Evidence that the linker between the methyltransferase and helicase domains of potato virus X replicase is involved in homologous RNA recombination

Journal of Virology

Volumn 83, Issue 15, 2009, Pages 7761-7769

  Draghici, Heidrun Katharina ^a   Varrelmann, Mark ^a,b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Institute of Sugar Beet Research   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; GREEN FLUORESCENT PROTEIN; HELICASE; METHYLTRANSFERASE;

ARTICLE; DNA SEQUENCE; GENE DELETION; GENE INSERTION; GENE MUTATION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; MOLECULAR CLONING; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; POTEXVIRUS; PRIORITY JOURNAL; RHIZOBIUM RADIOBACTER; RNA RECOMBINATION; RNA VIRUS; TOBACCO; VIRUS ISOLATION; VIRUS REPLICATION;

POTEXVIRUS; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; RNA REPLICASE; TOBACCO; VIRAL PROTEINS;

AGROBACTERIUM TUMEFACIENS; NICOTIANA BENTHAMIANA; POTATO VIRUS X; RNA VIRUSES;

EID: 67650882552     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00179-08     Document Type: Article

References (98)

1. Aaziz, R., and M. Tepfer. 1999. Recombination in RNA viruses and in virus-resistant transgenic plants. J. Gen. Virol. 80:1339-1346.
2. Aaziz, R., and M. Tepfer. 1999. Recombination between genomic RNAs of two cucumoviruses under condition of minimal selection pressure. Virology 263:282-289.
3. Adair, T. L., and C. M. Kearney. 2000. Recombination between a 3-kilobase tobacco mosaic virus transgene and a homologous viral construct in the restoration of viral and nonviral genes. Arch. Virol. 145:1867-1883.
4. Adams, M. J., J. F. Antoniw, M. Bar-Joseph, A. A. Brunt, T. Candresse, G. D. Foster, G. P. Martelli, R. G. Milne, and C. M. Fauquet. 2004. The new plant virus family Flexiviridae and assessment of molecular criteria for species demarcation. Arch. Virol. 149:1045-1060.
5. Alejska, M., A. Kurzynska-Kokornika, M. Broda, R. Kierzek, and M. Figlerowicz. 2001. How RNA viruses exchange their genetic material. Acta Biochim. Pol. 48:391-407.
6. Alejska, M., M. Figlerowicz, N. Malinowska, A. Urbanowicz, and M. Figlerowicz. 2005. A universal BMV-based RNA recombination system-how to search for general rules in RNA recombination. Nucleic Acids Res. 33:1-14.
7. Allison, R. F., G. Thompson, and P. Ahlquist. 1990. Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proc. Natl. Acad. Sci. USA 87:1820-1824.
8. Allison, R. F., W. L. Schneider, and A. E. Greene. 1996. Recombination in plants expressing viral transgenes. Semin. Virol. 7:417-422.
9. Arnold, J. J., and C. E. Cameron. 1999. Poliovirus RNA-dependent RNA polymerase (3Dpol) is sufficient for template switching in vitro. J. Biol. Chem. 274:2706-2716.
10. Banner, L. R., J. G. Keck, and M. M. C. Lai. 1990. A clustering of RNA recombination sites adjacent to hyper-variable region of the peplomer gene of murine coronavirus. J. Virol. 175:548-555.
11. Barajas, D., F. Tenllado, and J. R. Diaz-Ruiz. 2006. Characterization of the recombinant forms arising from a potato virus X chimeric virus infection under RNA silencing pressure. Mol. Plant-Microbe Interact. 19:904-913.
12. Baulcombe, D. C., S. Chapman, and S. Santa Cruz. 1995. Jellyfish green fluorescent protein as a reporter for virus infections. Plant J. 7:1045-1053.
13. Beck, D. L., and W. O. Dawson. 1990. Deletion of repeated sequences from tobacco mosaic virus mutants with two coat protein genes. Virology 177:462-469.
14. Borja, M., T. Rubio, H. B. Scholthof, and A. O. Jackson. 1999. Restoration of wild-type virus by double recombination of tombusvirus mutants with a host transgene. Mol. Plant-Microbe Interact. 12:153-162.
15. Brown, D., and L. Gold. 1996. RNA replication by Q.β replicase: a working model. Proc. Natl. Acad. Sci. USA 93:11558-11562.
16. Bruyere, A., M. Wantroba, S. Flasinski, A. Dzianott, and J. J. Bujarski. 2000. Frequent homologous recombination events between molecules of one RNA component in a multipartite RNA virus. J. Virol. 74:4214-4219.
17. Bujarski, J. J., and P. Kaesberg. 1986. Genetic recombination between RNA components of a multipartite plant virus. Nature 321:528-531.
18. Canto, T., S. K. Choi, and P. Palukaitis. 2001. A subpopulation of RNA 1 of cucumber mosaic virus contains 3′ termini originating from RNAs 2 or 3. J. Gen. Virol. 82:941-945.
19. Cascone, P. J., T. F. Haydar, and A. E. Simon. 1993. Sequences and structures required for recombination between virus-associated RNAs. Science 260:801-805.
20. Chao, L. 1997. Evolution of sex and the molecular clock in RNA viruses. Gene 205:301-308.
21. Chapman, S., T. Kavanagh, and D. C. Baulcombe. 1992. Potato virus X as a vector for gene expression in plants. Plant J. 2:549-557.
22. Chare, E. R., and E. C. Holmes. 2006. A phylogenetic survey of recombination frequency in plant RNA viruses. Arch. Virol. 151:933-946.
23. Chetverin, A. B., H. V. Chetverina, A. A. Demidenko, and V. I. Ugarov. 1997. Nonhomologous RNA recombination in a celfree system: evidence for a transesterification mechanism guided by secondary structure. Cell 88:503-513.
24. Chetverina, H. V., A. A. Demidenko, V. I. Ugarov, and A. B. Chetverin. 1999. Spontaneous rearrangements in RNA sequences. FEBS Lett. 450:89-94.
25. Chung, B. N., T. Canto, and P. Palukaitis. 2007. Stability of recombinant plant viruses containing genes of unrelated plant viruses. J. Gen. Virol. 88:1347-1355.
26. Crotty, S., C. E. Cameron, and R. Andino. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. USA 98:6895-6900.
27. Denison, M. R. 2008. Seeking membranes: positive-strand RNA virus replication complexes. PLoS Biol. 6:e270.
28. de Wispelaere, M., S. Gaubert, S. Trouilloud, C. Belin, and M. Tepfer. 2005. A map of the diversity of RNA3 recombinants appearing in plants infected with Cucumber mosaic virus and Tomato aspermy virus. Virology 331:117-127.
29. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
30. Domingo, E., C. Escarmis, L. Menéndez-Arias, and J. J. Holland. 1999. Viral quasi-species and fitness variations, p. 141-161. In E. Domingo, R. G. Webster, and J. J. Holland (ed.), Origin and evolution of viruses. Academic Press, Inc., San Diego, CA.
31. Domingo, E., E. Baranowski, C. Escarmis, F. Sobrino, and J. J. Holland. 2002. Error frequencies of picornavirus RNA polymerases: evolutionary implications for virus populations, p. 285-298. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
32. Draghici, H.-K., R. Pilot, H. Thiel, and M. Varrelmann. 2009. Functional mapping of PVX RNA-dependent RNA-replicase using pentapeptide scanning mutagenesis: identification of regions indispensable for replication and subgenomic RNA amplification. Virus Res. 143:114-124.
33. Duggal, R., and E. Wimmer. 1999. Genetic recombination of poliovirus in vitro and in vivo: temperature-dependent alteration of crossover sites. Virology 258:30-41.
34. Dzianott, A., N. Rauffer-Bruyere, and J. J. Bujarski. 2001. Studies on functional interaction between brome mosaic virus replicase proteins during RNA recombination, using combined mutants in vivo and in vitro. Virology 289:137-149.
35. Fernández-Cuartero, B., J. Burgyán, M. A. Aranda, K. Salánki, E. Moriones, and F. García-Arenal. 1994. Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203:373-377.
36. Figlerowicz, M., P. D. Nagy, and J. J. Bujarski. 1997. A mutation in the putative RNA polymerase gene inhibits nonhomologous, but not homologous, genetic recombination in an RNA virus. Proc. Natl. Acad. Sci. USA 94:2073-2078.
37. Figlerowicz, M., P. D. Nagy, N. Tang, C. C. Kao, and J. J. Bujarski. 1998. Mutations in the N terminus of the brome mosaic virus polymerase affect genetic RNA-RNA recombination. J. Virol. 72:9192-9200.
38. Figlerowicz, M., and J. J. Bujarski. 1998. RNA recombination in brome mosaic virus, a model plus-stranded RNA virus. Acta Biochim. Pol. 45:1-23.
39. Fu, K., and R. S. Baric. 1992. Evidence for variable rates of recombination in the MHV genome. Virology 189:88-102.
40. Gal, S., B. Pisan, T. Hohn, N. Grimsley, and B. Hohn. 1992. Agroinfection of transgenic plants leads to viable cauliflower mosaic virus by intermolecular recombination. Virology 187:525-533.
41. Gallei, A., A. Pankraz, H. J. Thiel, and P. Becher. 2004. RNA recombination in vivo in the absence of viral replication. J. Virol. 78:6271-6281.
42. GaOn, A., E. Meiri, B. Raccah, and V. Gaba. 1998. Recombination of engineered defective RNA species produces infective potyvirus in planta. J. Virol. 72:5268-5270.
43. García-Arenal, F., A. Fraile, and J. M. Malpica. 2001. Variability and genetic structure of plant virus populations. Annu. Rev. Phytopathol. 39:157-186.
44. García-Arenal, F., A. Fraile, and J. M. Malpica. 2003. Variation and evolution of plant virus populations. Int. Microbiol. 6:225-232.
45. Gmyl, A. P., E. V. Belousov, S. V. Maslova, E. V. Khitrina, A. B. Chetverin, and V. I. Agol. 1999. Nonreplicative RNA recombination in poliovirus. J. Virol. 73:8958-8965.
46. Gmyl, A. P., S. A. Korshenko, E. V. Belousov, E. V. Khitrina, and V. I. Agol. 2003. Nonreplicative homologous RNA recombination: promiscuous joining of RNA pieces? RNA 9:1221-1223.
47. Gmyl, A. P., and V. I. Agol. 2005. Diverse mechanisms of RNA recombination. Mol. Biol. 39:529-542.
48. Goldbach, R., and P. de Haan. 1994. RNA viral supergroups and the evolution of RNA viruses, p. 105-119. In S. Morse (ed.), The evolutionary biology of viruses. Raven Press, New York, NY.
49. Greene, A. E., and R. F. Allison. 1994. Recombination between viral RNA and transgenic plant transcripts. Science 263:1423-1425.
50. Greene, A. E., and R. F. Allison. 1996. Deletions in the 3′ untranslated region of cowpea chlorotic mottle virus transgene reduce recovery of recombinant viruses in transgenic plants. Virology 225:231-234.
51. Gray, D. J., E. Hiebert, C. M. Lin, M. E. Compton, D. W. McColley, R. J. Harrison, and V. P. Gaba. 1994. Simplified construction and performance of a device for particle bombardment. Plant Cell Tissue Organ Culture 37:179-184.
52. Habili, N., and R. H. Symons. 1989. Evolutionary relationship between luteoviruses and other RNA plant viruses based on sequence motifs in their putative RNA polymerases and nucleic acid helicases. Nucleic Acids Res. 17:9543-9555.
53. Han, Y. T., C. S. Tsai, Y. C. Chen, M. K. Lin, Y. H. Hsu, and M. Meng. 2007. Mutational analysis of a helicase motif-based RNA 5′-triphosphatase/NTPase from bamboo mosaic virus. Virology 367:41-50.
54. Hellens, R. P., E. A. Edwards, N. R. Leyland, S. Bean, and P. M. Mullineaux. 2000. pGreen: a versatile and flexible binary Ti vector for agrobacteriummediated plant transformation. Plant Mol. Biol. 42:819-832.
55. Hoekema, A., P. R. Hirsch, P. J. J. Hooykaas, and R. A. Schilperoort. 1983. A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179-180.
56. Huisman, M. J., B. J. C. Cornelissen, C. F. M. Groenendijk, J. F. Bol, and L. van Vloten-Doting. 1989. Alfalfa mosaic virus temperature-sensitive mutants. V. The nucleotide sequence of TBS 7 RNA 3 shows limited nucleotide changes and evidence for heterologous recombination. Virology 171:409-416.
57. Jakab, G., F. E. Vaistij, E. Droz, and P. Malnoë. 1997. Transgenic plants expressing viral sequences create a favourable environment for recombination between viral sequences, p. 45-51. In M. Tepfer and E. Balázs (ed.), Virus-resistant transgenic plants: potential ecological impact. Springer-Verlag, Heidelberg, Germany.
58. Jarvis, T. C., and K. Kirkegaard. 1992. Poliovirus RNA recombination: mechanistic studies in the absence of selection. EMBO J. 11:3135-3145.
59. Jones, L., A. J. Hamilton, O. Voinnet, C. L. Thomas, A. J. Maule, and D. C. Baulcombe. 1999. RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11:2291-2301.
60. Kagiwada, S., Y. Yamaji, H. Nakabayashi, M. Ugaki, and S. Namba. 2002. The complete nucleotide sequence of Potato virus X strain OS: the first complete sequence of a Japanese isolate. J. Gen. Plant Pathol. 68:94-98.
61. Kirkegaard, K., and D. Baltimore. 1986. The mechanism of RNA recombination in poliovirus. Cell 47:433-443.
62. Kim, M. J., and C. Kao. 2001. Factors regulating template switch in vitro by viral RNA-dependent RNA polymerases: implications for RNA-RNA recombination. Proc. Natl. Acad. Sci. USA 98:4972-4977.
63. Kong, F., K. Sivakumaran, and C. Kao. 1999. The N-terminal half of the brome mosaic virus 1a protein has RNA capping-associated activities: specificity for GTP and S-adenosylmethionine. Virology 1:200-210.
64. Koonin, E. V., and V. V. Dolja. 1993. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. Biol. 28:375-430.
65. Kopek, B. G., G. Perkins, D. J. Miller, M. H. Ellisman, and P. Ahlquist. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5:e220.
66. Li, Y. I., Y. M. Cheng, Y. L. Huang, C. H. Tsai, Y. H. Hsu, and M. Meng. 1998. Identification and characterization of the Escherichia coli-expressed RNA-dependent RNA polymerase of bamboo mosaic virus. J. Virol. 72:10093-10099.
67. Li, Y. I., Y. J. Chen, Y. H. Hsu, and M. Meng. 2001. Characterization of the AdoMet-dependent guanylyltransferase activity that is associated with the N terminus of bamboo mosaic virus replicase. J. Virol. 75:782-788.
68. Li, Y. I., T. W. Shih, Y. H. Hsu, Y. T. Han, Y. L. Huang, and M. Meng. 2001. The helicase-like domain of plant Potexvirus replicase participates in formation of RNA 5′ cap structure by exhibiting RNA 5′-triphosphatase activity. J. Virol. 75:12114-12120.
69. Lommel, A., and Z. Xiong. 1991. Reconstitution of a functional red clover necrotic mosaic virus by recombinational rescue of the celto-cell movement gene expressed in a transgenic plant. J. Cell. Biochem. 15A(Suppl.):151.
70. Lu, R., I. Malcuit, P. Moffett, M. T. Ruiz, J. Peart, A. J. Wu, J. P. Rathjen, A. Bendahmane, L. Day, and D. C. Baulcombe. 2003. High throughput virus induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 22:5690-5699.
71. Masuta, C., S. Ueda, M. Suzuki, and I. Uyeda. 1998. Evolution of a quadripartite hybrid virus by interspecific exchange and recombination between replicase components of two related tripartite RNA viruses. Proc. Natl. Acad. Sci. USA 95:10487-10492.
72. Miller, E. D., C. A. Plante, K. H. Kim, J. W. Brown, and C. Hemenway. 1998. Stem-loop structure in the 59 region of potato virus X genome required for plus-strand RNA accumulation. J. Mol. Biol. 284:591-608.
73. Nagy, P. D., and J. J. Bujarski. 1993. Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences. Proc. Natl. Acad. Sci. USA 90:6390-6394.
74. Nagy, P. D., and J. J. Bujarski. 1995. Efficient system of homologous RNA recombination in brome mosaic virus: sequence and structure requirements and accuracy of crossovers. J. Virol. 69:131-140.
75. Nagy, P. D., and J. J. Bujarski. 1997. Engineering of homologous recombination hotspots with AU-rich sequences in brome mosaic virus. J. Virol. 71:3799-3810.
76. Nagy, P. D., and A. E. Simon. 1997. New insights into the mechanisms of RNA recombination. Virology 235:1-9.
77. Nagy, P. D., and A. E. Simon. 1998. In vitro characterization of late steps of RNA recombination in turnip crinkle virus.I. Role of the motif1-hairpin structure. Virology 249:379-392.
78. Nagy, P. D., A. Dzianott, P. Ahlquist, and J. J. Bujarski. 1995. Mutations in the helicase-like domain of protein 1a alter the sites of RNA-RNA recombination in Brome mosaic virus. J. Virol. 69:2547-2556.
79. Nagy, P. D., C. Zhang, and A. E. Simon. 1998. Dissecting RNA recombination in vitro: role of RNA sequences and the viral replicase. EMBO J. 17:2392-2403.
80. Olsthoorn, R. C. L., A. Bruyére, A. Dzianott, and J. J. Bujarski. 2002. RNA recombination in brome mosaic virus: effects of strand-specific stem-loop inserts. J. Virol. 76:12654-12662.
81. Panavas, T., and P. D. Nagy. 2003. Yeast as a model host to study replication and recombination of defective interfering RNA of tomato bushy stunt virus. Virology 314:315-325.
82. Panaviene, Z., and P. D. Nagy. 2003. Mutations in the RNA-binding domains of tombusvirus replicase proteins affect RNA recombination in vivo. Virology 317:359-372.
83. Prasher, D. C., V. K. Eckenrode, W. W. Ward, F. G. Prendergast, and M. J. Cormier. 1992. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111:229-233.
84. Puchta, H. 2005. The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J. Exp. Bot. 56:1-14.
85. Roossinck, M. J. 1997. Mechanisms of plant virus evolution. Annu. Rev. Phytopathol. 35:191-209.
86. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
87. Santa Cruz, S., and D. C. Baulcombe. 1995. Analysis of potato virus X coat protein genes in relation to resistance conferred by the genes Nx, Nb, and Rx1 of potato. J. Gen. Virol. 76:2057-2061.
88. Silhavy, D., A. Molnar, A. Lucioli, G. Szittya, C. Hornyik, M. Tavazza, and J. Burgyán. 2002. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 21:3070-3080.
89. Shapka, N., and P. D. Nagy. 2004. The AU-rich RNA recombination hot spot sequence of brome mosaic virus is functional in tombusviruses: implications for the mechanism of RNA recombination. J. Virol. 78:2288-2300.
90. Sherpa, A. R., V. Hallan, P. Pathak, and A. A. Zaidi. 2007. Complete nucleotide sequence analysis of Cymbidium mosaic virus Indian isolate: further evidence for natural recombination among potexviruses. J. Biosci. 32:663-669.
91. Tzfira, T., J. Li, B. Lacroix, and V. Citovsky. 2004. Agrobacterium T-DNA integration: molecules and models. Trends Genet. 20:375-383.
92. Van der Heijden, M. W., and J. F. Bol. 2002. Composition of alphavirus-like replication complexes: involvement of virus and host encoded proteins. Arch. Virol. 147:875-898.
93. Van der Kuyl, A. C., L. Neeleman, and J. F. Bol. 1991. Complementation and recombination between alfalfa mosaic virus RNA3 mutants in tobacco plants. Virology 183:731-738.
94. Varrelmann, M., L. Palkovics, and E. Maiss. 2000. Transgenic or plant expression vector-mediated recombination of plum pox virus. J. Virol. 74:7462-7469.
95. Voinnet, O., C. Lederer, and D. C. Baulcombe. 2000. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103:157-167.
96. White, K. A., and T. J. Morris. 1994. Recombination between defective tombusvirus RNAs generates functional hybrid genomes. Proc. Natl. Acad. Sci. USA 91:3642-3646.
97. Yeh, T. Y., B. Y. Lin, Y. C. Chang, Y. H. Hsu, and N. S. Lin. 1999. A defective RNA dissociated with bamboo mosaic virus and the possible common mechanisms for RNA recombination in potexviruses. Virus Genes 18:121-128.
98. Zhang, C., P. J. Cascone, and A. E. Simon. 1991. Recombination between satellite and genomic RNAs of turnip crinkle virus. Virology 184:791-794.