1887

Abstract

(CaMV) is transmitted in a non-circulative manner by aphids following the helper strategy. Helper proteins P2 and P3 act as a bridge between virions and the aphid cuticle. Electronic monitoring of aphid stylet activities (EPG technique), transmission tests and electron microscopy showed that CaMV is preferentially acquired from the phloem by its most common aphid vectors, and . We also found that CaMV is semipersistently transmitted and that the rate of acquisition does not follow a typical bimodal curve. Instead, the virus could be acquired from non-phloem tissues at a low and fairly constant rate after one or more intracellular punctures within a few minutes, but the probability of acquisition rose significantly when aphids reached the phase of committed ingestion from the phloem. The acquisition rate of CaMV did not increase with increasing number of intracellular punctures, but the total duration of intracellular puncture was one of the variables selected by the stepwise logistic regression model used to fit the data that best explained acquisition of CaMV. Furthermore, aphids reaching the phloem faster had a higher probability of acquiring the virus. Our results support the hypothesis that multiple intracellular punctures of epidermal and mesophyll cells result in loading aphids with the CaMV-encoded aphid transmission factor (P2), and that aphids, in most cases, subsequently acquire CaMV particles during phloem sap ingestion. Consistently, immunoelectron microscopy showed that P3–virions are frequently found in the sieve element lumen, whereas P2 could not be detected.

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2002-12-01
2019-10-23
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References

  1. Abacus Concepts (1989). Statview II. Berkeley, CA: Abacus Concepts.
  2. Afifi, A. A. & Clark, V. (1990). Computer-aided Multivariate Analysis, 2nd edn. Belmont, CA: Lifetime Learning Publications.
  3. Ammar, E. D. & Nault, L. R. ( 1991; ). Maize chlorotic dwarf virus-like particles associated with the foregut in vector and nonvector leafhopper species. Phytopathology 81, 444-448.[CrossRef]
    [Google Scholar]
  4. Blanc, S., Hébrard, E., Drucker, M. & Froissart, R. ( 2001; ). Molecular basis of vector transmission: caulimoviruses. In Virus–Insect–Plant Interactions , pp. 143-166. Edited by K. Harris, O. P. Smith & J. E. Duffus. San Diego, CA:Academic Press.
  5. Bouchery, Y., Givord, L. & Monestiez, P. ( 1990; ). Comparison of short-and long-feed transmission of the cauliflower mosaic virus Cabb-S strain and S delta II hybrid by two species of aphid: Myzus persicae (Sulzer) and Brevicoryne brassicae (L.). Research in Virology 141, 677-683.[CrossRef]
    [Google Scholar]
  6. Broadbent, L. ( 1957; ). Investigation of virus diseases of brassica crops. In Agricultural Research Council Report Series , pp. 99. Edited by L. Broadbent. Cambridge, UK:Cambridge University Press.
  7. Chalfant, R. B. & Chapman, R. K. ( 1962; ). Transmission of cabbage viruses A and B by the cabbage aphid and the green peach aphid. Journal of Economic Entomology 55, 584-590.[CrossRef]
    [Google Scholar]
  8. Childress, S. A. & Harris, K. F. ( 1989; ). Localization of virus-like particles in the foreguts of viruliferous Graminella nigrifrons leafhoppers carrying the semi-persistent maize chlorotic dwarf virus. Journal of General Virology 70, 247-251.[CrossRef]
    [Google Scholar]
  9. Cole, R. A. ( 1994; ). Locating a resistance mechanism to the cabbage aphid in two wild brassicas. Entomologia Experimentalis et Applicata 71, 23-31.[CrossRef]
    [Google Scholar]
  10. Collar, J. L., Avilla, C. & Fereres, A. ( 1997; ). New correlations between aphid stylet paths and nonpersistent virus transmission. Environmental Entomology 26, 537-544.[CrossRef]
    [Google Scholar]
  11. Drucker, M., Froissart, R., Hébrard, E., Uzest, M., Ravallec, M., Espérandieu, P., Mani, J.-C., Pugnière, M., Roquet, F., Fereres, A. & Blanc, S. ( 2002; ). Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector. Proceedings of the National Academy of Sciences, USA 99, 2422-2427.[CrossRef]
    [Google Scholar]
  12. Esau, K., Cronshaw, J. & Hoefert, L. L. ( 1967; ). Organization of beet yellows virus inclusions in leaf cells of beta. Proceedings of the National Academy of Sciences, USA 55, 486-493.
    [Google Scholar]
  13. Espinoza, A. M., Medina, V., Hull, R. & Markham, P. G. ( 1991; ). Cauliflower mosaic virus gene II product forms distinct inclusion bodies in infected plant cells. Virology 185, 337-344.[CrossRef]
    [Google Scholar]
  14. Febvay, G., Rahbé, Y. & van Helden, M. ( 1996; ). MacStylet, software to analyse electrical penetration graph data on the Macintosh. Entomologia Experimentalis et Applicata 80, 105-108.[CrossRef]
    [Google Scholar]
  15. Fereres, A. & Collar, J. L. (2001). Analysis of noncirculative transmission by electrical penetration graphs. In Virus-insect-plant interactions. Edited by K. F. Harris, O. P. Smith & J. E. Duffus. San Diego, CA: Academic Press.
  16. Fereres, A., Perez, P., Gemeno, C. & Ponz, F. ( 1993; ). Transmission of spanish pepper and potato PPY isolates by aphid (homoptera: aphididae) vectors: epidemiological implications. Environmental Entomology 22, 1260-1265.[CrossRef]
    [Google Scholar]
  17. Franck, A., Guilley, H., Jonard, J., Richards, K. & Hirth, L. ( 1980; ). Nucleotide sequence of cauliflower mosaic virus DNA. Cell 21, 285-294.[CrossRef]
    [Google Scholar]
  18. Francki, R. I. B., Milne, R. N. & Hatta, T. (1985). Caulimovirus group. In Atlas of Plant Viruses, pp. 17–32. San Diego: Academic Press.
  19. Gibbs, A. J. & Gower, J. C. ( 1960; ). The use of a multiple-transfer method in plant virus transmission studies: some statistical points arising in the analysis of results. Annals of Applied Biology 48, 75-83.[CrossRef]
    [Google Scholar]
  20. Gray, S. M. & Banerjee, N. ( 1999; ). Mechanisms of arthropod transmission of plant and animal viruses. Microbiology and Molecular Biology Reviews 63, 128-148.
    [Google Scholar]
  21. Hamlyn, B. M. G. ( 1955; ). Aphid transmission of cauliflower mosaic on turnips. Plant Pathology 4, 13-16.[CrossRef]
    [Google Scholar]
  22. Hull, R. (2001). Matthews’ Plant Virology, 4th edn. San Diego: Academic Press.
  23. Kennedy, J. S., Day, M. F. & Eastop, V. F. (1962). A Conspectus of Aphids as Vectors of Plant Viruses. London: Commonwealth Institute of Entomology.
  24. Kitajima, E. W., Lauritis, J. A. & Swift, H. ( 1969; ). Fine structure of zinnial leaf tissues infected with dahlia mosaic virus. Virology 39, 240-249.[CrossRef]
    [Google Scholar]
  25. Leh, V., Jacquot, E., Geldreich, A., Hermann, T., Leclerc, D., Cerrutti, M., Yot, P., Keller, M. & Blanc, S. ( 1999; ). Aphid transmission of cauliflower mosaic virus requires the viral PIII protein. EMBO Journal 18, 7077-7085.[CrossRef]
    [Google Scholar]
  26. Leh, V., Jacquot, E., Geldreich, A., Haas, M., Blanc, S., Keller, M. & Yot, P. ( 2001; ). Interaction between cauliflower mosaic virus ORFIII product and the coat protein is required for transmission of the virus by aphids. Journal of Virology 75, 100-106.[CrossRef]
    [Google Scholar]
  27. Lim, W. L. & Hagedorn, D. J. ( 1977; ). Bimodal transmission of plant virus. In Aphids as Virus Vectors , pp. 237-251. Edited by K. F. Harris & K. Maramorosh. New York:Academic Press.
  28. Limburg, D. D., Mauk, P. A. & Godfrey, L. D. ( 1997; ). Characteristics of beet yellows closterovirus transmission to sugar beets by Aphis fabae. Phytopathology 87, 766-771.[CrossRef]
    [Google Scholar]
  29. López-Abella, D., Bradley, L. R. & Harris, K. F. ( 1988; ). Correlation between stylets paths made during superficial probing and the ability of aphids to transmit nonpersistent viruses. Advances in Disease Vector Research 5, 251-285.
    [Google Scholar]
  30. Markham, P. G., Pinner, M. S., Raccah, B. & Hull, R. ( 1987; ). The acquisition of a caulimovirus by different aphid species: comparison with a potyvirus. Annals of Applied Biology 111, 571-587.[CrossRef]
    [Google Scholar]
  31. Martin, B., Collar, J. L., Tjallingii, W. F. & Fereres, A. ( 1997; ). Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. Journal of General Virology 78, 2701-2705.
    [Google Scholar]
  32. Murant, A. F., Roberts, I. M. & Elnagar, S. ( 1976; ). Association of virus-like particles with the foregut of the aphid Cavariella aegpodii transmitting the semipersistent viruses anthriscus yellows and parsnip yellow fleck. Journal of General Virology 31, 47-57.[CrossRef]
    [Google Scholar]
  33. Pirone, T. & Blanc, S. ( 1996; ). Helper-dependent vector transmission of plant viruses. Annual Review of Phytopathology 34, 227-247.[CrossRef]
    [Google Scholar]
  34. Powell, G., Pirone, T. P. & Hardie, J. (1995). Aphid stylet activities during potyvirus acquisition from plants and in vitro systems that correlate with subsequent transmission. European Journal of Plant Pathology, 411–420.
  35. Prado, E. & Tjallingii, W. F. ( 1994; ). Aphid activities during sieve element punctures. Entomologia Experimentalis et Applicata 72, 157-165.[CrossRef]
    [Google Scholar]
  36. Reese, J. C., Tjallingii, W. F., van Helden, M. & Prado, E. (2000). Waveform comparisons among AC and DC electronic monitoring systems for aphid (homoptera: Aphididae) feeding behaviour. In Principles and Applications of Electronic Monitoring and other Techniques in the Study of Homopteran Feeding Behaviour, pp. 70–101. Edited by G. P. Walker & E. A. Backus: Thomas Say Publications in Entomology.
  37. SAS Institute (1996). SAS/STAT software: changes and enhancements through release 6.11. Cary, NC: SAS Institute.
  38. SPSS (2001). SPSS statistical package. Chicago, Il: SPSS.
  39. Tjallingii, W. F. ( 1990; ). Continuous recording of stylet penetration activities by aphids. In Aphid–Plant Genotype Interactions , pp. 89-99. Edited by R. K. Campell & R. D. Eikenbary. Amsterdam:Elsevier.
  40. Tjallingii, W. F. & Prado, E. ( 2001; ). Analysis of circulative transmission by electrical penetration graphs. In Virus–Insect–Plant Interactions , pp. 69-85. Edited by K. F. Harris, O. P. Smith & J. E. Duffus. San Diego, CA:Academic Press.
  41. van Hoof, H. A. (1958). An investigation of the biological transmission of a nonpersistent virus. In Meded. Inst. Planteziektenkundig. Alkmaar: Wageningen Agricultural University, The Netherlands.
  42. Woolston, C. J., Czaplewski, L. G., Markham, P. G., Goad, A. S., Hull, R. & Davies, J. W. ( 1987; ). Location and sequence of a region of cauliflower mosaic virus gene II responsible for aphid transmissibility. Virology 160, 246-251.[CrossRef]
    [Google Scholar]
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