1887

Abstract

Tomato spotted wilt virus (TSWV) particles are spherical and enveloped, an uncommon feature among plant infecting viruses. Previous studies have shown that virus particle formation involves the enwrapment of ribonucleoproteins with viral glycoprotein containing Golgi stacks. In this study, the localization and behaviour of the viral glycoproteins Gn and Gc were analysed, upon transient expression in plant protoplasts. When separately expressed, Gc was solely observed in the endoplasmic reticulum (ER), whereas Gn was found both within the ER and Golgi membranes. Upon co-expression, both glycoproteins were found at ER-export sites and ultimately at the Golgi complex, confirming the ability of Gn to rescue Gc from the ER, possibly due to heterodimerization. Interestingly, both Gc and Gn were shown to induce the deformation of ER and Golgi membranes, respectively, also observed upon co-expression of the two glycoproteins. The behaviour of both glycoproteins within the plant cell and the phenomenon of membrane deformation are discussed in light of the natural process of viral infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.2008/001164-0
2008-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/8/1811.html?itemId=/content/journal/jgv/10.1099/vir.0.2008/001164-0&mimeType=html&fmt=ahah

References

  1. Andersson A. M., Melin L., Persson R., Raschperger E., Wikstrom L., Pettersson R. F. 1997; Processing and membrane topology of the spike proteins G1 and G2 of Uukuniemi virus. J Virol 71:218–225
    [Google Scholar]
  2. Barco A., Carrasco L. 1995; Human virus protein, poliovirus protein 2bc, induces membrane proliferation and blocks the exocytic pathway in the yeast Saccharomyces cerevisiae . EMBO J 14:3349–3364
    [Google Scholar]
  3. Boevink P., Oparka K., Cruz S. S., Martin B., Betteridge A., Hawes C. 1998; Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447 [CrossRef]
    [Google Scholar]
  4. Booth T. F., Gould E. A., Nuttall P. A. 1991; Structure and morphogenesis of dugbe virus ( Bunyaviridae , Nairovirus) studied by immunogold electron-microscopy of ultrathin cryosections. Virus Res 21:199–212 [CrossRef]
    [Google Scholar]
  5. Brandizzi F., Snapp E. L., Roberts A. G., Lippincott-Schwartz J., Hawes C. 2002; Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 14:1293–1309 [CrossRef]
    [Google Scholar]
  6. Carette J. E., Stuiver M., Van Lent J., Wellink J., Van Kammen A. B. 2000; Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J Virol 74:6556–6563 [CrossRef]
    [Google Scholar]
  7. Carette J. E., van Lent J., MacFarlane S. A., Wellink J., van Kammen A. 2002; Cowpea mosaic virus 32- and 60-kilodalton replication proteins target and change the morphology of endoplasmic reticulum membranes. J Virol 76:6293–6301 [CrossRef]
    [Google Scholar]
  8. daSilva L. L. P., Taylor J. P., Hadlington J. L., Hanton S. L., Snowden C. J., Fox S. J., Foresti O., Brandizzi F., Denecke J. 2005; Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17:132–148 [CrossRef]
    [Google Scholar]
  9. Denecke J., Vitale A. 1995; The use of plant protoplasts to study protein synthesis, quality control, protein modification and transport through the plant endomembrane system. Methods Cell Biol 50:335–348
    [Google Scholar]
  10. Elliott R. M. 1990; Molecular biology of the Bunyaviridae . J Gen Virol 71:501–522 [CrossRef]
    [Google Scholar]
  11. Elliott R. M. 1996 The Bunyaviridae New York, NY: Plenum Press;
    [Google Scholar]
  12. Gahmberg N., Kuismanen E., Keranen S., Pettersson R. F. 1986; Uukuniemi virus glycoproteins accumulate in and cause morphological-changes of the Golgi-complex in the absence of virus maturation. J Virol 57:899–906
    [Google Scholar]
  13. Goldbach R., Peters D. 1996; Molecular and biological aspects of tospoviruses. In The Bunyaviridae pp 129–157Edited by Elliott R. M. New York, NY: Plenum Press;
    [Google Scholar]
  14. Griffiths G., Rottier P. 1992; Cell biology of viruses that assemble along the biosynthetic pathway. Semin Cell Biol 3:367–381 [CrossRef]
    [Google Scholar]
  15. Hanton S. L., Matheson L. A., Brandizzi F. 2006; Seeking a way out: export of proteins from the plant endoplasmic reticulum. Trends Plant Sci 11:335–343 [CrossRef]
    [Google Scholar]
  16. Haseloff J., Siemering K. R., Prasher D. C., Hodge S. 1997; Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci U S A 94:2122–2127 [CrossRef]
    [Google Scholar]
  17. Jantti J., Hilden P., Ronka H., Makiranta V., Keranen S., Kuismanen E. 1997; Immunocytochemical analysis of Uukuniemi virus budding compartments: role of the intermediate compartment and the Golgi stack in virus maturation. J Virol 71:1162–1172
    [Google Scholar]
  18. Karimi M., Inze D., Depicker A. 2002; GATEWAYTM vectors for Agrobacterium -mediated plant transformation. Trends Plant Sci 7:193–195 [CrossRef]
    [Google Scholar]
  19. Kikkert M., van Poelwijk F., Storms M., Kassies W., Bloksma H., van Lent J., Kormelink R., Goldbach R. 1997; A protoplast system for studying tomato spotted wilt virus infection. J Gen Virol 78:1755–1763
    [Google Scholar]
  20. Kikkert M., van Lent J., Storms M., Bodegom P., Kormelink R., Goldbach R. 1999; Tomato spotted wilt virus particle morphogenesis in plant cells. J Virol 73:2288–2297
    [Google Scholar]
  21. Kikkert M., Verschoor A., Kormelink R., Rottier P., Goldbach R. 2001; Tomato spotted wilt virus glycoproteins exhibit trafficking and localization signals that are functional in mammalian cells. J Virol 75:1004–1012 [CrossRef]
    [Google Scholar]
  22. Kitajima E., de Avila A. C., Resende R., Goldbach R. W., Peters D. 1992; Comparative cytological and immunogold labelling studies on different isolates of Tomato spotted wilt virus. J Submicrosc Cytol Pathol 24:1–14
    [Google Scholar]
  23. Kolesnikova L., Berghofer B., Bamberg S., Becker S. 2004; Multivesicular bodies as a platform for formation of the Marburg virus envelope. J Virol 78:12277–12287 [CrossRef]
    [Google Scholar]
  24. Kuismanen E., Hedman K., Saraste J., Pettersson R. F. 1982; Uukuniemi virus maturation: accumulation of virus-particles and viral-antigens in the Golgi-complex. Mol Cell Biol 2:1444–1458
    [Google Scholar]
  25. Latham T., Galarza J. M. 2001; Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J Virol 75:6154–6165 [CrossRef]
    [Google Scholar]
  26. Lyons M. J., Heyduk J. 1973; Aspects of developmental morphology of California encephalitis-virus in cultured vertebrate and arthropod cells and in mouse brain. Virology 54:37–52 [CrossRef]
    [Google Scholar]
  27. Maliga P., Sz-Breznovits A., Márton L. 1973; Streptomycin-resistant plants from callus culture of haploid tobacco. Nat New Biol 244:29–30 [CrossRef]
    [Google Scholar]
  28. Matsuoka Y., Chen S. Y., Holland C. E., Compans R. W. 1996; Molecular determinants of Golgi retention in the Punta Toro G1 glycoprotein. Arch Biochem Biophys 336:184–189 [CrossRef]
    [Google Scholar]
  29. Mohamed N. A., Randles J. W., Francki R. I. B. 1973; Protein composition of Tomato spotted wilt virus. Virology 56:12–21 [CrossRef]
    [Google Scholar]
  30. Murashige R., Skoog F. 1962; A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497 [CrossRef]
    [Google Scholar]
  31. Pettersson R. F., Melin L. 1996; Synthesis, assembly, and intracellular transport of Bunyaviridae membrane proteins. In The Bunyaviridae pp 159–188Edited by Elliott R. M. New York, NY: Plenum Press;
    [Google Scholar]
  32. Rönnholm R. 1992; Localization to the Golgi complex of Uukuniemi virus glycoproteins G1 and G2 expressed from clones cDNAs. J Virol 66:4525–4531
    [Google Scholar]
  33. Rwambo P. M., Shaw M. K., Rurangirwa F. R., DeMartini J. C. 1996; Ultrastructural studies on the replication and morphogenesis of Nairobi sheep disease virus, a Nairovirus. Arch Virol 141:1479–1492 [CrossRef]
    [Google Scholar]
  34. Salanueva I. J., Novoa R. R., Cabezas P., Lopez-Iglesias C., Carrascosa J. L., Elliott R. M., Risco C. 2003; Polymorphism and structural maturation of Bunyamwera virus in Golgi and post-golgi compartments. J Virol 77:1368–1381 [CrossRef]
    [Google Scholar]
  35. Shaw K. L., Lindemann D., Mulligan M. J., Goepfert P. A. 2003; Foamy virus envelope glycoprotein is sufficient for particle budding and release. J Virol 77:2338–2348 [CrossRef]
    [Google Scholar]
  36. Smith J. F., Pifat D. Y. 1982; Morphogenesis of Sandfly fever viruses ( Bunyaviridae family). Virology 121:61–81 [CrossRef]
    [Google Scholar]
  37. Snippe M., Borst J.-W., Goldbach R., Kormelink R. 2007; Tomato spotted wilt virus Gc and N proteins interact in vivo . Virology 357:115–123 [CrossRef]
    [Google Scholar]
  38. Stefano G., Renna L., Chatre L., Hanton S. L., Moreau P., Hawes C., Brandizzi F. 2006; In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J 46:95–110 [CrossRef]
    [Google Scholar]
  39. Veijola J., Pettersson R. F. 1999; Transient association of calnexin and calreticulin with newly synthesized G1 and G2 glycoproteins of Uukuniemi virus (family Bunyaviridae ). J Virol 73:6123–6127
    [Google Scholar]
  40. Whitfield A. E., Ullman D. E., German T. L. 2005; Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489 [CrossRef]
    [Google Scholar]
  41. Wijkamp I., van Lent J., Kormelink R., Goldbach R., Peters D. 1993; Multiplication of tomato spotted wilt virus in its insect vector, Frankliniella occidentalis . J Gen Virol 74:341–349 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.2008/001164-0
Loading
/content/journal/jgv/10.1099/vir.0.2008/001164-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error