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. 1997 Nov;71(11):8624–8631. doi: 10.1128/jvi.71.11.8624-8631.1997

VPg of tobacco etch potyvirus is a host genotype-specific determinant for long-distance movement.

M C Schaad 1, A D Lellis 1, J C Carrington 1
PMCID: PMC192326  PMID: 9343220

Abstract

The V20 cultivar of Nicotiana tabacum was shown previously to exhibit a strain-specific restriction of long-distance movement of tobacco etch potyvirus (TEV). In V20, both TEV-HAT and TEV-Oxnard strains are capable of genome amplification and cell-to-cell movement, but only TEV-Oxnard is capable of systemic infection by vasculature-dependent long-distance movement. To investigate the basis for host-specific movement of TEV, chimeric virus genomes were assembled from TEV-HAT and TEV-Oxnard. Viruses containing the TEV-Oxnard coding regions for HC-Pro and/or capsid protein (CP), two proteins that are known to be essential for TEV long-distance movement, failed to infect V20 systemically. In contrast, chimeric viruses encoding the TEV-Oxnard VPg domain of NIa were able to infect V20 systemically. The critical region controlling the infection phenotype in V20 was mapped to a 67-nucleotide segment containing 10-nucleotide differences, but only five amino acid differences, between TEV-HAT and TEV-Oxnard. In V20 coinfection experiments, a restricted strain had no effect on systemic infection by a long-distance movement-competent chimeric strain, suggesting that the restricted strain was not inducing a generalized systemic resistance response. These data suggest that the VPg domain, which is covalently attached to the 5' end of genomic RNA, interacts either directly or indirectly with host components to facilitate long-distance movement.

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Selected References

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  1. Atreya C. D., Pirone T. P. Mutational analysis of the helper component-proteinase gene of a potyvirus: effects of amino acid substitutions, deletions, and gene replacement on virulence and aphid transmissibility. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11919–11923. doi: 10.1073/pnas.90.24.11919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Callaway A., Liu W., Andrianov V., Stenzler L., Zhao J., Wettlaufer S., Jayakumar P., Howell S. H. Characterization of cauliflower mosaic virus (CaMV) resistance in virus-resistant ecotypes of Arabidopsis. Mol Plant Microbe Interact. 1996 Dec;9(9):810–818. doi: 10.1094/mpmi-9-0810. [DOI] [PubMed] [Google Scholar]
  4. Carrington J. C., Freed D. D., Leinicke A. J. Bipartite signal sequence mediates nuclear translocation of the plant potyviral NIa protein. Plant Cell. 1991 Sep;3(9):953–962. doi: 10.1105/tpc.3.9.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carrington J. C., Haldeman R., Dolja V. V., Restrepo-Hartwig M. A. Internal cleavage and trans-proteolytic activities of the VPg-proteinase (NIa) of tobacco etch potyvirus in vivo. J Virol. 1993 Dec;67(12):6995–7000. doi: 10.1128/jvi.67.12.6995-7000.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carrington J. C., Kasschau K. D., Mahajan S. K., Schaad M. C. Cell-to-Cell and Long-Distance Transport of Viruses in Plants. Plant Cell. 1996 Oct;8(10):1669–1681. doi: 10.1105/tpc.8.10.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cronin S., Verchot J., Haldeman-Cahill R., Schaad M. C., Carrington J. C. Long-distance movement factor: a transport function of the potyvirus helper component proteinase. Plant Cell. 1995 May;7(5):549–559. doi: 10.1105/tpc.7.5.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Dolja V. V., Haldeman-Cahill R., Montgomery A. E., Vandenbosch K. A., Carrington J. C. Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology. 1995 Feb 1;206(2):1007–1016. doi: 10.1006/viro.1995.1023. [DOI] [PubMed] [Google Scholar]
  10. Dolja V. V., Haldeman R., Robertson N. L., Dougherty W. G., Carrington J. C. Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J. 1994 Mar 15;13(6):1482–1491. doi: 10.1002/j.1460-2075.1994.tb06403.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dolja V. V., McBride H. J., Carrington J. C. Tagging of plant potyvirus replication and movement by insertion of beta-glucuronidase into the viral polyprotein. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10208–10212. doi: 10.1073/pnas.89.21.10208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gal-On A., Kaplan I., Roossinck M. J., Palukaitis P. The kinetics of infection of zucchini squash by cucumber mosaic virus indicate a function for RNA 1 in virus movement. Virology. 1994 Nov 15;205(1):280–289. doi: 10.1006/viro.1994.1644. [DOI] [PubMed] [Google Scholar]
  13. Holt C. A., Hodgson R. A., Coker F. A., Beachy R. N., Nelson R. S. Characterization of the masked strain of tobacco mosaic virus: identification of the region responsible for symptom attenuation by analysis of an infectious cDNA clone. Mol Plant Microbe Interact. 1990 Nov-Dec;3(6):417–423. doi: 10.1094/mpmi-3-417. [DOI] [PubMed] [Google Scholar]
  14. Horton R. M. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol Biotechnol. 1995 Apr;3(2):93–99. doi: 10.1007/BF02789105. [DOI] [PubMed] [Google Scholar]
  15. Kasschau K. D., Carrington J. C. Requirement for HC-Pro processing during genome amplification of tobacco etch potyvirus. Virology. 1995 May 10;209(1):268–273. doi: 10.1006/viro.1995.1254. [DOI] [PubMed] [Google Scholar]
  16. Kasschau K. D., Cronin S., Carrington J. C. Genome amplification and long-distance movement functions associated with the central domain of tobacco etch potyvirus helper component-proteinase. Virology. 1997 Feb 17;228(2):251–262. doi: 10.1006/viro.1996.8368. [DOI] [PubMed] [Google Scholar]
  17. Klein P. G., Klein R. R., Rodríguez-Cerezo E., Hunt A. G., Shaw J. G. Mutational analysis of the tobacco vein mottling virus genome. Virology. 1994 Nov 1;204(2):759–769. doi: 10.1006/viro.1994.1591. [DOI] [PubMed] [Google Scholar]
  18. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  19. Lee S., Stenger D. C., Bisaro D. M., Davis K. R. Identification of loci in Arabidopsis that confer resistance to geminivirus infection. Plant J. 1994 Oct;6(4):525–535. doi: 10.1046/j.1365-313x.1994.6040525.x. [DOI] [PubMed] [Google Scholar]
  20. Leisner S. M., Turgeon R., Howell S. H. Effects of host plant development and genetic determinants on the long-distance movement of cauliflower mosaic virus in Arabidopsis. Plant Cell. 1993 Feb;5(2):191–202. doi: 10.1105/tpc.5.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Leisner S. M., Turgeon R. Movement of virus and photoassimilate in the phloem: a comparative analysis. Bioessays. 1993 Nov;15(11):741–748. doi: 10.1002/bies.950151107. [DOI] [PubMed] [Google Scholar]
  22. Li X. H., Carrington J. C. Complementation of tobacco etch potyvirus mutants by active RNA polymerase expressed in transgenic cells. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):457–461. doi: 10.1073/pnas.92.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mahajan S., Dolja V. V., Carrington J. C. Roles of the sequence encoding tobacco etch virus capsid protein in genome amplification: requirements for the translation process and a cis-active element. J Virol. 1996 Jul;70(7):4370–4379. doi: 10.1128/jvi.70.7.4370-4379.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Murphy J. F., Klein P. G., Hunt A. G., Shaw J. G. Replacement of the tyrosine residue that links a potyviral VPg to the viral RNA is lethal. Virology. 1996 Jun 15;220(2):535–538. doi: 10.1006/viro.1996.0344. [DOI] [PubMed] [Google Scholar]
  26. Murphy J. F., Rhoads R. E., Hunt A. G., Shaw J. G. The VPg of tobacco etch virus RNA is the 49-kDa proteinase or the N-terminal 24-kDa part of the proteinase. Virology. 1990 Sep;178(1):285–288. doi: 10.1016/0042-6822(90)90405-g. [DOI] [PubMed] [Google Scholar]
  27. Murphy J. F., Rychlik W., Rhoads R. E., Hunt A. G., Shaw J. G. A tyrosine residue in the small nuclear inclusion protein of tobacco vein mottling virus links the VPg to the viral RNA. J Virol. 1991 Jan;65(1):511–513. doi: 10.1128/jvi.65.1.511-513.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Riechmann J. L., Laín S., García J. A. The genome-linked protein and 5' end RNA sequence of plum pox potyvirus. J Gen Virol. 1989 Oct;70(Pt 10):2785–2789. doi: 10.1099/0022-1317-70-10-2785. [DOI] [PubMed] [Google Scholar]
  29. Schaad M. C., Carrington J. C. Suppression of long-distance movement of tobacco etch virus in a nonsusceptible host. J Virol. 1996 Apr;70(4):2556–2561. doi: 10.1128/jvi.70.4.2556-2561.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schaad M. C., Haldeman-Cahill R., Cronin S., Carrington J. C. Analysis of the VPg-proteinase (NIa) encoded by tobacco etch potyvirus: effects of mutations on subcellular transport, proteolytic processing, and genome amplification. J Virol. 1996 Oct;70(10):7039–7048. doi: 10.1128/jvi.70.10.7039-7048.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shahabuddin M., Shaw J. G., Rhoads R. E. Mapping of the tobacco vein mottling virus VPg cistron. Virology. 1988 Apr;163(2):635–637. doi: 10.1016/0042-6822(88)90307-8. [DOI] [PubMed] [Google Scholar]
  32. Sheng J., Citovsky V. Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell. 1996 Oct;8(10):1699–1710. doi: 10.1105/tpc.8.10.1699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Weber H., Schultze S., Pfitzner A. J. Two amino acid substitutions in the tomato mosaic virus 30-kilodalton movement protein confer the ability to overcome the Tm-2(2) resistance gene in the tomato. J Virol. 1993 Nov;67(11):6432–6438. doi: 10.1128/jvi.67.11.6432-6438.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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