Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1993 May;67(5):2815–2823. doi: 10.1128/jvi.67.5.2815-2823.1993

Bromovirus movement protein genes play a crucial role in host specificity.

K Mise 1, R F Allison 1, M Janda 1, P Ahlquist 1
PMCID: PMC237606  PMID: 7682628

Abstract

Monocot-adapted brome mosaic virus (BMV) and dicot-adapted cowpea chlorotic mottle virus (CCMV) are closely related bromoviruses with tripartite RNA genomes. Although RNAs 1 and 2 together are sufficient for RNA replication in protoplasts, systemic infection also requires RNA3, which encodes the coat protein and the nonstructural 3a movement protein. We have previously shown with bromoviral reassortants that host specificity determinants in both viruses are encoded by RNA3 as well as by RNA1 and/or RNA2. Here, to test their possible role in host specificity, the 3a movement protein genes were precisely exchanged between BMV and CCMV. The hybrid viruses, but not 3a deletion mutants, systemically infected Nicotiana benthamiana, a permissive host for both parental viruses. The hybrids thus retain basic competence for replication, packaging, cell-to-cell spread, and long-distance (vascular) spread. However, the hybrids failed to systemically infect either barley or cowpea, selective hosts for parental viruses. Thus, the 3a gene and/or its encoded 3a protein contributes to host specificity of both monocot- and dicot-adapted bromoviruses. Tests of inoculated cowpea leaves showed that the spread of the CCMV hybrid containing the BMV 3a gene was blocked at a very early stage of infection. Moreover, the BMV hybrid containing the CCMV 3a gene appeared to spread farther than wt BMV in inoculated cowpea leaves. Several pseudorevertants directing systemic infection in cowpea leaves were obtained from plants inoculated with the CCMV(BMV 3a) hybrid, suggesting that the number of mutations required to adapt the hybrid to dicots is small.

Full text

PDF
2816

Images in this article

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., Janda M. cDNA cloning and in vitro transcription of the complete brome mosaic virus genome. Mol Cell Biol. 1984 Dec;4(12):2876–2882. doi: 10.1128/mcb.4.12.2876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  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. F., Janda M., Ahlquist P. Sequence of cowpea chlorotic mottle virus RNAs 2 and 3 and evidence of a recombination event during bromovirus evolution. Virology. 1989 Sep;172(1):321–330. doi: 10.1016/0042-6822(89)90134-7. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Atabekov J. G., Taliansky M. E. Expression of a plant virus-coded transport function by different viral genomes. Adv Virus Res. 1990;38:201–248. doi: 10.1016/s0065-3527(08)60863-5. [DOI] [PubMed] [Google Scholar]
  9. Dasgupta R., Harada F., Kaesberg P. Blocked 5' termini in brome mosaic virus RNA. J Virol. 1976 Apr;18(1):260–267. doi: 10.1128/jvi.18.1.260-267.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dasgupta R., Kaesberg P. Complete nucleotide sequences of the coat protein messenger RNAs of brome mosaic virus and cowpea chlorotic mottle virus. Nucleic Acids Res. 1982 Jan 22;10(2):703–713. doi: 10.1093/nar/10.2.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Deom C. M., Lapidot M., Beachy R. N. Plant virus movement proteins. Cell. 1992 Apr 17;69(2):221–224. doi: 10.1016/0092-8674(92)90403-y. [DOI] [PubMed] [Google Scholar]
  13. Dreher T. W., Rao A. L., Hall T. C. Replication in vivo of mutant brome mosaic virus RNAs defective in aminoacylation. J Mol Biol. 1989 Apr 5;206(3):425–438. doi: 10.1016/0022-2836(89)90491-9. [DOI] [PubMed] [Google Scholar]
  14. Dzianott A. M., Bujarski J. J. The nucleotide sequence and genome organization of the RNA-1 segment in two bromoviruses: broad bean mottle virus and cowpea chlorotic mottle virus. Virology. 1991 Dec;185(2):553–562. doi: 10.1016/0042-6822(91)90525-g. [DOI] [PubMed] [Google Scholar]
  15. French R., Ahlquist P. Intercistronic as well as terminal sequences are required for efficient amplification of brome mosaic virus RNA3. J Virol. 1987 May;61(5):1457–1465. doi: 10.1128/jvi.61.5.1457-1465.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. French R., Janda M., Ahlquist P. Bacterial gene inserted in an engineered RNA virus: efficient expression in monocotyledonous plant cells. Science. 1986 Mar 14;231(4743):1294–1297. doi: 10.1126/science.231.4743.1294. [DOI] [PubMed] [Google Scholar]
  17. Hibi T., Rezelman G., Van Kammen A. Infection of cowpea mesophyll protoplasts with cowpea mosaic virus. Virology. 1975 Apr;64(2):308–318. doi: 10.1016/0042-6822(75)90107-5. [DOI] [PubMed] [Google Scholar]
  18. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. doi: 10.1126/science.7041255. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Pacha R. F., Ahlquist P. Substantial portions of the 5' and intercistronic noncoding regions of cowpea chlorotic mottle virus RNA3 are dispensable for systemic infection but influence viral competitiveness and infection pathology. Virology. 1992 Mar;187(1):298–307. doi: 10.1016/0042-6822(92)90318-j. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Pacha R. F., Allison R. F., Ahlquist P. cis-acting sequences required for in vivo amplification of genomic RNA3 are organized differently in related bromoviruses. Virology. 1990 Feb;174(2):436–443. doi: 10.1016/0042-6822(90)90097-b. [DOI] [PubMed] [Google Scholar]
  24. Smith D. B., Inglis S. C. The mutation rate and variability of eukaryotic viruses: an analytical review. J Gen Virol. 1987 Nov;68(Pt 11):2729–2740. doi: 10.1099/0022-1317-68-11-2729. [DOI] [PubMed] [Google Scholar]
  25. Steinhauer D. A., Holland J. J. Direct method for quantitation of extreme polymerase error frequencies at selected single base sites in viral RNA. J Virol. 1986 Jan;57(1):219–228. doi: 10.1128/jvi.57.1.219-228.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Traynor P., Ahlquist P. Use of bromovirus RNA2 hybrids to map cis- and trans-acting functions in a conserved RNA replication gene. J Virol. 1990 Jan;64(1):69–77. doi: 10.1128/jvi.64.1.69-77.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]

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

RESOURCES