Abstract
The ability of viruses to move through infected plants is an important determinant of host range and pathogenicity. We have investigated the genetic basis for the inability of the Type strain of barley stripe mosaic hordeivirus to undergo long-range systemic movement in the tobacco Nicotiana benthamiana. We show that, in this model system, a short open reading frame in the 5' leader of the smallest viral genomic RNA prevents long-range vascular movement. As predicted by the ribosome scanning model, the leader open reading frame decreases the efficiency with which the 5'-proximal gene is translated in vitro. Thus, systemic pathogenicity in this system may be determined by the efficiency of translation of a viral gene in vivo and is not determined by the primary sequence of the encoded protein.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Atabekov J. G., Dorokhov YuL Plant virus-specific transport function and resistance of plants to viruses. Adv Virus Res. 1984;29:313–364. doi: 10.1016/s0065-3527(08)60412-1. [DOI] [PubMed] [Google Scholar]
- Dasso M. C., Jackson R. J. On the fidelity of mRNA translation in the nuclease-treated rabbit reticulocyte lysate system. Nucleic Acids Res. 1989 Apr 25;17(8):3129–3144. doi: 10.1093/nar/17.8.3129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deom C. M., Oliver M. J., Beachy R. N. The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science. 1987 Jul 24;237(4813):389–394. doi: 10.1126/science.237.4813.389. [DOI] [PubMed] [Google Scholar]
- Geballe A. P., Mocarski E. S. Translational control of cytomegalovirus gene expression is mediated by upstream AUG codons. J Virol. 1988 Sep;62(9):3334–3340. doi: 10.1128/jvi.62.9.3334-3340.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gustafson G., Armour S. L., Gamboa G. C., Burgett S. G., Shepherd J. W. Nucleotide sequence of barley stripe mosaic virus RNA alpha: RNA alpha encodes a single polypeptide with homology to corresponding proteins from other viruses. Virology. 1989 Jun;170(2):370–377. doi: 10.1016/0042-6822(89)90427-3. [DOI] [PubMed] [Google Scholar]
- Gustafson G., Armour S. L. The complete nucleotide sequence of RNA beta from the type strain of barley stripe mosaic virus. Nucleic Acids Res. 1986 May 12;14(9):3895–3909. doi: 10.1093/nar/14.9.3895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gustafson G., Hunter B., Hanau R., Armour S. L., Jackson A. O. Nucleotide sequence and genetic organization of barley stripe mosaic virus RNA gamma. Virology. 1987 Jun;158(2):394–406. doi: 10.1016/0042-6822(87)90211-x. [DOI] [PubMed] [Google Scholar]
- 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]
- Kozak M. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol Cell Biol. 1987 Oct;7(10):3438–3445. doi: 10.1128/mcb.7.10.3438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Regulation of protein synthesis in virus-infected animal cells. Adv Virus Res. 1986;31:229–292. doi: 10.1016/S0065-3527(08)60265-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Meshi T., Watanabe Y., Saito T., Sugimoto A., Maeda T., Okada Y. Function of the 30 kd protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J. 1987 Sep;6(9):2557–2563. doi: 10.1002/j.1460-2075.1987.tb02544.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petty I. T., Hunter B. G., Jackson A. O. A novel strategy for one-step cloning of full-length cDNA and its application to the genome of barley stripe mosaic virus. Gene. 1988 Dec 30;74(2):423–432. doi: 10.1016/0378-1119(88)90175-8. [DOI] [PubMed] [Google Scholar]
- Petty I. T., Hunter B. G., Wei N., Jackson A. O. Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. Virology. 1989 Aug;171(2):342–349. doi: 10.1016/0042-6822(89)90601-6. [DOI] [PubMed] [Google Scholar]
- SIEGEL A., ZAITLIN M., SEHGAL O. P. The isolation of defective tobacco mosaic virus strains. Proc Natl Acad Sci U S A. 1962 Oct 15;48:1845–1851. doi: 10.1073/pnas.48.10.1845. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Saito T., Meshi T., Takamatsu N., Okada Y. Coat protein gene sequence of tobacco mosaic virus encodes a host response determinant. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6074–6077. doi: 10.1073/pnas.84.17.6074. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saito T., Yamanaka K., Okada Y. Long-distance movement and viral assembly of tobacco mosaic virus mutants. Virology. 1990 Jun;176(2):329–336. doi: 10.1016/0042-6822(90)90002-9. [DOI] [PubMed] [Google Scholar]
- Saito T., Yamanaka K., Watanabe Y., Takamatsu N., Meshi T., Okada Y. Mutational analysis of the coat protein gene of tobacco mosaic virus in relation to hypersensitive response in tobacco plants with the N' gene. Virology. 1989 Nov;173(1):11–20. doi: 10.1016/0042-6822(89)90217-1. [DOI] [PubMed] [Google Scholar]
- Sedman S. A., Good P. J., Mertz J. E. Leader-encoded open reading frames modulate both the absolute and relative rates of synthesis of the virion proteins of simian virus 40. J Virol. 1989 Sep;63(9):3884–3893. doi: 10.1128/jvi.63.9.3884-3893.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]