Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1995 Mar;69(3):1485–1492. doi: 10.1128/jvi.69.3.1485-1492.1995

Host-specific alterations in viral RNA accumulation and infection spread in a brome mosaic virus isolate with an expanded host range.

W De Jong 1, P Ahlquist 1
PMCID: PMC188738  PMID: 7853481

Abstract

To facilitate studies of virus-host interaction and the determinants of viral host range, we constructed full-length cDNA clones to all three genomic RNAs of an unusual brome mosaic virus (BMV) isolate with an expanded host range. While other BMV strains, including the previously cloned M1 strain, systemically infect barley and other grasses but not legumes, the expanded-host-range isolate and the set of transcripts from its cDNA clones, designated the M2 strain of BMV, systemically infect both barley and cowpea line TVu-612, a legume. All reassorted combinations of M1 and M2 genomic RNAs were equally competent for replication in barley protoplasts and systemic infection of barley plants but showed widely varying levels of viral RNA accumulation in cowpea protoplasts and systemic infection in TVu-612 cowpea plants. Systemic infection levels were influenced by all three genomic RNAs. M2 RNA2 and M2 RNA3 made independent and additive contributions to the frequency with which reassortants infected TVu-612 systemically. The greater individual effect segregated with M2 RNA3, which encodes functions required for infection spread (the 3a movement protein and coat protein). M2 RNA3 also directed accelerated expansion of BMV lesions in inoculated TVu-612 leaves. If the inoculum contained M2 RNA3, the frequency with which reassortants infected TVu-612 systemically could be further enhanced by the presence of M2 RNA1 rather than M1 RNA1. RNA1 encodes the 1a RNA replication protein, and despite similar accumulation in barley protoplasts, in cowpea protoplasts all reassortants bearing M2 RNA1 accumulated positive- and negative-strand RNAs to levels at least six- to eightfold higher than reassortants bearing M1 RNA1. Overall, the results indicate that changes in several distinct virus functions contribute to adapting BMV-M2 to systemically infect TVu-612 cowpea.

Full Text

The Full Text of this article is available as a PDF (619.0 KB).

Selected References

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

  1. Ahlquist P., Dasgupta R., Kaesberg P. Nucleotide sequence of the brome mosaic virus genome and its implications for viral replication. J Mol Biol. 1984 Feb 5;172(4):369–383. doi: 10.1016/s0022-2836(84)80012-1. [DOI] [PubMed] [Google Scholar]
  2. Ahlquist P., French R., Janda M., Loesch-Fries L. S. Multicomponent RNA plant virus infection derived from cloned viral cDNA. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7066–7070. doi: 10.1073/pnas.81.22.7066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ahlquist P., Luckow V., Kaesberg P. Complete nucleotide sequence of brome mosaic virus RNA3. J Mol Biol. 1981 Nov 25;153(1):23–38. doi: 10.1016/0022-2836(81)90524-6. [DOI] [PubMed] [Google Scholar]
  4. Ahlquist P., Strauss E. G., Rice C. M., Strauss J. H., Haseloff J., Zimmern D. Sindbis virus proteins nsP1 and nsP2 contain homology to nonstructural proteins from several RNA plant viruses. J Virol. 1985 Feb;53(2):536–542. doi: 10.1128/jvi.53.2.536-542.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Allison R. F., Janda M., Ahlquist P. Infectious in vitro transcripts from cowpea chlorotic mottle virus cDNA clones and exchange of individual RNA components with brome mosaic virus. J Virol. 1988 Oct;62(10):3581–3588. doi: 10.1128/jvi.62.10.3581-3588.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. De Jong W., Ahlquist P. A hybrid plant RNA virus made by transferring the noncapsid movement protein from a rod-shaped to an icosahedral virus is competent for systemic infection. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6808–6812. doi: 10.1073/pnas.89.15.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dinant S., Janda M., Kroner P. A., Ahlquist P. Bromovirus RNA replication and transcription require compatibility between the polymerase- and helicase-like viral RNA synthesis proteins. J Virol. 1993 Dec;67(12):7181–7189. doi: 10.1128/jvi.67.12.7181-7189.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gorbalenya A. E., Koonin E. V., Donchenko A. P., Blinov V. M. A novel superfamily of nucleoside triphosphate-binding motif containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett. 1988 Aug 1;235(1-2):16–24. doi: 10.1016/0014-5793(88)81226-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Knorr D. A., Dawson W. O. A point mutation in the tobacco mosaic virus capsid protein gene induces hypersensitivity in Nicotiana sylvestris. Proc Natl Acad Sci U S A. 1988 Jan;85(1):170–174. doi: 10.1073/pnas.85.1.170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kohm B. A., Goulden M. G., Gilbert J. E., Kavanagh T. A., Baulcombe D. C. A Potato Virus X Resistance Gene Mediates an Induced, Nonspecific Resistance in Protoplasts. Plant Cell. 1993 Aug;5(8):913–920. doi: 10.1105/tpc.5.8.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kroner P. A., Young B. M., Ahlquist P. Analysis of the role of brome mosaic virus 1a protein domains in RNA replication, using linker insertion mutagenesis. J Virol. 1990 Dec;64(12):6110–6120. doi: 10.1128/jvi.64.12.6110-6120.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kroner P., Richards D., Traynor P., Ahlquist P. Defined mutations in a small region of the brome mosaic virus 2 gene cause diverse temperature-sensitive RNA replication phenotypes. J Virol. 1989 Dec;63(12):5302–5309. doi: 10.1128/jvi.63.12.5302-5309.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lehto K., Grantham G. L., Dawson W. O. Insertion of sequences containing the coat protein subgenomic RNA promoter and leader in front of the tobacco mosaic virus 30K ORF delays its expression and causes defective cell-to-cell movement. Virology. 1990 Jan;174(1):145–157. doi: 10.1016/0042-6822(90)90063-w. [DOI] [PubMed] [Google Scholar]
  15. Meshi T., Motoyoshi F., Adachi A., Watanabe Y., Takamatsu N., Okada Y. Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J. 1988 Jun;7(6):1575–1581. doi: 10.1002/j.1460-2075.1988.tb02982.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meshi T., Motoyoshi F., Maeda T., Yoshiwoka S., Watanabe H., Okada Y. Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell. 1989 May;1(5):515–522. doi: 10.1105/tpc.1.5.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mi S., Stollar V. Expression of Sindbis virus nsP1 and methyltransferase activity in Escherichia coli. Virology. 1991 Sep;184(1):423–427. doi: 10.1016/0042-6822(91)90862-6. [DOI] [PubMed] [Google Scholar]
  18. Mise K., Allison R. F., Janda M., Ahlquist P. Bromovirus movement protein genes play a crucial role in host specificity. J Virol. 1993 May;67(5):2815–2823. doi: 10.1128/jvi.67.5.2815-2823.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pacha R. F., Ahlquist P. Use of bromovirus RNA3 hybrids to study template specificity in viral RNA amplification. J Virol. 1991 Jul;65(7):3693–3703. doi: 10.1128/jvi.65.7.3693-3703.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sanfaçon H., Wieczorek A. Analysis of cauliflower mosaic virus RNAs in Brassica species showing a range of susceptibility to infection. Virology. 1992 Sep;190(1):30–39. doi: 10.1016/0042-6822(92)91189-2. [DOI] [PubMed] [Google Scholar]
  21. Traynor P., Young B. M., Ahlquist P. Deletion analysis of brome mosaic virus 2a protein: effects on RNA replication and systemic spread. J Virol. 1991 Jun;65(6):2807–2815. doi: 10.1128/jvi.65.6.2807-2815.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES