Evidence for similarity-assisted recombination and predicted stem-loop structure determinant in potato virus X RNA recombination

Journal of General Virology

Volumn 91, Issue 2, 2010, Pages 552-562

  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; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; GENE SEQUENCE; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT LEAF; POTEXVIRUS; PRIORITY JOURNAL; RHIZOBIUM; RNA RECOMBINATION; RNA STRUCTURE; VIRAL GENETICS; VIRUS MUTANT; 3' UNTRANSLATED REGION; CHEMISTRY; CONFORMATION; GENETIC RECOMBINATION; GENETICS; INVERTED REPEAT; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; TOBACCO; VIROLOGY;

AGROBACTERIUM; NICOTIANA BENTHAMIANA; POTATO VIRUS X;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; INVERTED REPEAT SEQUENCES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; POTEXVIRUS; RECOMBINATION, GENETIC; RNA, VIRAL; SEQUENCE ALIGNMENT; TOBACCO;

EID: 76249098104     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.014712-0     Document Type: Article

References (72)

1. Aaziz, R. & Tepfer, M. (1999a). Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol 80, 1339-1346.
2. Aaziz, R. & Tepfer, M. (1999b). Recombination between genomic RNAs of two cucumoviruses under conditions of minimal selection pressure. Virology 263, 282-289.
3. Alejska, M., Figlerowicz, M., Malinowska, N., Urbanowicz, A. & Figlerowicz, M. (2005). A universal BMV-based RNA recombination system - how to search for general rules in RNA recombination. Nucleic Acids Res 33, e105.
4. Allison, R. F., Schneider, W. L. & Greene, A. E. (1996). Recombination in plants expressing viral transgenes. Semin Virol 7, 417-422.
5. Banner, L. R., Keck, J. G. & Lai, M. M. C. (1990). A clustering of RNA recombination sites adjacent to a hypervariable region of the peplomer gene of murine coronavirus. Virology 175, 548-555.
6. Batten, J. S., Yoshinari, S. & Hemenway, C. (2003). Potato virus X: a model system for virus replication, movement and gene expression. Mol Plant Pathol 4, 125-131.
7. Borja, M., Rubio, T., Scholthof, H. B. & Jackson, A. O. (1999). Restoration of wild-type virus by double recombination of tombus-virus mutants with a host transgene. Mol Plant Microbe Interact 12, 153-162.
8. Brown, D. & Gold, L. (1996). RNA replication by Qβ replicase: a working model. Proc Natl Acad Sci U S A 93, 11558-11562.
9. Bruyere, A., Wantroba, M., Flasinski, S., Dzianott, A. & Bujarski, J. J. (2000). Frequent homologous recombination events between molecules of one RNA component in a multipartite RNA virus. J Virol 74, 4214-4219.
10. Carpenter, C. D. & Simon, A. E. (1996). In vivo restoration of biologically active 3′ ends of virus-associated RNAs by nonhomologous RNA recombination and replacement of a terminal motif. J Virol 70, 478-486.
11. Carpenter, C. D., Oh, J. W., Zhang, C. & Simon, A. E. (1995). Involvement of a stem-loop structure in the location of junction sites in viral RNA recombination. J Mol Biol 245, 608-622.
12. Cascone, P. J., Haydar, T. F. & Simon, A. E. (1993). Sequences and structures required for recombination between virus-associated RNAs. Science 260, 801-805.
13. Chare, E. R. & Holmes, E. C. (2006). A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151, 933-946.
14. Chetverin, A. B., Chetverina, H. V., Demidenko, A. A. & Ugarov, V. I. (1997). Nonhomologous RNA recombination in a cell-free system: evidence for a transesterification mechanism guided by secondary structure. Cell 88, 503-513.
15. Chetverina, H. V., Demidenko, A. A., Ugarov, V. I. & Chetverin, A. B. (1999). Spontaneous rearrangements in RNA sequences. FEBS Lett 450, 89-94.
16. de Wispelaere, M., Gaubert, S., Trouilloud, S., Belin, C. & Tepfer, M. (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.
17. Domingo, E. & Holland, J. J. (1997). RNA virus mutations and fitness for survival. Annu Rev Microbiol 51, 151-178.
18. Domingo, E., Escarmis, C., Menéndez-Arias, L. & Holland, J. J. (1999). Viral quasi-species and fitness variations. In Origin and Evolution of Viruses, pp. 141-161. Edited by E. Domingo, R. G. Webster & J. J. Holland. San Diego, CA: Academic Press.
19. Domingo, E., Baranowski, E., Escarmis, C., Sobrino, F. & Holland, J. J. (2002). Error frequencies of picornavirus RNA polymerases: evolutionary implications for virus populations. In Molecular Biology of Picornaviruses, pp. 285-298. Edited by B. L. Semler & E. Wimmer. Washington, DC: American Society for Microbiology.
20. Draghici, H. K. & Varrelmann, M. (2009). Evidence that the linker between the methyltransferase and helicase domains of the potato virus X replicase is involved in homologous RNA recombination. J Virol 83, 7761-7769.
21. Draghici, H.-K., Pilot, R., Thiel, H. & Varrelmann, M. (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.
22. Dzianott, A., Rauffer-Bruyere, N. & Bujarski, J. J. (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.
23. Fernández-Cuartero, B., Burgyán, J., Aranda, M. A., Salánki, K., Moriones, E. & García-Arenal, F. (1994). Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203, 373-377.
24. Figlerowicz, M. (2000). Role of RNA structure in non-homologous recombination between genomic molecules of brome mosaic virus. Nucleic Acids Res 28, 1714-1723.
25. Figlerowicz, M. & Bujarski, J. J. (1998). RNA recombination in brome mosaic virus, a model plus stranded RNA virus. Acta Biochim Pol 45, 847-868.
26. Figlerowicz, M., Nagy, P. D. & Bujarski, J. J. (1997). A mutation in the putative RNA polymerase gene inhibits nonhomologous, but not homologous, genetic recombination in an RNA virus. Proc Natl Acad Sci U S A 94, 2073-2078.
27. Figlerowicz, M., Nagy, P. D., Tang, N., Kao, C. C. & Bujarski, J. J. (1998). Mutations in the N terminus of the brome mosaic virus polymerase affect genetic RNA-RNA recombination. J Virol 72, 9192-9200.
28. Fu, K. & Baric, R. S. (1992). Evidence for variable rates of recombination in the MHV genome. Virology 189, 88-102.
29. Gallei, A., Pankraz, A., Thiel, H. J. & Becher, P. (2004). RNA recombination in vivo in the absence of viral replication. J Virol 78, 6271-6281.
30. Gal-On, A., Meiri, E., Raccah, B. & Gaba, V. (1998). Recombination of engineered defective RNA species produces infective potyvirus in planta. J Virol 72, 5268-5270.
31. Gmyl, A. P. & Agol, V. I. (2005). Diverse mechanisms of RNA recombination. Mol Biol 39, 529-542.
32. Gmyl, A. P., Belousov, E. V., Maslova, S. V., Khitrina, E. V., Chetverin, A. B. & Agol, V. I. (1999). Nonreplicative RNA recombination in poliovirus. J Virol 73, 8958-8965.
33. Gmyl, A. P., Korshenko, S. A., Belousov, E. V., Khitrina, E. V. & Agol, V. I. (2003). Nonreplicative homologous RNA recombination: promiscuous joining of RNA pieces? RNA 9, 1221-1223.
34. Goldbach, R. & de Haan, P. (1994). RNA viral supergroups and the evolution of RNA viruses. In The Evolutionary Biology of Viruses, pp. 105-119. Edited by S. Morse. New York: Raven Press.
35. Habili, N. & Symons, R. H. (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.
36. Hajjou, M., Hill, K. R., Subramaniam, S. V., Hu, J. Y. & Raju, R. (1996). Nonhomologous RNA-RNA recombination events at the 3′ non-translated region of Sindbis virus genome: hot spots and utilization of nonviral sequences. J Virol 70, 5153-5164.
37. Hu, B., Pillai-Nair, N. & Hemenway, C. (2007). Long-distance RNA-RNA interactions between terminal elements and the same subset of internal elements on the potato virus X genome mediate minus- and plus-strand RNA synthesis. RNA 13, 267-280.
38. Jager, J. & Pata, J. D. (1999). Getting a grip: polymerases and their substrate complexes. Curr Opin Struct Biol 9, 21-28.
39. Jarvis, T. C. & Kirkegaard, K. (1992). Poliovirus RNA recombination: mechanistic studies in the absence of selection. EMBO J 11, 3135-3145.
40. Jones, L., Hamilton, A. J., Voinnet, O., Thomas, C. L., Maule, A. J. & Baulcombe, D. C. (1999). RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11, 2291-2301.
41. Kagiwada, S., Yamaji, Y., Nakabayashi, H., Ugaki, M. & Namba, S. (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.
42. Kirkegaard, K. & Baltimore, D. (1986). The mechanism of RNA recombination in poliovirus. Cell 47, 433-443.
43. Koonin, E. V. & Dolja, V. V. (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.
44. Lu, R., Malcuit, I.,Moffett, P., Ruiz,M. T., Peart, J.,Wu, A. J., Rathjen, J. P., Bendahmane, A., Day, L. & Baulcombe, D. C. (2003). High throughput virus induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22, 5690-5699.
45. Mathews, D. H., Sabina, J., Zuker, M. & Turner, D. H. (1999). Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288, 911-940.
46. Meier, M. & Truve, E. (2006). An attempt to identify recombinants between two sobemoviruses in doubly infected oat plants. Environ Biosafety Res 5, 47-56.
47. Nagy, P. D. & Bujarski, J. J. (1993). Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences. Proc Natl Acad Sci U S A 90, 6390-6394.
48. Nagy, P. D. & Bujarski, J. J. (1995). Efficient system of homologous RNA recombination in brome mosaic virus: sequence and structure requirements and accuracy of crossovers. J Virol 69, 131-140.
49. Nagy, P. D. & Simon, A. E. (1997). New insights into the mechanisms of RNA recombination. Virology 235, 1-9.
50. Nagy, P. D. & Simon, A. E. (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.
51. Nagy, P. D., Dzianott, A., Ahlquist, P. & Bujarski, J. J. (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.
52. Nagy, P. D., Zhang, C. & Simon, A. E. (1998). Dissecting RNA recombination in vitro: role of RNA sequences and the viral replicase. EMBO J 17, 2392-2403.
53. Nagy, P. D., Pogany, J. & Simon, A. E. (1999). RNA elements required for RNA recombination function as replication enhancers in vitro and in vivo in a plus-strand RNA virus. EMBO J 18, 5653-5665.
54. Olsthoorn, R. C. L., Bruyére, A., Dzianott, A. & Bujarski, J. J. (2002). RNA recombination in brome mosaic virus: effects of strand-specific stem-loop inserts. J Virol 76, 12654-12662.
55. Panavas, T. & Nagy, P. D. (2003). Yeast as a model host to study replication and recombination of defective interfering RNA of tomato bushy stunt virus. Virology 314, 315-325.
56. Panaviene, Z. & Nagy, P. D. (2003). Mutations in the RNA-binding domains of tombusvirus replicase proteins affect RNA recombinaion in vivo. Virology 317, 359-372.
57. Romanova, L. I., Blinov, V. M., Tolskaya, E. A., Viktorova, E. G., Kolesnikova, M. S., Gueseva, E. A. & Agol, V. I. (1986). The primary structure of crossover regions of intertypic poliovirus recombinants: a model of recombination between RNA genomes. Virology 155, 202-213.
58. Roossinck, M. J. (1997). Mechanisms of plant virus evolution. Annu Rev Phytopathol 35, 191-209.
59. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
60. Santa Cruz, S. & Baulcombe, D. C. (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.
61. Shapka, N. & Nagy, P. D. (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.
62. Silhavy, D., Molnar, A., Lucioli, A., Szittya, G., Hornyik, C., Tavazza, M. & Burgyán, J. (2002). A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21, 3070-3080.
63. Simon, A. E. & Bujarski, J. J. (1994). RNA-RNA recombination and evolution in virus-infected plants. Annu Rev Phytopathol 32, 337-362.
64. Suzuki, M., Hibi, T. & Masuta, C. (2003). RNA recombination between cucumoviruses: possible role of predicted stem-loop structures and an internal subgenomic promoter-like motif. Virology 306, 77-86.
65. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876-4882.
66. van der Heijden, M. W. & Bol, J. F. (2002). Composition of alphavirus-like replication complexes: involvement of virus and host encoded proteins. Arch Virol 147, 875-898.
67. Varrelmann, M., Palkovics, L. & Maiss, E. (2000). Transgenic or plant expression vector-mediated recombination of plum pox virus. J Virol 74, 7462-7469.
68. Verchot-Lubicz, J., Ye, C. M. & Bamunusinghe, D. (2007). Molecular biology of potexviruses: recent advances. J Gen Virol 88, 1643-1655.
69. White, K. A. & Morris, T. J. (1994). Recombination between defective tombusvirus RNAs generates functional hybrid genomes. Proc Natl Acad Sci U S A 91, 3642-3646.
70. Wierzchoslawski, R., Dzianott, A. & Bujarski, J. (2004). Dissecting the requirement for subgenomic promoter sequences by RNA recombination of brome mosaic virus in vivo: evidence for functional separation of transcription and recombination. J Virol 78, 8552-8564.
71. Zhang, C. X., Cascone, P. J. & Simon, A. E. (1991). Recombination between satellite and genomic RNAs of turnip crinkle virus. Virology 184, 791-794.
72. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406-3415.