1887

Abstract

Members of the family (‘luteovirids’) rely strictly on aphid vectors for plant-to-plant transmission. This interaction operates according to a persistent and circulative manner, which implies that the virions are being endocytosed and exocytosed across two epithelial barriers (alimentary tract and accessory salivary glands) in the vector's body. In several luteovirid–aphid vector species combinations, the route of virions in the insect has been investigated ultrastructurally by transmission electron microscopy (TEM). Here, we used TEM to follow the route of (CABYV; genus ) in its two efficient vector species, and . We demonstrated that CABYV particles are acquired from the gut lumen to the haemocoel through two different sites in both aphid species, i.e. the posterior midgut (as for in . ) and the hindgut (as for complex in cereal aphids). This ‘dual’ tissue specificity of CABYV represents an original situation among viruses in the family examined so far by TEM. A variety of virion-containing structures (e.g. clathrin-coated and tubular vesicles, endosome-like bodies) are found in intestinal cells of both types in both aphids. Release of virus particles from midgut and hindgut cells into the haemolymph was confirmed by immunotrapping using CABYV-specific antibodies. In accessory salivary glands, transport of CABYV virions across the cells was similar in each aphid species, and occurred by a transcytosis mechanism involving formation of tubular and coated vesicles before release of free virions in the salivary canal.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19415-0
2003-12-01
2019-12-13
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/12/vir843473.html?itemId=/content/journal/jgv/10.1099/vir.0.19415-0&mimeType=html&fmt=ahah

References

  1. Bomsel, M. ( 1997; ). Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med 3, 42–47.[CrossRef]
    [Google Scholar]
  2. Bruyère, A., Brault, V., Ziegler-Graff, V., Simonis, M. T., van den Heuvel, J. F. J. M., Richards, K., Guilley, H., Jonard, G. & Herrbach, E. ( 1997; ). Effects of mutations in the beet western yellows virus readthrough protein on its expression and packaging and on virus accumulation, symptoms, and aphid transmission. Virology 230, 323–334.[CrossRef]
    [Google Scholar]
  3. Clark, M. F. & Adams, A. N. ( 1977; ). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34, 475–483.[CrossRef]
    [Google Scholar]
  4. Eskandari, F., Sylvester, E. S. & Richardson, J. ( 1979; ). Evidence for lack of propagation of potato leafroll virus in its aphid vector, Myzus persicae. Phytopathology 69, 45–47.[CrossRef]
    [Google Scholar]
  5. Garret, A., Kerlan, C. & Thomas, D. ( 1993; ). The intestine is a site of passage for potato leafroll virus from the gut lumen to the haemocoel in the aphid vector, Myzus persicae Sulz. Arch Virol 131, 377–392.[CrossRef]
    [Google Scholar]
  6. Gildow, F. E. ( 1982; ). Coated vesicle transport of luteovirus through the salivary gland of Myzus persicae. Phytopathology 72, 1289–1296.[CrossRef]
    [Google Scholar]
  7. Gildow, F. E. ( 1985; ). Transcellular transport of barley yellow dwarf virus into the haemocoel of the aphid vector, Rhopalosiphum padi. Phytopathology 75, 292–297.[CrossRef]
    [Google Scholar]
  8. Gildow, F. E. ( 1987; ). Virus-membrane interactions involved in circulative transmission of luteoviruses by aphids. Curr Top Vector Res 4, 93–120.
    [Google Scholar]
  9. Gildow, F. E. ( 1993; ). Evidence for receptor-mediated endocytosis regulating luteovirus acquisition by aphids. Phytopathology 83, 270–277.[CrossRef]
    [Google Scholar]
  10. Gildow, F. E. ( 1999; ). Luteovirus transmission and mechanisms regulating vector specificity. In The Luteoviridae, pp. 88–113. Edited by H. G. Smith & H. Barker. Wallingford: CAB International.
  11. Gildow, F. E. & Gray, S. ( 1993; ). The aphid salivary gland basal lamina as a selective barrier associated with vector-specific transmission of barley yellow dwarf luteovirus. Phytopathology 83, 1293–1302.[CrossRef]
    [Google Scholar]
  12. Gildow, F. E. & Rochow, W. F. ( 1980; ). Role of accessory salivary glands in aphid transmission of barley yellow dwarf virus. Virology 104, 97–108.[CrossRef]
    [Google Scholar]
  13. Gildow, F. E., Damsteegt, V. D., Stone, A. L., Smith, O. P. & Gray, S. M. ( 2000; ). Virus–vector cell interactions regulating transmission specificity of soybean dwarf luteoviruses. J Phytopathol 148, 333–342.[CrossRef]
    [Google Scholar]
  14. Guilley, H., Wipf-Scheibel, C., Richards, K., Lecoq, H. & Jonard, G. ( 1994; ). Nucleotide sequence of cucurbit aphid-borne yellows luteovirus. Virology 202, 1012–1017.[CrossRef]
    [Google Scholar]
  15. Harrewijn, P. ( 1983; ). The effect of cultural measures on behaviour and population development of potato aphids and transmission of viruses. Meded Fac Landbouwwet Rijksuniv Gent 48, 791–799.
    [Google Scholar]
  16. Herrbach, E. ( 1999; ). Introduction of vector–virus interactions. In The Luteoviridae, pp. 85–88. Edited by H. G. Smith & H. Barker. Wallingford: CAB International.
  17. Lecoq, H., Bourdin, D., Wipf-Scheibel, C., Bon, M., Lot, H., Lemaire, O. & Herrbach, E. ( 1992; ). A new yellowing disease of cucurbits caused by a luteovirus, cucurbit aphid-borne yellows virus. Plant Pathol 41, 749–761.[CrossRef]
    [Google Scholar]
  18. Lemaire, O., Gubler, W. D., Valencia, J., Lecoq, H. & Falk, B. W. ( 1993; ). First report of cucurbit aphid-borne yellows luteovirus in the United States. Plant Dis 77, 1169.
    [Google Scholar]
  19. Lett, J.-M., Granier, M., Hippolyte, I., Grondin, M., Royer, M., Blanc, S., Reynaud, B. & Peterschmitt, M. ( 2002; ). Spatial and temporal distribution of geminiviruses in leafhoppers of the genus Cicadulina monitored by conventional and quantitative polymerase chain reaction. Phytopathology 92, 65–74.[CrossRef]
    [Google Scholar]
  20. Mayo, M. A. & D'Arcy, C. J. ( 1999; ). Family Luteoviridae: a reclassification of luteoviruses. In The Luteoviridae, pp. 15–22. Edited by H. G. Smith & H. Barker. Wallingford: CAB International.
  21. Mayo, M. A. & Ziegler-Graff, V. ( 1996; ). Molecular biology of luteoviruses. Adv Virus Res 46, 413–460.
    [Google Scholar]
  22. Mostov, K. E. Verges M. & Altschuler, Y. ( 2000; ). Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol 12, 483–490.[CrossRef]
    [Google Scholar]
  23. O'Loughlin, G. T. & Chambers, T. C. ( 1972; ). Extracellular microtubules in the aphid gut. J Cell Biol 53, 575–578.[CrossRef]
    [Google Scholar]
  24. Pastan, I. & Willingham, M. C. ( 1985; ). The pathway of endocytosis. In Endocytosis, pp. 1–44. Edited by I. Pastan & M. C. Willingham. New York: Plenum Press.
  25. Ponsen, M. B. ( 1977; ). Anatomy of an aphid vector: Myzus persicae. In Aphids as Virus Vectors, pp. 63–82. Edited by K. F. Harris & K. Maramorosch. New York: Academic Press.
  26. Prüfer, D., Wipf-Scheibel, C., Richards, K., Guilley, H., Lecoq, H. & Jonard, G. ( 1995; ). Synthesis of a full-length infectious cDNA clone of cucurbit aphid-borne yellows virus and its use in gene exchange experiments with structural proteins from other luteoviruses. Virology 214, 150–158.[CrossRef]
    [Google Scholar]
  27. Reinbold, C., Gildow, F. E., Herrbach, E., Ziegler-Graff, V., Gonçalves, M. C., van den Heuvel, J. F. J. M. & Brault, V. ( 2001; ). Studies on the role of the minor capsid protein in the transport of Beet western yellows virus through Myzus persicae. J Gen Virol 82, 1995–2007.
    [Google Scholar]
  28. Reutenauer, A., Ziegler-Graff, V., Lot, H., Scheidecker, D., Guilley, H., Richards, K. & Jonard, G. ( 1993; ). Identification of beet western yellows luteovirus genes implicated in viral replication and particle morphogenesis. Virology 195, 692–699.[CrossRef]
    [Google Scholar]
  29. Roth, M. G. ( 1993; ). Endocytic receptors. Adv Cell Mol Biol Membranes 1, 19–50.
    [Google Scholar]
  30. Sieczkarski, S. B. & Whittaker, G. R. ( 2002; ). Dissecting virus entry via endocytosis. J Gen Virol 83, 1535–1545.
    [Google Scholar]
  31. Smith, G. R., Borg, Z., Lockhart, B. L., Braithwait, K. S. & Gibbs, M. ( 2000; ). Sugarcane yellow leaf virus: a novel member of the Luteoviridae that probably arose by inter-species recombination. J Gen Virol 81, 1865–1869.
    [Google Scholar]
  32. Tamada, T. & Harrison, B. D. ( 1981; ). Quantitative studies on the uptake and retention of potato leafroll virus by aphids in laboratory and field conditions. Ann Appl Biol 98, 261–276.[CrossRef]
    [Google Scholar]
  33. van den Heuvel, J. F. J. M., Boerma, T. M. & Peters, D. ( 1991; ). Transmission of potato leafroll virus from plants and artificial diets by Myzus persicae. Phytopathology 81, 150–154.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19415-0
Loading
/content/journal/jgv/10.1099/vir.0.19415-0
Loading

Data & Media loading...

Most Cited This Month

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