Expression of the Potyvirus Genome: The Role of Proteolytic Processing

  • William G. Dougherty
  • T. Dawn Parks
  • Holly A. Smith
  • John A. Lindbo
Conference paper

Abstract

The potato virus Y [potyvirus] group is comprised of a number of distinctive members, estimated to be between 100 and 150 dependent on the criteria used in classification (Edwardson, 1974; Hollings and Brunt, 1981). Although each member has a rather restrictive host range, the large number of putative members make these viruses ubiquitous pathogens present in most agricultural settings. As such, over the past 5 years they have become one of the more intensively studied plant virus groups. Using molecular biological approaches, our understanding of potyvirus gene structure, function, and expression has increased dramatically.

Keywords

Codon Tyrosine Catalysis Glycine Cysteine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allison, R.F., Sorenson, J.C., Kelly, M.E., Armstrong, F.B., and Dougherty, W.G. (1984). Sequence determination of the capsid protein gene and flanking regions of tobacco etch virus: evidence for the synthesis of a polyprotein in potyvirus genome expression. Proc. Natl. Acad. Sci. USA 82: 3969–3972.CrossRefGoogle Scholar
  2. Allison, R.F., Johnston, R.E., and Dougherty, W.G. (1986). Nucleotide sequence of the coding region of tobacco etch virus genomic RNA: evidence for the synthesis of a single polyprotein. Virology 154: 9–20.PubMedCrossRefGoogle Scholar
  3. Bazan, F.J., and Fletterick, R. (1988). Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications. Proc. Natl. Acad. Sci. USA 85: 7872–7876.PubMedCrossRefGoogle Scholar
  4. Carrington, J.C., Cary, S.M., and Dougherty, W.G. (1988). Mutational analysis of tobacco etch virus polyprotein processing: cis and trans proteolytic activities of polyproteins containing the 49-kilodalton proteinases. J. Virology 62, 2313–2320.PubMedGoogle Scholar
  5. Carrington, J.C., Cary, S.M., Parks, T.D., and Dougherty, W.G. (1989a). A second proteinase encoded by a plant potyvirus genome. EMBO J. 8, 365–370.PubMedGoogle Scholar
  6. Carrington, J.C., and Dougherty, W.G. (1987a). Small nuclear inclusion protein encoded by a plant potyvirus genome is a protease. J. Virology 61, 2540–2548.PubMedGoogle Scholar
  7. Carrington, J.C., and Dougherty, W.G. (1987b). Processing of the tobacco etch virus 49K protease requires autoproteolysis. Virology 160, 355–362.PubMedCrossRefGoogle Scholar
  8. Carrington, J.C., and Dougherty, W.G. (1988). A viral cleavage site cassette: identification of amino acid sequences required for tobacco etch virus polyprotein processing. Proc. Natl. Acad. Sci. USA 85, 3391–3395.PubMedCrossRefGoogle Scholar
  9. Carrington, J.C., Freed, D.D., and Sanders, T.C. (1989b). Autocatalytic processing of the potyvirus helper component proteinase in Escherichia coli and in vitro. J. of Virology 63: 4459–4463.Google Scholar
  10. Chang, C.-A., Hiebert, E., and Purcifull, D.E. (1988). Purification, characterization, and immunological analysis of nuclear inclusions induced by bean yellow mosaic and clover yellow vein potyviruses. Phytopathology 78: 1266–1275.CrossRefGoogle Scholar
  11. Christie, R.G., and Edwardson, J.R. (1977). Light and electron microscopy of plant virus inclusions. Fla Agric. Exp. Sta. Monogr. Ser. 9.198pp.Google Scholar
  12. De Mejia, M.V.G., Hiebert, E., and Purcifull, D.E. (1985). Isolation and partial characterization of the amorphous cytoplasmic inclusions associated with infections caused by two potyviruses. Virology 142: 24–33.PubMedCrossRefGoogle Scholar
  13. Domier, L.L., Franklin, K.M., Shahabuddin, M., Hellmann, G.M., Overmyer, J.H., Hiremath, ST., Siaw, M.F.E., Lomonossoff, G.P., Shaw, J.G., and Rhoades, R.E. (1986). The nucleotide sequence of tobacco vein mottling virus RNA. Nucleic Acids Res. 14: 5417–5430.PubMedCrossRefGoogle Scholar
  14. Dougherty, W.G. (1983). Analysis of viral RNA isolated from tobacco leaf tissue infected with tobacco etch virus. Virology 131, 473–481.PubMedCrossRefGoogle Scholar
  15. Dougherty, W.G., Allison, R.F., Parks, T.D., and Johnston, R.E. (1985). Nucleotide sequence at the 3′ terminus of pepper mottle virus. Virology 146: 282–291.PubMedCrossRefGoogle Scholar
  16. Dougherty, W.G., and Carrington, J.C., 1988. Expression and function of potyviral gene products. Annual Review of Phytopathology 26, 123–143.CrossRefGoogle Scholar
  17. Dougherty, W.G., Carrington, J.C., Cary, S.M., and Parks, T.D. (1988). Biochemical and mutational analysis of a plant virus polyprotein cleavage site. EMBO J. 7, 1281–1287.PubMedGoogle Scholar
  18. Dougherty, W.G., Cary, S.M., and Parks, T.D. (1989a). Molecular genetic analysis of a plant virus polyprotein cleavage site: A model. Virology 171: 356–364.PubMedCrossRefGoogle Scholar
  19. Dougherty, W.G., and Hiebert, E. (1980a). Translation of potyviral RNA in a rabbit reticulocyte lysate: identification of nuclear inclusion protein as products of tobacco etch virus RNA translation and cytoplasmic inclusion protein as a product of the potyvirus genome. Virology 104, 174–182.PubMedCrossRefGoogle Scholar
  20. Dougherty, W.G., and Hiebert, E. (1980b). Translation of potyvirus RNA in a rabbit reticulocyte lysate: Cell-free translation strategy and a genetic map of the potyviral genome. Virology 104: 183–194.PubMedCrossRefGoogle Scholar
  21. Dougherty, W.G., and Parks, T.D. (1989). Molecular genetic and biochemical evidence for the involvement of the heptapeptide cleavage sequence in determining the reaction profile at two tobacco etch virus cleavage site in cell-free assays. Virology 172: 145–155.PubMedCrossRefGoogle Scholar
  22. Dougherty, W.G., Parks, T.D., Cary, S., Bazan, F.J., and Fletterick, R. J. (1989b). Characterization of the catalytic residues of the tobacco etch virus 49kDa proteinase. Virology 172: 302–310.PubMedCrossRefGoogle Scholar
  23. Edwardson, J.R. (1974). Some properties of the potato virus Y-group. Fla. Agric. Exp. Sta. Monogr. Ser. 4.398pp.Google Scholar
  24. Eggenberger, A.L., Stark, D.M., and Beachy, R.N. (1989). The nucleotide sequence of a soybean virus coat protein-coding region and its expression in Escherichia coli, Agrobacterium tumefaciens, and tobacco callus. J. Gen. Virology 70: 1853–1860.CrossRefGoogle Scholar
  25. Garcia, J.-A., Riechmann, J.L., and Lain, S. (1989a). Proteolytic activity of the plum pox potyvirus NIa-like protein in Escherichia coli. Virology 170: 362–369.PubMedCrossRefGoogle Scholar
  26. Garcia, J.A., Reichmann, J.L., and Lain, S. (1989b) Artificial cleavage site recognized by plum pox potyvirus protease in Escherichia coli. J. Virology 63: 2457–2460.PubMedGoogle Scholar
  27. Gorbalenya, A.E., Donchenko, A.P., Blinov, V.M., and Koomin, E.V. (1989). Cysteine Proteases of positive strand RNA viruses and chymotrypsin-like serine protease; A distinct protein superfamily with a common structural fold. FEBS Letters 243: 103–114.PubMedCrossRefGoogle Scholar
  28. Gough, K., H., Azad, A.A., Hanna, P.J., and Shukla, D.D. (1987). Nucleotide sequence of the capsid protein and nuclear inclusion protein genes from the Johnson grass strain of sugarcane mosaic virus RNA. J. Gen. Virology 68: 297–304.CrossRefGoogle Scholar
  29. Hammond, J., and Hammond, R. W. (1989). Molecular cloning, sequencing and expression in Escherichia coli of bean yellow mosaic virus coat protein gene. J. Gen. Virology 70: 1961–1974.CrossRefGoogle Scholar
  30. Hari, V. (1981). The RNA of tobacco etch virus: further characterization and detection of protein linked to RNA. Virology 112: 391–399.PubMedCrossRefGoogle Scholar
  31. Hari, V., Siegel, A., Rozek, C., and Timberlake, W.E. (1979). The RNA of tobacco etch virus contains poly (A). Virology 92: 568–571.PubMedCrossRefGoogle Scholar
  32. Hiebert, E., Purcifull, D., and Christie, R.C. (1984). Purification and immunological analysis of plant viral inclusion bodies. Methods in Virology 7: 225–280., Eds. K. Maramorosh and H. Koprowski. Academic Press, N.Y.Google Scholar
  33. Hellmann, G.M., Shaw, J.G., and Rhoads, R.E. (1988). In vitro analysis of tobacco vein mottling virus NIa cistron; evidence for a virus-encoded protease. Virology 163, 554–562.PubMedCrossRefGoogle Scholar
  34. Hollings, M., and Brunt, A.A. (1981). Potyviruses. in “Handbook of Plant Virus Infections and Comparative Diagnosis”. (Ed. E. Kurstak). pp701–754. Elsevier/North-Holland Biomedical, New York.Google Scholar
  35. Knuhtsen, H., Hiebert, E., and Purcifull, D.E. (1974). Partial purification and some properties of tobacco etch virus intranuclear inclusions. Virology 61: 200–209.PubMedCrossRefGoogle Scholar
  36. Krausslich, H.-G., and Wirnmer, E. (1988). Viral Proteinases. Annual Rev. Biochem. 57, 701–754.CrossRefGoogle Scholar
  37. Lain, S., Reichmann, J.L., Mendez, E., and Garcia, J.A. (1988). Nucleotide sequence of the 3′ terminal region of plum pox potyvirus RNA. Virus Research 10: 325–342.CrossRefGoogle Scholar
  38. Langenberg, W.G. (1986). Virus protein associated with cylindrical inclusions of two viruses that infect wheat. J. Gen. Virology 67: 1161–1168.CrossRefGoogle Scholar
  39. Maiss, E., Timpe, U., Brisske, A., Jelkmann, W., Casper, R., Himmler, G., Mattanovich, D., and Katinger, H.W.D. (1989) The complete nucleotide sequence of plum pox virus RNA. J. Gen. Virology 70: 513–524.CrossRefGoogle Scholar
  40. Murphy, J., Shaw, J.G., and Rhoads, R.E. (1989). The VPg of tobacco etch virus. Phytopathology 79: 1214 (Abst.)Google Scholar
  41. Nicklin, M.J.H., Toyoda, H., Murray, M.G., and Wimmer, E. (1986). Proteolytic processing in the replication of polio and related viruses. Bio/Technology 4, 33–44.CrossRefGoogle Scholar
  42. Oh, C.-S., and Carrington, J.C. (1989). Identification of essential residues in potyvirus proteinase HC-PRO by site-directed mutagenesis. Virology. in press.Google Scholar
  43. Ravelonandro, M., Varveri, C., Delbos, R., and Dunez, J. (1988). Nucleotide sequence of the capsid protein gene of plum pox potyvirus. J. Gen Virology 69: 1509–1516.CrossRefGoogle Scholar
  44. Robaglia, C., Durand-Tardif, M., Tronchet, M., Boudazin, G., Astier-Manifacier, S. and Casse-Delbart, F. (1989). Nucleotide sequence of potato virus Y (N strain) genomic RNA. J. Gen. Virology 70: 935–947.CrossRefGoogle Scholar
  45. Shahabuddin, M., Shaw, J.G., and Rhoads, R.E. (1989). Mapping of the tobacco vein mottling virus VPg cistron. Virology 163: 635–637.CrossRefGoogle Scholar
  46. Siaw, M.F.E., Shahabuddin, M., Ballard, S., Shaw, J.G., and Rhoads, R.E. (1985) Identification of a protein covalently linked to the 5′terminus of tobacco vein mottling virus RNA. Virology 142: 134–143.PubMedCrossRefGoogle Scholar
  47. Slade, D.E., Johnston, R.E., and Dougherty, W.G. (1989). Generation and characterization of monoclonal antibodies reactive with the 49kDa proteinase of tobacco etch virus. Virology 173: in press.Google Scholar
  48. Wellink, J., and van Kammen, A. (1988). Proteases involved in the processing of viral polyproteins. Arch. Virol. 98, 1–26.PubMedCrossRefGoogle Scholar
  49. Vance, V.B., and Beachy, R.N. (1984a). Translation of soybean mosaic virus RNA in vitro: evidence of protein processing. Virology 132: 271–281.PubMedCrossRefGoogle Scholar
  50. Vance, V.B., and Beachy, R.N. (1984b). Detection of genomic-length soybean mosaic virus RNA on polyribosomes of infected soybean leaves. Virology 138: 26–36.PubMedCrossRefGoogle Scholar
  51. Yeh, S.-D, and Gonsalves, D. (1985). Translation of papaya ringspot virus RNA in vitro: detection of a possible polyprotein that is processed for capsid protein, cylindrical-inclusion protein and amorphous-inclusion protein. Virology 143: 260–271.PubMedCrossRefGoogle Scholar
  52. Ypma-Wong, M.F., Dewalt, P.G., Johnson, V.H., Lamb, J.G., and Semler, B.L. (1988a). Protein 3CD is the major poliovirus proteinase responsible for cleavage of the P1 capsid precursor. Virology 166, 265–270.PubMedCrossRefGoogle Scholar
  53. Ypma-Wong, M.F., Filman, D.J., Hogle, J.M., and Semler, B.L. (1988b). Structural domains of the poliovirus polyprotein are major determinants for polyprotein cleavage at gln-gly pairs. J. Biol. Chem. 263, 17846–17856.PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1990

Authors and Affiliations

  • William G. Dougherty
    • 1
  • T. Dawn Parks
    • 1
  • Holly A. Smith
    • 1
  • John A. Lindbo
    • 1
  1. 1.Department of MicrobiologyOregon State UniversityCorvallisUSA

Personalised recommendations