Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1995 Oct;7(10):1625–1634. doi: 10.1105/tpc.7.10.1625

Symptom attenuation by a normally virulent satellite RNA of turnip crinkle virus is associated with the coat protein open reading frame.

Q Kong 1, J W Oh 1, A E Simon 1
PMCID: PMC161022  PMID: 9750054

Abstract

Many satellite RNAs (sat-RNAs) can attenuate or intensify the symptoms produced by their helper virus. Sat-RNA C, associated with turnip crinkle virus (TCV), was previously found to intensify the symptoms of TCV on all plants in which TCV produced visible symptoms. However, when the coat protein open reading frame (ORF) of TCV was precisely exchanged with that of cardamine chlorotic fleck virus, sat-RNA C attenuated the moderate symptoms of the chimeric virus when Arabidopsis plants were coinoculated with the chimeric virus. Symptom attenuation was correlated with a reduction in viral RNA levels in inoculated and uninoculated leaves. In protoplasts, the presence of sat-RNA C resulted in a reduction of approximately 70% in the chimeric viral genomic RNA at 44 hr postinoculation, whereas the sat-RNA wa consistently amplified to higher levels by the chimeric virus than by wild-type TCV. TCV with a deletion of the coat protein ORF also resulted in a similar increase in sat-RNA C levels in protoplasts, indicating that the TVC coat protein, or its ORF, downregulates the synthesis of sat-RNA C. These results suggest that the coat protein or its ORF is a viral determinant for symptom modulation by sat-RNA C, and symptom attenuation is at least partly due to inhibition of virus accumulation.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allison R., Thompson C., Ahlquist P. 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 U S A. 1990 Mar;87(5):1820–1824. doi: 10.1073/pnas.87.5.1820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carrington J. C., Morris T. J., Stockley P. G., Harrison S. C. Structure and assembly of turnip crinkle virus. IV. Analysis of the coat protein gene and implications of the subunit primary structure. J Mol Biol. 1987 Mar 20;194(2):265–276. doi: 10.1016/0022-2836(87)90374-3. [DOI] [PubMed] [Google Scholar]
  3. Chapman S., Hills G., Watts J., Baulcombe D. Mutational analysis of the coat protein gene of potato virus X: effects on virion morphology and viral pathogenicity. Virology. 1992 Nov;191(1):223–230. doi: 10.1016/0042-6822(92)90183-p. [DOI] [PubMed] [Google Scholar]
  4. Culver J. N., Stubbs G., Dawson W. O. Structure-function relationship between tobacco mosaic virus coat protein and hypersensitivity in Nicotiana sylvestris. J Mol Biol. 1994 Sep 16;242(2):130–138. doi: 10.1006/jmbi.1994.1564. [DOI] [PubMed] [Google Scholar]
  5. Devic M., Jaegle M., Baulcombe D. Cucumber mosaic virus satellite RNA (strain Y): analysis of sequences which affect systemic necrosis on tomato. J Gen Virol. 1990 Jul;71(Pt 7):1443–1449. doi: 10.1099/0022-1317-71-7-1443. [DOI] [PubMed] [Google Scholar]
  6. Guilley H., Carrington J. C., Balàzs E., Jonard G., Richards K., Morris T. J. Nucleotide sequence and genome organization of carnation mottle virus RNA. Nucleic Acids Res. 1985 Sep 25;13(18):6663–6677. doi: 10.1093/nar/13.18.6663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Guzmán P., Ecker J. R. Development of large DNA methods for plants: molecular cloning of large segments of Arabidopsis and carrot DNA into yeast. Nucleic Acids Res. 1988 Dec 9;16(23):11091–11105. doi: 10.1093/nar/16.23.11091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hacker D. L., Petty I. T., Wei N., Morris T. J. Turnip crinkle virus genes required for RNA replication and virus movement. Virology. 1992 Jan;186(1):1–8. doi: 10.1016/0042-6822(92)90055-t. [DOI] [PubMed] [Google Scholar]
  9. Heaton L. A., Lee T. C., Wei N., Morris T. J. Point mutations in the turnip crinkle virus capsid protein affect the symptoms expressed by Nicotiana benthamiana. Virology. 1991 Jul;183(1):143–150. doi: 10.1016/0042-6822(91)90127-w. [DOI] [PubMed] [Google Scholar]
  10. Ishikawa M., Meshi T., Ohno T., Okada Y. Specific cessation of minus-strand RNA accumulation at an early stage of tobacco mosaic virus infection. J Virol. 1991 Feb;65(2):861–868. doi: 10.1128/jvi.65.2.861-868.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kaper J. M. Satellite-induced viral symptom modulation in plants: a case of nested parasitic nucleic acids competing for genetic expression. Res Virol. 1992 Jan-Feb;143(1):5–10. doi: 10.1016/s0923-2516(06)80070-1. [DOI] [PubMed] [Google Scholar]
  12. Kaper J. M., Tousignant M. E., Geletka L. M. Cucumber-mosaic-virus-associated RNA-5. XII. Symptom-modulating effect is codetermined by the helper virus satellite replication support function. Res Virol. 1990 Sep-Oct;141(5):487–503. doi: 10.1016/0923-2516(90)90082-t. [DOI] [PubMed] [Google Scholar]
  13. Li X. H., Heaton L. A., Morris T. J., Simon A. E. Turnip crinkle virus defective interfering RNAs intensify viral symptoms and are generated de novo. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9173–9177. doi: 10.1073/pnas.86.23.9173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Marsh L. E., Huntley C. C., Pogue G. P., Connell J. P., Hall T. C. Regulation of (+):(-)-strand asymmetry in replication of brome mosaic virus RNA. Virology. 1991 May;182(1):76–83. doi: 10.1016/0042-6822(91)90650-z. [DOI] [PubMed] [Google Scholar]
  15. Masuta C., Takanami Y. Determination of sequence and structural requirements for pathogenicity of a cucumber mosaic virus satellite RNA (Y-satRNA). Plant Cell. 1989 Dec;1(12):1165–1173. doi: 10.1105/tpc.1.12.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Naidu R. A., Collins G. B., Ghabrial S. A. Peanut stunt virus satellite RNA: analysis of sequences that affect symptom attenuation in tobacco. Virology. 1992 Aug;189(2):668–677. doi: 10.1016/0042-6822(92)90590-l. [DOI] [PubMed] [Google Scholar]
  17. Roossinck M. J., Sleat D., Palukaitis P. Satellite RNAs of plant viruses: structures and biological effects. Microbiol Rev. 1992 Jun;56(2):265–279. doi: 10.1128/mr.56.2.265-279.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Sacher R., Ahlquist P. Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. J Virol. 1989 Nov;63(11):4545–4552. doi: 10.1128/jvi.63.11.4545-4552.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shintaku M. H., Zhang L., Palukaitis P. A single amino acid substitution in the coat protein of cucumber mosaic virus induces chlorosis in tobacco. Plant Cell. 1992 Jul;4(7):751–757. doi: 10.1105/tpc.4.7.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Simon A. E., Howell S. H. The virulent satellite RNA of turnip crinkle virus has a major domain homologous to the 3' end of the helper virus genome. EMBO J. 1986 Dec 20;5(13):3423–3428. doi: 10.1002/j.1460-2075.1986.tb04664.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Skotnicki M. L., Mackenzie A. M., Torronen M., Gibbs A. J. The genomic sequence of cardamine chlorotic fleck carmovirus. J Gen Virol. 1993 Sep;74(Pt 9):1933–1937. doi: 10.1099/0022-1317-74-9-1933. [DOI] [PubMed] [Google Scholar]
  22. Sleat D. E., Palukaitis P. Induction of tobacco chlorosis by certain cucumber mosaic virus satellite RNAs is specific to subgroup II helper strains. Virology. 1990 May;176(1):292–295. doi: 10.1016/0042-6822(90)90256-q. [DOI] [PubMed] [Google Scholar]
  23. Van der Kuyl A. C., Neeleman L., Bol J. F. Role of alfalfa mosaic virus coat protein in regulation of the balance between viral plus and minus strand RNA synthesis. Virology. 1991 Nov;185(1):496–499. doi: 10.1016/0042-6822(91)90807-n. [DOI] [PubMed] [Google Scholar]
  24. Waterworth H. E., Kaper J. M., Tousignant M. E. CARNA 5, the Small Cucumber Mosaic Virus--Dependent Replicating RNA, Regulates Disease Expression. Science. 1979 May 25;204(4395):845–847. doi: 10.1126/science.204.4395.845. [DOI] [PubMed] [Google Scholar]
  25. Wu G., Kaper J. M. Widely separated sequence elements within cucumber mosaic virus satellites contribute to their ability to induce lethal tomato necrosis. J Gen Virol. 1992 Nov;73(Pt 11):2805–2812. doi: 10.1099/0022-1317-73-11-2805. [DOI] [PubMed] [Google Scholar]
  26. Zhang L., Kim C. H., Palukaitis P. The chlorosis-induction domain of the satellite RNA of cucumber mosaic virus: identifying sequences that affect accumulation and the degree of chlorosis. Mol Plant Microbe Interact. 1994 Mar-Apr;7(2):208–213. doi: 10.1094/mpmi-7-0208. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES