1887

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Volume 85, Issue 10

Expression of tombusvirus open reading frames 1 and 2 is sufficient for the replication of defective interfering, but not satellite, RNA Free

Abstract

Yeast cells co-expressing the replication proteins p36 and p95 of (CIRV) support the RNA-dependent replication of several defective interfering (DI) RNAs derived from either the genome of CIRV or the related (CymRSV), but not the replication of a satellite RNA (sat RNA) originally associated with CymRSV. DI, but not sat RNA, was replicated in yeast cells co-expressing both DI and sat RNA. Using transgenic plants constitutively expressing CymRSV replicase proteins (p33 and p92), or transiently expressing either these proteins or CIRV p36 and p95, it was shown that expression of replicase proteins alone was also not sufficient for the replication of sat RNA in plant cells. However, it was also shown that replicating CIRV genomic RNA deletion mutants encoding only replicase proteins could sustain replication of sat RNA in plant cells. These results suggest that sat RNA has a replication strategy differing from that of genomic and DI RNAs, for it requires the presence of a -replicating genome acting as a -replication enhancer.

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2004-10-01
2024-05-06
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References

  1. Albariño C. G., Price B. D., Eckerle L. D., Ball L. A. 2001; Characterization and template properties of RNA dimers generated during Flock house virus RNA replication. Virology 289:269–282 [CrossRef]
     [Google Scholar]
  2. Berben G., Dumont J., Gilliquet V., Bolle P. A., Hilger F. 1991; The YDp plasmids: a uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae . Yeast 7:475–477 [CrossRef]
     [Google Scholar]
  3. Burgyan J., Russo M. 1988; Studies on the replication of a satellite RNA associated with cymbidium ringspot virus. J Gen Virol 69:3089–3092 [CrossRef]
     [Google Scholar]
  4. Burgyan J., Rubino L., Russo M. 1991; De novo generation of cymbidium ringspot virus defective interfering RNA. J Gen Virol 72:505–509 [CrossRef]
     [Google Scholar]
  5. Burgyan P., Dalmay T., Rubino L., Russo M. 1992; The replication of cymbidium ringspot tombusvirus defective interfering-satellite RNA hybrid molecules. Virology 190:579–586 [CrossRef]
     [Google Scholar]
  6. Burgyan J., Rubino L., Russo M. 1996; The 5′-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. J Gen Virol 77:1967–1974 [CrossRef]
     [Google Scholar]
  7. Carrington J. C., Freed D. D., Oh C. S. 1990; Expression of potyviral polyproteins in transgenic plants reveals three proteolytic activities required for complete processing. EMBO J 9:1347–1353
     [Google Scholar]
  8. Celix A., Rodriguez-Cerezo E., Garcia-Arenal F. 1997; New satellite RNAs, but no DI RNAs, are found in natural populations of tomato bushy stunt tombusvirus. Virology 239:277–284 [CrossRef]
     [Google Scholar]
  9. Celix A., Burgyan J., Rodriguez-Cerezo E. 1999; Interactions between tombusviruses and satellite RNAs of tomato bushy stunt virus: a defect in sat RNA B1 replication maps to ORF1 of a helper virus. Virology 262:129–138 [CrossRef]
     [Google Scholar]
  10. Chang Y. C., Borja M., Scholthof H. B., Jackson A. O., Morris T. J. 1995; Host effects and sequences essential for accumulation of defective interfering RNAs of cucumber necrosis and tomato bushy stunt tombusviruses. Virology 210:41–53 [CrossRef]
     [Google Scholar]
  11. Chen J., Noueiry A., Ahlquist P. 2001; Brome mosaic virus protein 1a recruits viral RNA2 to RNA replication through a 5′ proximal RNA2 signal. J Virol 75:3207–3219 [CrossRef]
     [Google Scholar]
  12. Dalmay T., Rubino L. 1994; The nature of multimeric forms of cymbidium ringspot tombusvirus satellite RNA. Arch Virol 138:161–167 [CrossRef]
     [Google Scholar]
  13. Dalmay T., Rubino L. 1995; Replication of cymbidium ringspot virus satellite RNA mutants. Virology 206:1092–1098 [CrossRef]
     [Google Scholar]
  14. Dalmay T., Rubino L., Burgyan J., Kollar A., Russo M. 1993a; Functional analysis of cymbidium ringspot virus genome. Virology 194:697–704 [CrossRef]
     [Google Scholar]
  15. Dalmay T., Russo M., Burgyan J. 1993b; Repair in vivo of altered 3′ terminus of cymbidium ringspot tombusvirus RNA. Virology 192:551–555 [CrossRef]
     [Google Scholar]
  16. Dalmay T., Szittya G., Burgyan J. 1995; Generation of defective interfering RNA dimers of cymbidium ringspot tombusvirus. Virology 207:510–517 [CrossRef]
     [Google Scholar]
  17. Eckerle L. D., Ball L. A. 2002; Replication of the RNA segments of a bipartite viral genome is coordinated by a transactivating subgenomic RNA. Virology 296:165–176 [CrossRef]
     [Google Scholar]
  18. Eckerle L. D., Albarino C. G., Ball L. A. 2003; Flock house virus subgenomic RNA3 is replicated and its replication correlates with transactivation of RNA2. Virology 317:95–108 [CrossRef]
     [Google Scholar]
  19. Fabian M. R., Na H., Ray D., White K. A. 2003; 3′-Terminal RNA secondary structures are important for accumulation of tomato bushy stunt virus DI RNAs. Virology 313:567–580 [CrossRef]
     [Google Scholar]
  20. Finnen R. L., Rochon D. M. 1995; Characterization and biological activity of DI RNA dimers formed during cucumber necrosis virus coinfections. Virology 207:282–286 [CrossRef]
     [Google Scholar]
  21. Havelda Z., Burgyan J. 1995; 3′ Terminal putative stem–loop structure required for the accumulation of cymbidium ringspot viral RNA. Virology 214:269–272 [CrossRef]
     [Google Scholar]
  22. Havelda Z., Dalmay T., Burgyan J. 1995; Localization of cis -acting sequences essential for cymbidium ringspot tombusvirus defective interfering RNA replication. J Gen Virol 76:2311–2316 [CrossRef]
     [Google Scholar]
  23. Havelda Z., Szittya G., Burgyan J. 1998; Characterization of the molecular mechanism of defective interfering RNA-mediated symptom attenuation in tombusvirus-infected plants. J Virol 72:6251–6256
     [Google Scholar]
  24. Ishikawa M., Janda M., Krol M. A., Ahlquist P. 1997; In vivo DNA expression of functional brome mosaic virus RNA replicons in Saccharomyces cerevisiae . J Virol 71:7781–7790
     [Google Scholar]
  25. Kollar A., Burgyan J. 1994; Evidence that ORF 1 and 2 are the only virus-encoded replicase genes of cymbidium ringspot tombusvirus. Virology 201:169–172 [CrossRef]
     [Google Scholar]
  26. Lupo R., Rubino L., Russo M. 1994; Immunodetection of the 33K/92K polymerase proteins in cymbidium ringspot-infected and in transgenic plant tissue extracts. Arch Virol 138:135–142 [CrossRef]
     [Google Scholar]
  27. Nagy P. D., Pogany J. 2000; Partial purification and characterization of Cucumber necrosis virus and Tomato bushy stunt virus RNA-dependent RNA polymerases: similarities and differences in template usage between tombusvirus and carmovirus RNA-dependent RNA polymerases. Virology 276:279–288 [CrossRef]
     [Google Scholar]
  28. Oh C. S., Carrington J. C. 1989; Identification of essential residues in potyvirus proteinase HC-Pro by site-directed mutagenesis. Virology 173:692–699 [CrossRef]
     [Google Scholar]
  29. 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 [CrossRef]
     [Google Scholar]
  30. Panavas T., Pogany J., Nagy P. D. 2002a; Analysis of minimal promoter sequences for plus-strand synthesis by the Cucumber necrosis virus RNA-dependent RNA polymerase. Virology 296:263–274 [CrossRef]
     [Google Scholar]
  31. Panavas T., Pogany J., Nagy P. D. 2002b; Internal initiation by the Cucumber necrosis virus RNA-dependent RNA polymerase is facilitated by promoter-like sequences. Virology 296:275–287 [CrossRef]
     [Google Scholar]
  32. Pantaleo V., Rubino L., Russo M. 2003; Replication of Carnation Italian ringspot virus defective interfering RNA in Saccharomyces cerevisiae . J Virol 77:2116–2123 [CrossRef]
     [Google Scholar]
  33. Pantaleo V., Rubino L., Russo M. 2004; The p36 and p95 replicase proteins of Carnation Italian ringspot virus cooperate in stabilizing defective interfering RNA. J Gen Virol 85:2429–2433 [CrossRef]
     [Google Scholar]
  34. Ray D., White K. A. 1999; Enhancer-like properties of an RNA element that modulates Tombusvirus RNA accumulation. Virology 256:162–171 [CrossRef]
     [Google Scholar]
  35. Ray D., White K. A. 2003; An internally located RNA hairpin enhances replication of tomato bushy stunt virus RNAs. J Virol 77:245–257 [CrossRef]
     [Google Scholar]
  36. Rubino L., Russo M. 1995; Characterization of resistance to cymbidium ringspot virus in transgenic plants expressing a full-length viral replicase gene. Virology 212:240–243 [CrossRef]
     [Google Scholar]
  37. Rubino L., Burgyan J., Grieco F., Russo M. 1990; Sequence analysis of cymbidium ringspot virus satellite and defective interfering RNAs. J Gen Virol 71:1655–1660 [CrossRef]
     [Google Scholar]
  38. Rubino L., Carrington J. C., Russo M. 1992; Biologically active cymbidium ringspot virus satellite RNA in transgenic plants suppresses accumulation of DI RNAs. Virology 188:429–437 [CrossRef]
     [Google Scholar]
  39. Rubino L., Lupo R., Russo M. 1993; Resistance to cymbidium ringspot tombusvirus infection in transgenic Nicotiana benthamiana plants expressing a full-length viral replicase gene. Mol Plant Microbe Interact 6:729–734 [CrossRef]
     [Google Scholar]
  40. Rubino L., Burgyan J., Russo M. 1995; Molecular cloning and complete nucleotide sequence of carnation Italian ringspot tombusvirus genomic and defective interfering RNAs. Arch Virol 140:2027–2039 [CrossRef]
     [Google Scholar]
  41. Rubino L., Di Franco A., Russo M. 2000; Expression of a plant virus non-structural protein in Saccharomyces cerevisiae causes membrane proliferation and altered mitochondrial morphology. J Gen Virol 81:279–286
     [Google Scholar]
  42. Rubino L., Weber-Lotfi F., Dietrich A., Stussi-Garaud C., Russo M. 2001; The open reading frame 1-encoded (‘36K’) protein of Carnation Italian ringspot virus localizes to mitochondria. J Gen Virol 82:29–34
     [Google Scholar]
  43. Russo M., Burgyan J., Martelli G. P. 1994; Molecular biology of Tombusviridae . Adv Virus Res 44:381–428
     [Google Scholar]
  44. Silhavy D., Molnar A., Lucioli A., Szittya G., Hornyik C., Tavazza M., Burgyan J. 2002; A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21:3070–3080 [CrossRef]
     [Google Scholar]
  45. Sit T. L., Vaewhongs A. A., Lommel S. A. 1998; RNA-mediated transactivation of transcription from a viral RNA. Science 281:829–832 [CrossRef]
     [Google Scholar]
  46. Töpfer R., Matzeit V., Gronenborn B., Schell J., Steinbiss H. H. 1987; A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res 15:5890 [CrossRef]
     [Google Scholar]
  47. 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 [CrossRef]
     [Google Scholar]
  48. Wu B., White K. A. 1998; Formation and amplification of a novel tombusvirus defective RNA which lacks the 5′ nontranslated region of the viral genome. J Virol 72:9897–9905
     [Google Scholar]
  49. Wu B., Vanti W. B., White K. A. 2001; An RNA domain within the 5′ untranslated region of the tomato bushy stunt virus genome modulates viral RNA replication. J Mol Biol 305:741–756 [CrossRef]
     [Google Scholar]
  50. Zhang G., Slowinski V., White K. A. 1999; Subgenomic mRNA regulation by a distal RNA element in a (+)-strand RNA virus. RNA 5:550–561 [CrossRef]
     [Google Scholar]
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Expression of tombusvirus open reading frames 1 and 2 is sufficient for the replication of defective interfering, but not satellite, RNA
J. Gen. Virol. 85, 3115 (2004); https://doi.org/10.1099/vir.0.80296-0
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