The effect of pre-acquisition starvation on aphid transmission of potyviruses during observed and electrically recorded stylet penetrations (original) (raw)
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European Journal of Plant Pathology, 1995
The behavioural events associated with acquisition of tobacco etch potyvirus by starved Myzus 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 I13. 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 II3-1ike pulses during acquisition. The duration of occurrence of recorded phase I13 pulses, either on plants or the in 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-egesfion' hypothesis for nonpersistent transmission. Starved aphids acquiring virus from infected leaf tissue or the in 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. 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.
Modification of Non-Vector Aphid Feeding Behavior on Virus-Infected Host Plant
Journal of Insect Science, 2013
Virus-infected host plants can have positive, neutral or negative effects on vector aphids. Even though the proportion of non-vector aphids associated with a plant far exceeds that of vector species, little is known about the effect of virus-infected plants on non-vector aphids. In the present study, the English grain aphid Sitobion avenae (Fabricius) (Hemiptera: Aphididae), a non-vector of Wheat dwarf virus (WDV) and Cereal yellow dwarf virus-RPV (CYDV-RPV), was monitored on, virus-infected, virus-free and leafhopper/aphid-infested, and virus-and insect-free (control) barley, Hordeum vulgare L. (Poales: Poaceae), plants. Electrical penetration graph recordings were performed. Compared with the control plants, S. avenae on infected plants exhibited reduced non-probing and pathway phase, and increased phloem sap ingestion phase, and more aphids reached sustained phloem ingestion. However, the electrical penetration graph parameters described above showed no significant differences in aphid feeding behavior on virus-free and vector pre-infested plants and the control barley plants during S. avenae feeding. The results suggest that WDV/CYDV-RPV-infected host plants positively affected the feeding behavior of the non-vector aphid S. avenae. Based on these results, the reasons and trends among the virusinfected host plants' effects on the feeding behavior of non-vector aphids are discussed.
Journal of General Virology, 2012
Inoculation of the semi-persistent cauliflower mosaic virus (CaMV, genus Caulimovirus) is associated with successive brief (5-10 s) intracellular stylet punctures (pd) when aphids probe in epidermal and mesophyll cells. In contrast to non-persistent viruses, there is no evidence for which of the pd subphases (II-1, II-2 and II-3) is involved in the inoculation of CaMV. Experiments were conducted using the electrical penetration graph (EPG) technique to investigate what particular subphases of the pd are associated with the inoculation of CaMV to turnip by its aphid vector Brevicoryne brassicae. In addition, the same aphid species/test plant combination was used to compare the role of the pd subphases in the inoculation of the non-persistent turnip mosaic virus (TuMV, genus Potyvirus). Inoculation of TuMV was found to be related to subphase II-1, confirming earlier results, but CaMV inoculation appeared to be related exclusively to subphase II-2 instead. The mechanism of CaMV inoculation and the possible nature of subphase II-2 are discussed in the scope of our findings. %paper no. vir037887 charlesworth ref: vir037887& Plant
Journal of General Virology, 1996
The hypothesis that loss of aphid transmissibility of potyvirus mutants is due to non-retention of virions in the mouthparts was tested by feeding aphids through membranes on purified virions of aphid transmissible (AT or HAT) and non-aphid-transmissible (NAT) tobacco vein mottling virus (TVMV) or tobacco etch virus (TEV), in the presence of functional [potato virus Y (PVY) HC or TVMV HC] or non-functional (PVC HC) helper component (HC). TVMV virions were detected, by electron microscopic examination of immunogoldlabelled thin sections, in the food canal or cibarium of 57 % of 28 aphids fed on the transmissible combination of TVMV-AT and functional HC, while no virions were found in these structures in 25 aphids fed on the nontransmissible combinations: TVMV-NAT and PVY HC, or TVMV-AT and PVC HC. Autoradiography of intact stylets allowed the examination of much larger numbers of aphids, fed on 125I-labelled TEV; 48 % of 523 aphids fed on the TEV-HAT and PVY HC combination retained label in the stylets; this correlated well with the percentage transmission in bioassays. In contrast, in non-transmissible combinations, label was found in the stylets of 0.77% of 389 aphids fed on TEV-NAT and PVY HC, and 1-35 % of 223 aphids fed on TEV-HAT and PVC HC. No differences were found in the overall amount of label in the bodies of aphids fed on the transmissible and non-transmissible combinations.
Archives of Virology, 2019
Potato virus Y (PVY) is a common pathogen affecting agricultural production worldwide, and is mainly transmitted by Myzus persicae in a non-persistent manner. Insect-borne plant viruses can modify the abundance, performance, and behavior of their vectors by altering host plant features; however, most studies have overlooked the fact that the dynamic progression of virus infection in plants can have variable effects on their vectors. We addressed this point in the present study by dividing the PVY infection process in tobacco into three stages (early state, steady state and late state) according to viral copy number, and then compared the variational effects of PVY-infected tobacco (Nicotiana tabacum) plants on host selection and feeding behavior of M. persicae. A Y-shaped olfactory apparatus and electrical penetration graph (EPG) method were used to evaluate host selection and feeding behavior, respectively. Interestingly, we found that PVY-infected plants at the steady state of infection attracted more aphids than healthy plants, whereas no differences were observed for those at the early and late states. In terms of feeding behavior, intracellular punctures which are closely related to PVY acquisition and transmission were more abundant on PVY-infected tobacco plants at the early and steady states of infection than in non-infected plants. These results indicate that PVY-infected host plants can alter the host selection and feeding behavior of aphids in a stage-dependent manner manner, which is an important consideration when studying the interactions among host plants, virus, and insect vectors.
Aphids secrete watery saliva into plant tissues from the onset of stylet penetration
Entomologia Experimentalis et Applicata, 2011
Aphid feeding requires the secretion of two types of saliva: gelling saliva (from the principal gland) that forms an intercellular sheath for the penetrating stylet, and watery saliva [from accessory salivary glands (ASGs)] that facilitates intracellular penetration and phloem feeding. Plant viruses can be used as salivary markers to investigate key steps in aphid feeding, and penetration can be monitored electrically using the electrical penetration graph (EPG) approach. We conducted a series of EPG-controlled transmission experiments using Cucurbit aphid-borne yellows virus [CABYV; Polerovirus spec. (Luteoviridae)], which is retained in the ASGs, as a marker for watery saliva secretions. The melon aphid, Aphis gossypii Glover (Hemiptera: Aphididae), was used as a vector and melon seedlings, Cucumis melo L. (Cucurbitaceae), as host plants. Viruliferous aphids were interrupted at various stages during stylet penetration, i.e., during intercellular penetration prior to intracellular puncture and following a potential drop within the first probe. Viruliferous aphids and leaf disc samples obtained from the stylet penetration site were used to detect CABYV by quantitative real-time RT-PCR. Approximately half of the inoculated leaf discs were found to be infected with CABYV after very brief (12.9 ± 1.9 s) intercellular stylet probes and before intracellular stylet puncture. The number of virus particles ejected during such probes was similar to the number ejected by aphids during longer probes including a single intracellular puncture. Our results therefore suggest that watery saliva is secreted by aphids from the onset of stylet penetration.
Entomologia Experimentalis et Applicata, 2001
Five distinct electrical penetration graph waveforms characterising the feeding behaviour of the leafhopper Cicadulina mbila Naudé (Homoptera: Cicadellidae) on maize (Zea mays L.) were obtained using a DC based system. The waveforms were distinguished by spectral features and by statistical analysis of their median voltages, durations and time to first waveform recording. By changing the polarity of the system voltage and the level of the input resistor it was shown that the waveforms are mainly determined by the electromotive force (emf) component. Based on the correlation between waveforms and the fine structure of the stylet pathways observed by transmission electron microscopy, insect's activities have been associated with five waveforms: stylet pathway formation (waveform 1), active ingestion (waveform 2), putative stylet work (waveform 3), salivation (waveform 4) and passive ingestion (waveform 5). Like waveform E1 and E2 of aphids, waveforms 4 and 5 of C. mbila correspond to feeding activities in sieve tubes. However, unlike aphids which probe briefly in non-vascular cells, waveform 2 corresponds to active ingestion in cells, where the cell content is partially ingested and hence the organelles' integrity severely affected. These observations suggest that this specific feeding feature, typical of leafhoppers, determines their ability to acquire geminivirus virions located in the plant cell nucleus.
Japanese Journal of Phytopathology, 1973
This paper reports the results of further investigations of the transmission and retention of inoculativity of potato leaf-roll virus (PLRV) in the green peach aphid, Myzus persicae (Sulz.). The frequency of virus transmission, the length of the latent period, and the retention period of inoculativity of the virus in the injected aphids were dependen ton the virus concentration of inocula. Virus recovery from viruliferous aphid extracts was influenced by the length of the acquisition feeding period of the aphids used as sources of inoculum. However, irrespective of the length of the acquisition feeding period, the virus concentration in the aphids tended gradually to decrease after leaving the source plant. The virus was recovered from the guts and blood, but not from the salivary glands of aphids given a 4-day acquisition feeding period on infected plants. Virus recovery from the aphid blood was also dependent on the length of the acquisition feeding period of aphids used as sources of inoculum. PLRV was detected in the blood of aphids up to 2 days after injection with a massive dose of the virus solution using aphid extracts as the inoculum. The results of virus recovery with the blood of the injected aphids were the same as for those following an acquisition feeding period. Attempts to maintain the virus inoculativity in serial passage using extracts or blood of viruliferous aphids were unsuccessful.
Annals of Applied Biology, 2003
Aphis gossypii is the main virus vector in muskmelon crops. The melon gene Vat confers resistance to non-persistent virus transmission by this aphid. The mechanism of this resistance is not well understood, but no relationship has been detected between resistance and the probing behaviour of aphids on resistant plants. Results presented here suggest that temporary blockage of aphid stylet tips preventing virus particle release may explain the resistance conferred by Vat gene. We performed experiments in which viruliferous aphids were allowed to probe different sequences of resistant (Vatbearing) and/or susceptible melon plants. The results demonstrated that A. gossypii inoculates Cucumber mosaic virus (CMV) efficiently in susceptible plants having previously probed resistant plants, showing that the resistance mechanism is reversible. Furthermore, the infection rate obtained for susceptible plants was the same (25%) regardless of whether the transmitting aphid had come directly from the CMV source or had subsequently probed on resistant plants. This result suggests that virus is not lost from stylet to plant during probing of resistant plants, supporting the temporary blockage hypothesis. We also found that the ability of Myzus persicae to transmit CMV is noticeably reduced after probing on resistant plants, providing evidence that this aphid species also responds to the presence of the Vat gene. Finally, we also found that in probes immediately after virus acquisition M. persicae inoculates resistant plants with CMV more efficiently than susceptible plants, perhaps because the Vat gene product induces increased salivation by this aphid.
Environmental Entomology, 2009
Previous research has shown that green peach aphids, Myzus persicae (Sulzer), preferentially settle on leaßets of potato plants (Solanum tuberosum L.) infected with potato leafroll virus (PLRV) compared with sham-inoculated controls, at least in part because of aphid responses to volatile cues from the plants. The prior work used plants 4 wk after inoculation. In this study, aphid emigration from the vicinity of leaßets of PLRV-infected plants at 2, 4, 6, 8, and 10 wk after inoculation was compared with emigration from leaßets of sham-inoculated control plants. For the bioassay, 30 aphids were placed directly above a test leaßet on screening to exclude gustatory and tactile cues and in darkness to exclude visual cues. The numbers emigrating were recorded every 10 min for 1 h. Volatile organic compounds (VOCs) were collected from the headspace of the test plants, quantiÞed, and compared among treatments. In bioasssays with leaßets of upper nodes of the plants, aphid immigration rates were signiÞcantly lower from leaßets of PLRV-infected plants than from sham-inoculated plants at 4 and 6 wk after inoculation, but not at 2, 8, and 10 wk after inoculation. In bioassays with leaßets from lower nodes, emigration did not differ between PLRV-infected plants and shaminoculated plants at any stage in the infection. Volatile compounds detectable in the headspace of intact plants at 2, 4, and 8 wk after inoculation (or sham inoculation) changed with plant age and with disease progression, potentially explaining behavioral responses of the aphids.