Abstract
The behavioural events associated with acquisition of tobacco etch potyvirus by starvedMyzus persicae during single, electrically-recorded penetrations of plants or a Parafilm membrane were compared. Twenty nine percent of aphids acquired virus from plants and subsequently transmitted to test plants. Stylet puncture of the plasmalemma, indicated by a potential drop (pd) to the intracellular signal voltage level, occurred during 84% of penetrations, and virus transmission was always associated with this behavioural event during acquisition. Periods of intracellular stylet tip location, known as pd phase II, ranged from 3.6–12.2s, and always comprised three consecutive sub-phases, designated II1, II2 and II3. Ninety six percent of pds included distinct pulses during phase II3. A waveform which closely resembled these pulses was produced by 59% of aphids that probed a virus suspension through a Parafilm membrane; nineteen percent of the aphids subsequently transmitted membrane-acquired virus and transmission was significantly associated with the occurrence of the phase II3-like pulses during acquisition. The duration of occurrence of recorded phase II3 pulses, either on plants or thein vitro system, did not influence the virus transmission efficiency of aphids. The association of virus uptake from aqueous suspension with a particular behavioural activity is discussed as evidence for the ‘ingestion-egestion’ hypothesis for nonpersistent transmission. Starved aphids acquiring virus from infected leaf tissue or thein vitro system had significantly higher transmission efficiencies than non-starved aphids. Starved and non-starved insects were electrically-recorded penetrating the artificial membrane, and again there was a clear difference in transmission efficiency (starved aphids, 26%; non-starved aphids, 2%). The higher transmission efficiency of starved insects could not be explained by behavioural differences, and the results lend support to the hypothesis that non-behavioural factors determine the enhancement of potyvirus transmission by preacquisition starvation.
Similar content being viewed by others
Abbreviations
- BMV:
-
Beet mosaic virus
- EMF:
-
Electromotive force
- HAT:
-
Highly aphid-transmissible
- HC:
-
Helper component
- pd:
-
Potential drop
- PVY:
-
Potato virus Y
- TEV:
-
Tobacco etch virus
References
Ammar ED, Jarlfors, U and Pirone TP (1994) Association of potyvirus helper component protein with virions and the cuticle lining the maxillary food canal and foregut of an aphid vector. Phytopathology 84: 1054–1060
Berger PH and Pirone TP (1986) The effect of helper component on the uptake and localization of potyviruses inMyzus persicae. Virology 153: 256–261
Bradley RHE (1964) Aphid transmission of stylet-borne viruses. In: Corbett MK and Sisler HD (eds) Plant Virology (pp. 148–174) Florida Press, Gainsville
Day MF and Irzykiewicz H (1954) On the mechanism of transmission of non-persistent phytopathogenic viruses by aphids. Aust. J. Biol. Sci. 7: 251–273
Gamez R and Watson MA (1964) Failure of anaesthetised aphids to acquire or transmit henbane mosaic virus when their stylets were artificially inserted into leaves of infected or healthy tobacco plants. Virology 22: 292–295
Govier DA and Kassanis B (1974) A virus-induced component of plant sap needed when aphids acquire potato virus Y from purified preparations. Virology 61: 420–426
Govier DA, Kassanis B and Pirone TP (1977) Partial purification and characterisation of the potato virus Y helper component. virology 78: 306–314
Hardie J, Holyoak M, Taylor NJ and Griffiths DC (1992) The combination of electronic monitoring and video-assisted observations of plant penetration by aphids and behavioural effects of polygodial. Entomol. exp. appl. 62: 233–239
Hardie J and Powell G (1995) Close-up video combined with electronic monitoring of plant penetration and behavioural effects of an aphid antifeedant. In: Walker GP and Backus EA (eds). Homopteran feeding behaviour: recent advances and experimental techniques. Thomas Say Publications in Entomology, Lanham, MD. In press
Harris KF (1977) an ingestion-egestion hypothesis of noncirculative virus transmission. In: Harris KF and Maramorosch K (eds). Aphids as Virus Vectors (pp. 165–220) Academic Press, New York
Kennedy JS, Day MF and Eastop VF (1962) A Conspectus of Aphids as Vectors of Plant Viruses. Commonwealth Agricultural Bureau
Klingauf FA (1987) Host plant finding and acceptance. In: Minks AK and Harrewijn P (eds). Aphids: Their Biology, Natural Enemies and Control. Vol. A (pp. 209–223) Elsevier, Amsterdam
Lopez-Abella D, Bradley RHE and Harris KF (1988) Correlation between the stylet paths made during superficial probing and the ability of aphids to transmit nonpersistent viruses. Adv. Dis. Vect. Res. 5: 251–285
Nault LR and Gyrisco GG (1966) Relation of the feeding process of the pea aphid to the inoculation of pea enation mosaic virus. Ann. Entomol. Soc. Am. 59: 1185–1197
Pelletier Y (1990) The role of the color of the substratum on the initiation of the probing behavior inMyzus persicae (Sulzer) andMacrosiphum euphorbiae (Thomas) (Homoptera: Aphididae). Can. J. Zool. 68: 694–698
Pirone TP (1969) Mechanism of transmission of stylet-borne viruses. In: Maramorosch K (ed) Viruses, Vectors and Vegetation (pp. 199–210) Wiley-Interscience, New York
Pirone TP (1981) Efficiency and selectivity of the helpercomponent-mediated aphid transmission of purified potyviruses. Phytopathology 71: 922–924
Pirone TP (1991) Viral genes and gene products that determine insect transmissibility. Seminars in Virology 2: 81–87
Pirone TP and Thornbury DW (1983) Role of virion and helper component in regulating aphid transmission of tobacco etch virus. Phytopathology 73: 872–875
Pirone TP and Thornbury DW (1984) The involvement of a helper component in nonpersistent transmission of plant viruses by aphids. Microbiological Sciences 1: 191–193
Pirone TP and Thornbury DW (1988) Quantity of virus required for aphid transmission of a potyvirus. Phytopathology 78: 104–107
Powell G (1991a) Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Ann. appl. Biol. 119: 313–321
Powell G (1991b) Stylet activities and potyvirus transmission by aphids. PhD Thesis (166 pp.) University of London
Powell G (1993) The effect of pre-acquisition starvation on aphid transmission of potyviruses during observed and electrically recorded stylet penetrations. Entomol. exp. appl. 66: 255–260
Powell G, Hardie J and Pickett JA (1993) Effects of the antifeedant polygodial on plant penetration by aphids, assessed by video and electrical recording. Entomol. exp. appl. 68: 193–200
Powell G, Hardie J and Pickett JA (1995) Responses ofMyzus persicae to the repellent polygodial in choice and nochoice video assays with young and mature leaf tissue. Entomol. exp. appl. 74: 91–94
Powell G, Harrington R and Spiller NJ (1992) Stylet activities and potato virus Y vector efficiencies by the aphidsBrachycaudus helichrysi andDrepanosiphum platanoidis. Entomol. exp. appl. 62: 293–300
Prado E and Tjallingii WF (1993) Aphid activities during sieve element punctures. In: Kindlmann P and Dixon AFG (eds) Critical Issues in Aphid Biology (pp. 109–112) Faculty of Biological Sciences, University of South Bohemia, Ceske Budejovice
Raccah B and Pirone TP (1984) Characteristics of and factors affecting helper-component-mediated aphid transmission of a potyvirus. Phytopathology 74: 305–308
Siegel S (1956) Nonparametric statistics for the behavioural sciences. McGraw-Hill International
Sylvester ES (1954) Aphid transmission of nonpersistent plant viruses with special reference to theBrassica nigra virus. Hilgardia 23: 53–98
Sylvester ES (1955) Lettuce mosaic virus transmission by the green peach aphid. Phytopathology 45: 357–370
Sylvester ES (1989) Viruses transmitted by aphids. In: Minks AK and Harrewijn P (eds) Aphids: Their Biology, Natural Enemies and Control. Vol. C (pp. 65–87) Elsevier, Amsterdam
Thornbury DW, Hellmann GM, Rhoads RE and Pirone TP (1985) Purification and characterization of potyvirus helper component. Virology 144: 260–267
Tjallingii WF (1978) Electronic recording of plant penetration behaviour by aphids. Entomol. exp. appl. 24: 721–730
Tjallingii WF (1985a) Membrane potentials as an indication for plant cell penetration by aphid stylets. Entomol. exp. appl. 38: 187–195
Tjallingii WF (1985b) Electrical nature of recorded signals during stylet penetration by aphids. Entomol. exp. appl. 38: 177–186
Tjallingii WF (1988) Electrical recording of stylet penetration activities. In: Minks AK and harrewijn P (eds) Aphids: Their Biology Natural Enemies and Control. Vol. B (pp. 95–108) Elsevier, Amsterdam
Tjallingii WF (1990) Continuous recording of stylet penetration activities by aphids. In: Campbell RK and Eikenbary RD (eds) Aphid-Plant Genotype Interactions (pp. 89–99) Elsevier, Amsterdam
Watson MA (1938) Further studies on the relationship betweenHyoscyamus virus 3 and the aphisMyzus persicae (Sulz.) with special reference to the effects of fasting. Proc. Royal Soc. London, Ser. B 125: 144–170
Watson MA and Roberts FM (1939) A comparative study of the transmission ofHyoscyamus virus 3, potato virus Y, and cucumber virus 1 by the vectorsMyzus persicae (Sulz.),M. circumflexus (Buckton) andMacrosiphum gei (Koch.). Proc. Royal Soc. London, Ser. B, 127: 543–576
Watson MA and Roberts FM (1940) Evidence against the hypothesis that certain plant viruses are transmitted mechanically by aphids. Ann. appl. Biol. 27: 227–233
Wensler RJD (1962) Mode of host selection by an aphid. Nature 195: 830–831
Wensler RJD and Filshie BK (1969) Gustatory sense organs in the food canal of aphids. J. Morphology 129: 473–492
Yates F (1934) Contingency tables involving small numbers and the χ2 tests. Journal of the Royal Statistical Supplement 1: 217–235
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Powell, G., Pirone, T. & Hardie, J. Aphid stylet activities during potyvirus acquisition from plants and anin vitro system that correlate with subsequent transmission. Eur J Plant Pathol 101, 411–420 (1995). https://doi.org/10.1007/BF01874855
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01874855