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The intestine is a site of passage for potato leafroll virus from the gut lumen into the haemocoel in the aphid vector,Myzus persicae Sulz

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Summary

Four detection techniques, three of which gave reliable identification of the virus particles, were used to locate potato leafroll virus (PLRV) in the alimentary canal of its main aphid vector,Myzus persicae Sulz: immunofluorescence on cryostat sections, conventional transmission electron microscopy on ultrathin sections and immune electron microscopy with gold labeling, either prior to or after fixation-embedding. Each method clearly showed the presence of the virus in the intestine epithelium and its absence in cells of the other parts of the alimentary canal. Under the experimental conditions used, the intestinal cells seemed to be the pathway for PLRV transport from the gut lumen into the haemocoel. Electron microscopy examinations showed many virus particles close to the apical plasmalemma of the epithelial cells in the gut lumen of the intestine. Other particles were seen in shallow pit-like regions or surrounded by coated vesicles in the apical part of these cells. Thus the virus particles seemed to enter the epithelial cells of the intestine by a mechanism of endocytosis. In the cytoplasm of these cells, virions were also frequently observed in isolated — or more often aggregated — tubular vesicles. The latter could be involved in PLRV transport through the cell since they were observed fusing with different cell organelles. A few viral particles were also detected in lysosomes as well as in multivesicular bodies. Virus particles were observed between the plasmalemma and basal lamina of the intestine cells but not in the haemocoel, where probably they were quickly dispersed. Our results are discussed in relation to other reports which have shown hindgut and stomach as sites of passage from the gut lumen into the aphid's body cavity for PLRV and other circulative viruses.

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References

  1. Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay (ELISA) for the detection of plant viruses. J Gen Virol 34: 475–483

    PubMed  Google Scholar 

  2. Debruyn PP, Michelson S, Becker RP (1975) Endocytosis, transfer tubules, and lysosomal activity in myeloid sinusoidal endothelium. J Ultrastruct Res 53: 133–151

    PubMed  Google Scholar 

  3. Eskandari F, Sylvester ES, Richardson J (1979) Evidence for lack of propagation of potato leafroll virus in its aphid vector,Myzus persicae. Phytopathology 69: 45–47

    Google Scholar 

  4. Garret A, Kerlan C, Thomas D (1991) Visualization of a luteovirus in the vector aphid's body by two gold immunolabelling techniques: a comparative study. J Virol Methods 35: 93–107

    PubMed  Google Scholar 

  5. Gildow FE (1982) Coated-vesicle transport of luteoviruses through salivary glands ofMyzus persicae. Phytopathology 72: 1289–1296

    Google Scholar 

  6. Gildow FE (1985) Transcellular transport of barley yellow dwarf virus into the haemocoel of the aphid vector,Rhopalosiphum padi. Phytopathology 75: 292–297

    Google Scholar 

  7. Gildow FE (1987) Virus-membrane interactions involved in circulative transmission of luteoviruses by aphids. In: Harris KF (ed) Current topics in vector research, vol 4. Springer, Berlin Heidelberg New York Tokyo, pp 93–120

    Google Scholar 

  8. Gildow FE, Rochow WF (1980 a) Role of accessory salivary glands in aphid transmission of barley yellow dwarf virus. Virology 104: 97–108

    Google Scholar 

  9. Gildow FE, Rochow WF (1980 b) Importance of capsid integrity for interference between two isolates of barley yellow dwarf virus inMacrosiphum avenae. Phytopathology 70: 1013–1015

    Google Scholar 

  10. Hardy JL, Houk EJ, Kramer LD, Reeves WC (1983) Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28: 229–262

    PubMed  Google Scholar 

  11. Harris KF (1979) Leafhoppers and aphids as biological vectors: vector virus relationships. In: Maramorosch K, Harris KF (ed) Leafhopper vectors and plant disease agents. Academic Press, New York, pp 217–308

    Google Scholar 

  12. Harris KF, Bath JE (1972) The fate of pea enation mosaic virus in the pea aphid vectorAcyrthosiphum pisum (Harris). Virology 50: 778–790

    PubMed  Google Scholar 

  13. Harrison BD (1984) Potato leafroll virus. CMI/AAB Descriptions of Plant Viruses, no 291

  14. Kitajima EW (1976) Isometric virus-like particles in the green peach aphidMyzus persicae. J Invertebr Pathol 28: 1–10

    Google Scholar 

  15. Levine JS, Nakane PK, Allen RH (1981) Human intrinsic factor secretion: immunochemical demonstration of membrane-associated vesicular transport in parietal cells. J Cell Biol 90: 644–655

    PubMed  Google Scholar 

  16. Murphy FA, Whitefield SG, Sudia WD, Chamberlain RW (1975) Interactions of vector with vertebrate pathogenic viruses. In: Maramorosch K, Shope RE (eds) Invertebrate immunity. Academic Press, New York, pp 25–48

    Google Scholar 

  17. Peters D (1965) The purification of virus-like particles from the aphidMyzus persicae. Virology 26: 159–161

    PubMed  Google Scholar 

  18. Peters D (1967) Potato leafroll virus, its purification from its vectorMyzus persicae. Meded Fonds Landb Exp Bur 45: 1–100

    Google Scholar 

  19. Ponsen MB (1987) Alimentary tract. In: Minks AK, Harrewijn P (eds) Aphids, their biology, natural enemies, and control, vol 2A. Elsevier, Amsterdam, pp 79–87

    Google Scholar 

  20. Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17: 208–212

    PubMed  Google Scholar 

  21. Robert Y, Maury Y (1970) Capacités vectrices comparées de plusieurs souches deMyzus persicae Sulz,Aulacorthum solani Kltb. etMacrosiphum euphorbiae Thomas dans l'étude de la transmission de l'enroulement de la pomme de terre. Potato Res 13: 199–209

    Google Scholar 

  22. Rochow WF, Gill CC (1978) Dependent virus transmission byRhopalosiphum padi from mixed infections of various isolates of barley yellow dwarf virus. Phytopathology 68: 451–456

    Google Scholar 

  23. Rodevald R (1980) Distribution of immunoglobulin G receptors in the small intestine of the young rat. J Cell Biol 85: 18–32

    PubMed  Google Scholar 

  24. Shikata E, Maramorosch K, Granados RR (1966) Electron microscopy of pea enation mosaic virus in plants and aphid vectors. Virology 29: 426–436

    PubMed  Google Scholar 

  25. Sylvester ES (1980) Circulative and propagative viruses. Transmission by aphids. Annu Rev Entomol 25: 257–286

    Google Scholar 

  26. Takanami Y, Kubo S (1979) Enzyme-assisted purification of two phloem-limited plant viruses: tobacco necrotic dwarf and potato leafroll. J Gen Virol 44: 153–159

    Google Scholar 

  27. Weidemann HL (1982) Zur Vermehrung des Kartoffelblattrollvirus in der BlattlausMyzus persicae (Sulz). Z Ang Ent 94: 321–330

    Google Scholar 

  28. Whitefield SG, Murphy FA, Sudia WD (1973) St Louis encephalitis virus: an ultrastructural study of infection in a mosquito vector. Virology 56: 70–87

    PubMed  Google Scholar 

  29. Whitehouse RL, Benichou JC, Couture-Tosi E, Schenkman S, Ryter A (1984) Immunolabeling of bacteriophage lambda receptor protein (Lam B) on thin sections ofE. coli embedded in Lowicryl. Biol Cell 51: 389–394

    PubMed  Google Scholar 

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Garret, A., Kerlan, C. & Thomas, D. The intestine is a site of passage for potato leafroll virus from the gut lumen into the haemocoel in the aphid vector,Myzus persicae Sulz. Archives of Virology 131, 377–392 (1993). https://doi.org/10.1007/BF01378639

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  • DOI: https://doi.org/10.1007/BF01378639

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