanut clump virus particles. J Gen Virol 84:2585-2594. http://dx.doi.org/10.1099/vir.0.19247-0.
9. Johnson SF, Telesnitsky A. 2010. Retroviral RNA dimerization and packaging: the what, how, when, where, and why. PLoS Pathog 6:e1001007. http://dx.doi.org/10.1371/journal.ppat.1001007.
10. Kemler I, Barraza R, Poeschla EM. 2002. Mapping the encapsidation determinants of feline immunodeficiency virus. J Virol 76:11889-11903. http://dx.doi.org/10.1128/JVI.76.23.11889-11903.2002.
11. Kwon SJ, Park MR, Kim KW, Plante CA, Hemenway CL, Kim KH.cis-Acting sequences required for coat protein binding and in vitro assembly of potato virus X. Virology 334:83-97. http://dx.doi.org/10.1016 /j.virol.2005.01.018.
12. McBride MS, Schwartz MD, Panganiban AT. 1997. Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J Virol 71:4544- 4554.
13. Murakami S, Terasaki K, Narayanan K, Makino S. 2012. Roles of the coding and noncoding regions of Rift Valley fever virus RNA genome segments in viral RNA packaging. J Virol 86:4034-4039. http://dx.doi.org /10.1128/JVI.06700-11.
14. Qu F, Morris TJ. 1997. Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. J Virol 71:1428-1435.
15. Rochon D, Siegel A. 1984. Chloroplast DNA transcripts are encapsidated by tobacco mosaic virus coat protein. Proc Natl Acad Sci U S A 81:1719-1723 http://dx.doi.org/10.1073/pnas.81.6.1719.
16. Zhong W, Dasgupta R, Rueckert R. 1992. Evidence that the packaging signal for nodaviral RNA2 is a bulged stem-loop. Proc Natl Acad Sci U S A 89:11146-11150. http://dx.doi.org/10.1073/pnas.89.23.11146.
17. Zimmern D, Butler PJ. 1977. The isolation of tobacco mosaic virus RNA fragments containing the origin for viral assembly. Cell 11:455-462. http: //dx.doi.org/10.1016/0092-8674(77)90064-2.
18. Gopal R, Venter PA, Schneemann A. 2014. Differential segregation of nodaviral coat protein and RNA into progeny virions during mixed infection with FHV and NoV. Virology 454-455:280-290. http://dx.doi.org/10 .1016/j.virol.2014.03.003.
19. Patel N, Dykeman EC, Coutts RH, Lomonossoff GP, Rowlands DJ, Phillips SE, Ranson N, Twarock R, Tuma R, Stockley PG. 2015. Revealing the density of encoded functions in a viral RNA. Proc Natl Acad Sci U S A 112:2227-2232. http://dx.doi.org/10.1073/pnas.1420812112.
20. Liu Y, Wang C, Mueller S, Paul AV, Wimmer E, Jiang P. 2010. Direct interaction between two viral proteins, the nonstructural protein 2C and the capsid protein VP3, is required for enterovirus morphogenesis. PLoS Pathog 6:e1001066. http://dx.doi.org/10.1371/journal.ppat.1001066.
21. Pickett GG, Peabody DS. 1993. Encapsidation of heterologous RNAs by bacteriophage MS2 coat protein. Nucleic Acids Res 21:4621-4626. http: //dx.doi.org/10.1093/nar/21.19.4621.
22. Johnson KN, Tang L, Johnson JE, Ball LA. 2004. Heterologous RNA encapsidated in Pariacoto virus-like particles forms a dodecahedral cage similar to genomic RNA in wild-type virions. J Virol 78:11371-11378. http://dx.doi.org/10.1128/JVI.78.20.11371-11378.2004.
23. Routh A, Domitrovic T, Johnson JE. 2012. Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus. Proc Natl Acad Sci U S A 109:1907-1912. http://dx.doi.org/10.1073/pnas .1116168109.
24. Suluja E, Strokowskaja L, Zagorski-Ostoja W, Palucha A. 2005. Viruslike particles of potato leafroll virus as potential carrier system for nucleic acids. Acta Biochim Pol 52:699-702.
25. Annamalai P, Rao AL. 2005. Replication-independent expression of genome components and capsid protein of brome mosaic virus in planta: a functional role for viral replicase inRNApackaging. Virology 338:96-111. http://dx.doi.org/10.1016/j.virol.2005.05.013.
26. Siegel A. 1971. Pseudovirions of tobacco mosaic virus. Virology 46:50-59. http://dx.doi.org/10.1016/0042-6822(71)90005-5.
27. Rochon D, Lommel S, Martelli GP, Rubino L, Russo M. 2012. Tombusviridae, p 1111-1138. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, CA.
28. Rochon DM, Tremaine JH. 1988. Cucumber necrosis virus is a member of the tombusvirus group. J Gen Virol 69:395-400. http://dx.doi.org/10 .1099/0022-1317-69-2-395.
29. Rochon DM, Tremaine JH. 1989. Complete nucleotide sequence of the cucumber necrosis virus genome. Virology 169:251-259. http://dx.doi .org/10.1016/0042-6822(89)90150-5.
30. Rochon DM, Johnston JC. 1991. Infectious transcripts from cloned cucumber necrosis virus cDNA: evidence for a bifunctional subgenomic mRNA. Virology 181:656-665. http://dx.doi.org/10.1016/0042-6822(91)90899-M.
31. Johnston JC, Rochon DM. 1990. Translation of cucumber necrosis virus RNA in vitro. J Gen Virol 71(Pt 10):2233-2241. http://dx.doi.org/10.1099 /0022-1317-71-10-2233.
32. Sit TL, Johnston JC, ter Borg MG, Frison E, McLean MA, Rochon D. 1995. Mutational analysis of the cucumber necrosis virus coat protein gene. Virology 206:38-48. http://dx.doi.org/10.1016/S0042-6822(95)80017-4.
33. Johnston JC, Rochon DM. 1996. Both codon context and leader length contribute to efficient expression of two overlapping open reading frames of a cucumber necrosis virus bifunctional subgenomic mRNA. Virology 221:232-239. http://dx.doi.org/10.1006/viro.1996.0370.
34. Li M, Kakani K, Katpally U, Johnson S, Rochon D, Smith TJ. 2013. Atomic structure of cucumber necrosis virus and the role of the capsid in vector transmission. J Virol 87:12166-12175. http://dx.doi.org/10.1128 /JVI.01965-13.
35. Katpally U, Kakani K, Reade R, Dryden K, Rochon D, Smith TJ. 2007. Structures of T=1 and T=3 particles of cucumber necrosis virus: evidence of internal scaffolding. J Mol Biol 365:502-512. http://dx.doi.org/10.1016 /j.jmb.2006.09.060.
36. Kakani K, Reade R, Katpally U, Smith T, Rochon D. 2008. Induction of particle polymorphism by cucumber necrosis virus coat protein mutants in vivo. J Virol 82:1547-1557. http://dx.doi.org/10.1128/JVI.01976-07.
37. Reade R, Kakani K, Rochon D. 2010. A highly basic KGKKGK sequence in the RNA-binding domain of the cucumber necrosis virus coat protein is associated with encapsidation of full-length CNV RNA during infection. Virology 403:181-188. http://dx.doi.org/10.1016/j.virol.2010.03.045.
38. Xiang Y, Kakani K, Reade R, Hui E, Rochon D. 2006. A 38-amino-acid sequence encompassing the arm domain of the cucumber necrosis virus coat protein functions as a chloroplast transit peptide in infected plants. J Virol 80:7952-7964. http://dx.doi.org/10.1128/JVI.00153-06.
39. Hui E, Xiang Y, Rochon D. 2010. Distinct regions at the N-terminus of the cucumber necrosis virus coat protein target chloroplasts and mitochondria. Virus Res 153:8-19. http://dx.doi.org/10.1016/j.virusres.2010 .06.021.
40. Ghoshal K, Theilmann J, Reade R, Sanfacon H, Rochon D. 2014. The cucumber leaf spot virus p25 auxiliary replicase protein binds and modifies the endoplasmic reticulum via N-terminal transmembrane domains. Virology 468-470:36-46. http://dx.doi.org/10.1016/j.virol.2014.07.020.
41. Voinnet O, Rivas S, Mestre P, Baulcombe D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949-956. http://dx .doi.org/10.1046/j.1365-313X.2003.01676.x.
42. Kakani K, Sgro JY, Rochon D. 2001. Identification of specific cucumber necrosis virus coat protein amino acids affecting fungus transmission and zoospore attachment. J Virol 75:5576-5583. http://dx.doi.org/10.1128 /JVI.75.12.5576-5583.2001.
43. Robbins MA, Reade RD, Rochon DM. 1997. A cucumber necrosis virus variant deficient in fungal transmissibility contains an altered coat protein shell domain. Virology 234:138-146. http://dx.doi.org/10.1006/viro.1997 .8635.
44. Hillman BI, Hearne P, Rochon D, Morris TJ. 1989. Organization of tomato bushy stunt virus genome: characterization of the coat protein gene and the 3= terminus. Virology 169:42-50. http://dx.doi.org/10.1016 /0042-6822(89)90039-1.
45. Yukawa M, Tsudzuki T, Sugiura M. 2005. The 2005 version of the chloroplast DNA sequence from tobacco (Nicotiana tabacum). Plant Mol Biol Rep 23:359-365. http://dx.doi.org/10.1007/BF02788884.
46. Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M. 2005. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272:603-615. http://dx.doi.org/10.1007/s00438-004-1075-8.
47. 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. http://dx.doi.org/10.1371/journal.pone.0059534.
48. Chaturvedi S, Rao AL. 2014. Live cell imaging of interactions between replicase and capsid protein of brome mosaic virus using bimolecular fluorescence complementation: implications for replication and genome packaging. Virology 464-465:67-75. http://dx.doi.org/10.1016 /j.virol.2014.06.030.
49. Rao AL, Chaturvedi S, Garmann RF. 2014. Integration of replication and assembly of infectious virions in plantRNAviruses. Curr Opin Virol 9:61-66 http://dx.doi.org/10.1016/j.coviro.2014.09.008.
50. Rochon D, Singh B, Reade R, Theilmann J, Ghoshal K, Alam SB, Maghodia A. 2014. The p33 auxiliary replicase protein of cucumber necrosis virus targets peroxisomes and infection induces de novo peroxisome formation from the endoplasmic reticulum. Virology 452-453:133-142 http://dx.doi.org/10.1016/j.virol.2013.12.035.
51. Domingues DS, Cruz GM, Metcalfe CJ, Nogueira FT, Vicentini R, Alves CDS, Van Sluys MA. 2012. Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns. BMC Genomics 13:137. http://dx.doi.org/10.1186/1471-2164-13-137.
52. Feschotte C, Jiang N, Wessler SR. 2002. Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329-341. http://dx.doi .org/10.1038/nrg793.
53. Suoniemi A, Tanskanen J, Schulman AH. 1998. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J 13:699-705. http://dx .doi.org/10.1046/j.1365-313X.1998.00071.x.
54. Ungerer MC, Strakosh SC, Stimpson KM. 2009. Proliferation of Ty3/ gypsy-like retrotransposons in hybrid sunflower taxa inferred from phylogenetic data.BMCBiol 7:40. http://dx.doi.org/10.1186/1741-7007-7-40.
55. Voytas DF, Cummings MP, Koniczny A, Ausubel FM, Rodermel SR. 1992 Copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad SciUSA89:7124-7128. http://dx.doi.org/10.1073/pnas.89.15.7124.
56. Beguiristain T, Grandbastien MA, Puigdomenech P, Casacuberta JM.2001 Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol 127:212-221.
57. Casacuberta JM, Vernhettes S, Audeon C, Grandbastien MA. 1997. Quasispecies in retrotransposons: a role for sequence variability in Tnt1 evolution. Genetica 100:109-117. http://dx.doi.org/10.1023/A:1018309007841.
58. Jones RB, Song H, Xu Y, Garrison KE, Buzdin AA, Anwar N, Hunter DV, Mujib S, Mihajlovic V, Martin E, Lee E, Kuciak M, Raposo RA, Bozorgzad A, Meiklejohn DA, Ndhlovu LC, Nixon DF, Ostrowski MA.2013 LINE-1 retrotransposable element DNA accumulates in HIV-1- infected cells. J Virol 87:13307-13320. http://dx.doi.org/10.1128/JVI .02257-13.
59. Takeda S, Sugimoto K, Otsuki H, Hirochika H. 1998. Transcriptional activation of the tobacco retrotransposon Tto1 by wounding and methyl jasmonate. Plant Mol Biol 36:365-376. http://dx.doi.org/10 .1023/A:1005911413528.
60. Diao X, Freeling M, Lisch D. 2006. Horizontal transfer of a plant transposon. PLoS Biol 4:e5. http://dx.doi.org/10.1371/journal.pbio.0040005.
61. El Baidouri M, Carpentier MC, Cooke R, Gao D, Lasserre E, Llauro C, Mirouze M, Picault N, Jackson SA, Panaud O. 2014. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24:831-838. http://dx.doi.org/10.1101/gr.164400.113.
62. Reade R, Delroux K, Macdonald K, Sit TL, Lommel SA, Rochon D.2001 Spontaneous deletion enhances movement of a cucumber necrosis virus based chimera expressing the red clover necrotic mosaic virus movement protein gene. Mol Plant Pathol 2:13-25. http://dx.doi.org/10.1046/j .1364-3703.2001.00045.x.