1887

Abstract

A fasting period prior to non-circulative virus acquisition has been shown to increase the rate of transmission by aphids. However, this effect has only been studied for a few virus–vector combinations, and there are contradictory results in the literature as to the role of fasting on virus acquisition. We analysed the influence of fasting on the transmission of three non-circulative viruses, , and , by two aphid vector species: Sulzer (Hemiptera: Aphididae) and Glover (Hemiptera: Aphididae). All variables tested, including the virus species and isolate, and the species of aphid, influenced the effect of a fasting period on virus transmission efficiency. Furthermore, when aphids were subjected to an overnight feeding period on a sucrose solution, the fasting effect disappeared and the probing behaviour of these aphids was markedly different to plant-reared aphids. The electrical penetration graph (EPG) technique revealed that fasting altered the probing behaviour of and , with fasted aphids beginning to feed sooner and having a significantly longer first intracellular puncture, measured as a potential drop. Significantly longer sub-phase II-3 of the potential drop and more archlets during this sub-phase were also observed for fasted aphids of both species. However, these behavioural changes were not predictive of increasing virus transmission following a fasting period. The impacts of pre-acquisition fasting on aphid probing behaviour and on the mechanisms of non-circulative virus transmission are discussed.

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2017-12-01
2020-01-25
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References

  1. Watson MA. F Further studies on the relationship between hyoscyamus virus 3 and the aphid Myzus persicae (Sulz.) with special reference to the effects of fasting. Proc R Soc Lond B 1938;125:144–170 [CrossRef]
    [Google Scholar]
  2. Watson MA, Roberts FM. A Comparative study of the transmission of hyoscyamus virus 3, potato virus y and cucumber virus 1 by the vectors Myzus persicae (Sulz), M. circumflexus (Buckton), and Macrosiphum gei (Koch). Proc R Soc London B 1939;127:543–576 [CrossRef]
    [Google Scholar]
  3. Cockbain AJ, Gibbs AJ, Heathcote GD. Some factors affecting the transmission of sugar-beet mosaic and pea mosaic viruses by Aphis fubue and Myzus persicae. Ann Appl Biol 1963;52:133–143 [CrossRef]
    [Google Scholar]
  4. Day MF, Irzykiewicz H. On the mechanism of transmission of non-persistent phytopathogenic viruses by aphids. Aust J Biol Sci 1954;7:251–261 [CrossRef][PubMed]
    [Google Scholar]
  5. Sylvester ES. Serial transmission of beet-mosaic virus by the green peach aphid. Phytopathology 1950;40:737–742
    [Google Scholar]
  6. Sylvester ES. Lettuce mosaic virus transmission by the green peach aphid. Phytopathology 1955;45:357–370
    [Google Scholar]
  7. Watson MA. The transmission of beet mosaic and beet yellows viruses by aphides; a comparative study of a nonpersistent and a persistent virus having host plants and vectors in common. Proc R Soc Med 1946;133:200–219 [CrossRef][PubMed]
    [Google Scholar]
  8. Hamlyn BMG. Quantitative studies on the transmission of cabbage black ring spot virus by Myzus persicae (Sulz.). Ann Appl Biol 1953;40:393–402 [CrossRef]
    [Google Scholar]
  9. Powell G. The effect of pre-acquisition starvation on aphid transmission of potyviruses during observed and electrically recorded stylet penetrations. Entomol Exp Appl 1993;66:255–260 [CrossRef]
    [Google Scholar]
  10. Fereres A, Blua MJ, Perring TM. Retention and transmission characteristics of zucchini yellow mosaic virus by Aphis gossypii and Myzus persicae (Homoptera: Aphididae). J Econ Entomol 1992;85:759–765 [CrossRef]
    [Google Scholar]
  11. Hamlyn BMG. Aphid transmission of cauliflower mosaic on turnips. Plant Pathol 1955;4:13–16 [CrossRef]
    [Google Scholar]
  12. Martini C. Eine Herkunft des Blumenkohlmosaikavirus (Cauliflower mosaic virus) aus der Umgebung von Bonn. Z PflKrankh Pflpath PflSchutz 1956;63:577–583
    [Google Scholar]
  13. Wang RY, Pirone TP. Potyvirus transmission is not increased by pre-acquisition fasting of aphids reared on artificial diet. J Gen Virol 1996;77:3145–3148 [CrossRef][PubMed]
    [Google Scholar]
  14. Bradley RHE. Studies on the aphid transmission of a strain of henbane Mosaic virus. Ann Appl Biol 1952;39:78–97 [CrossRef]
    [Google Scholar]
  15. Bradley RH. Effects of depth of stylet penetration on aphid transmission of Potato virus Y. Can J Microbiol 1956;2:539–547 [CrossRef][PubMed]
    [Google Scholar]
  16. Collar JL, Fereres A. Nonpersistent virus transmission efficiency determined by aphid probing behavior during intracellular punctures. Environ Entomol 1998;27:583–591 [CrossRef]
    [Google Scholar]
  17. Tjallingii WF. Mechanoreceptors of the aphid labium. Entomol Exp Appl 1978;24:731–737 [CrossRef]
    [Google Scholar]
  18. Collar JL, Avilla C, Martin B, Duque M, Fereres A. Non-persistent virus transmission studied through aphid probing behaviour. [Spanish]. Boletin de Sanidad Vegetal, Plagas 1998;24:687–694
    [Google Scholar]
  19. Martín B, Collar JL, Tjallingii WF, Fereres A. Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. J Gen Virol 1997;78:2701–2705 [CrossRef][PubMed]
    [Google Scholar]
  20. Powell G, Pirone T, Hardie J. Aphid stylet activities during potyvirus acquisition from plants and an in vitro system that correlate with subsequent transmission. Eur J Plant Pathol 1995;101:411–420 [CrossRef]
    [Google Scholar]
  21. Palacios I, Drucker M, Blanc S, Leite S, Moreno A et al. Cauliflower mosaic virus is preferentially acquired from the phloem by its aphid vectors. J Gen Virol 2002;83:3163–3171 [CrossRef][PubMed]
    [Google Scholar]
  22. Symmes EJ, Walker GP, Perring TM. Stylet penetration behavior of Myzus persicae related to transmission of Zucchini yellow mosaic virus. Entomol Exp Appl 2008;129:258–267 [CrossRef]
    [Google Scholar]
  23. Collar JL, Avilla C, Fereres A. New correlations between aphid stylet paths and nonpersistent virus transmission. Environ Entomol 1997;26:537–544 [CrossRef]
    [Google Scholar]
  24. Swenson KG. Bean yellow mosaic virus transmission by Myzus persicae. Aust J Biol Sci 1962;15:468–482 [CrossRef]
    [Google Scholar]
  25. Shukle RH. Aphid feeding behavior: relationship to barley yellow dwarf virus resistance in Agropyron Species. Phytopathology 1987;77:725–729 [CrossRef]
    [Google Scholar]
  26. Symmes EJ, Perring TM. Intraspecific variation in zucchini yellow mosaic virus transmission by Myzus persicae and the impact of aphid host plant. J Econ Entomol 2007;100:1764–1772 [CrossRef][PubMed]
    [Google Scholar]
  27. Krenz B, Bronikowski A, Lu X, Ziebell H, Thompson JR et al. Visual monitoring of Cucumber mosaic virus infection in Nicotiana benthamiana following transmission by the aphid vector Myzus persicae. J Gen Virol 2015;96:2904–2912 [CrossRef][PubMed]
    [Google Scholar]
  28. Tjallingii WF. Electrical recording of stylet penetration activities. In Minks AK, Harrewijn PJ. (editors) Aphids: Their Biology Nature Enemies and Control Amsterdam: Elsevier; 1988; pp.95–108
    [Google Scholar]
  29. Carroll JE, Smith DM, Gray SM. Preferential acquisition and inoculation of PVYNTN over PVYO in potato by the green peach aphid Myzus persicae (Sulzer). J Gen Virol 2016;97:797–802 [CrossRef][PubMed]
    [Google Scholar]
  30. Fereres A, Raccah B. Plant virus transmission by insects. In eLS Chichester: John Wiley & Sons, Ltd; 2015; pp.1–12
    [Google Scholar]
  31. Fereres A, Moreno A. Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 2009;141:158–168 [CrossRef][PubMed]
    [Google Scholar]
  32. Wang RY, Powell G, Hardie J, Pirone TP. Role of the helper component in vector-specific transmission of potyviruses. J Gen Virol 1998;79:1519–1524 [CrossRef][PubMed]
    [Google Scholar]
  33. Mauck KE, de Moraes CM, Mescher MC. Effects of pathogens on sensory-mediated interactions between plants and insect vectors. Curr Opin Plant Biol 2016;32:53–61 [CrossRef][PubMed]
    [Google Scholar]
  34. Uzest M, Gargani D, Dombrovsky A, Cazevieille C, Cot D et al. The “acrostyle”: a newly described anatomical structure in aphid stylets. Arthropod Struct Dev 2010;39:221–229 [CrossRef][PubMed]
    [Google Scholar]
  35. Villada ES, González EG, López-Sesé AI, Castiel AF, Gómez-Guillamón ML. Hypersensitive response to Aphis gossypii Glover in melon genotypes carrying the Vat gene. J Exp Bot 2009;60:3269–3277 [CrossRef][PubMed]
    [Google Scholar]
  36. Chen J-Q, Martin B, Rahbé Y, Fereres A. Early intracellular punctures by two aphid species on near-isogenic melon lines with and without the virus aphid transmission (Vat) resistance gene. Eur J Plant Pathol 1997;103:521–536 [CrossRef]
    [Google Scholar]
  37. Labonne G, Quiot JB. Aphids can acquire plum pox virus from infected fruits. Acta Hortic 2001;550:79–84 [CrossRef]
    [Google Scholar]
  38. Lecoq H. Resistance to cucumber mosaic virus transmission by aphids in Cucumis melo. Phytopathology 1979;69:1223–1225 [CrossRef]
    [Google Scholar]
  39. Desbiez C, Gal-On A, Girard M, Wipf-Scheibel C, Lecoq H. Increase in zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology 2003;93:1478–1484 [CrossRef][PubMed]
    [Google Scholar]
  40. Perry KL, Zhang L, Palukaitis P. Amino acid changes in the coat protein of cucumber mosaic virus differentially affect transmission by the aphids Myzus persicae and Aphis gossypii. Virology 1998;242:204–210 [CrossRef][PubMed]
    [Google Scholar]
  41. van Munster M, Yvon M, Vile D, Dader B, Fereres A et al. Water deficit enhances the transmission of plant viruses by insect vectors. PLoS One 2017;12:e0174398 [CrossRef][PubMed]
    [Google Scholar]
  42. Powell G. Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Ann Appl Biol 1991;119:313–321 [CrossRef]
    [Google Scholar]
  43. Abacus Concepts Statview: The Ultimate Integrated Data Analysis and Presentation System: For the Macintosh: Version 4.0 1992
    [Google Scholar]
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