A Midgut Barrier to Tomato Spotted Wilt Virus Acquisition by Adult Western Flower Thrips

Ullman, Diane E.; Cho, J. J.; Mau, Ronald F. L.; Westcot, Daphne M.; Custer, D. M.

doi:10.1094/phyto-82-1333

Cited by 154 publications

(119 citation statements)

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“…F. occidentalis and TSWV isolate MT2 were originally collected in Hawaii. Thrips were reared on green bean pods (Phaseolus vulgaris L.), and virus was maintained in Emelia sonchifolia (L.) as previously described (35). Virus-infected and control treatment groups were obtained by allowing first instar thrips 24 h of access to infected and uninfected E. sonchifolia leaves, respectively, as previously described (35).…”

Section: Methodsmentioning

confidence: 99%

Infection with a plant virus modifies vector feeding behavior

Stafford

Walker²,

Ullman³

2011

Proc. Natl. Acad. Sci. U.S.A.

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282

236

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Vector infection by some animal-infecting parasites results in altered feeding that enhances transmission. Modification of vector behavior is of broad adaptive significance, as parasite fitness relies on passage to a new host, and vector feeding is nearly always essential for transmission. Although several plant viruses infect their insect vectors, we have shown that vector infection by a plant virus alters feeding behavior. Here we show that infection with Tomato spotted wilt virus (TSWV), type member of the only plant-infecting genus in the Bunyaviridae, alters the feeding behavior of its thrips vector, Frankliniella occidentalis (Pergande). Male thrips infected with TSWV fed more than uninfected males, with the frequency of all feeding behaviors increasing by up to threefold, thus increasing the probability of virus inoculation. Importantly, infected males made almost three times more noningestion probes (probes in which they salivate, but leave cells largely undamaged) compared with uninfected males. A functional cell is requisite for TSWV infection and cell-to-cell movement; thus, this behavior is most likely to establish virus infection. Some animalinfecting members of the Bunyaviridae (La Crosse virus and Rift Valley fever virus) also cause increased biting rates in infected vectors. Concomitantly, these data support the hypothesis that capacity to modify vector feeding behavior is a conserved trait among plant-and animal-infecting members of the Bunyaviridae that evolved as a mechanism to enhance virus transmission. Our results underscore the evolutionary importance of vector behavioral modification to diverse parasites with host ranges spanning both plant and animal kingdoms. virus evolution | Tospovirus | virus-vector interactions

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Section: Methodsmentioning

confidence: 99%

Infection with a plant virus modifies vector feeding behavior

Stafford

Walker²,

Ullman³

2011

Proc. Natl. Acad. Sci. U.S.A.

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282

236

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“…The gut bacteria have to be acquired via food contaminated by the bacteria in frass, saliva, and faeces of other thrips (De Vries et al, 2008 Variation in the capacity of the various stages to ingest or transmit viruses has been previously recorded (Ammar, 1994;. Several reasons have been suggested to account for this variation, such as, the mid-gut barriers to infection differ between larval stages (Ullman et al, 1992), the barriers between the midgut and salivary glands may differ (Moritz et al, 2004), and/or there is variation in efficiency with which the salivary glands are infected . The omnipresence of gut bacteria in old first and second instar larvae, and their absence in young first instar larvae, led us to formulate the hypothesis that the increase in the number of gut bacteria is negatively associated with the ability to transmit tospovirus, because the bacteria adversely affect the ability of the virus to infect mid-gut epithelial cells and its subsequent transmission.…”

Section: Introductionmentioning

confidence: 99%

Symbiotic bacteria (Erwinia sp.) in the gut of Frankliniella occidentalis (Thysanoptera: Thripidae) do not affect its ability to transmit tospovirus

Vries¹,

Wetering²,

Hoek³

et al. 2012

Eur. J. Entomol.

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Abstract. Tomato spotted wilt virus (TSWV) is one of the most harmful plant viruses and one of its most important vectors is the western flower thrips [Frankliniella occidentalis Pergande (Thysanoptera: Thripidae)]. Recently, we reported the close association of Erwinia sp. gut bacteria with this species of thrips. The first instar larvae acquire these bacteria from their food source. A high proportion of adult western flower thrips transmit TSWV after acquiring the virus during the first larval stage when there are no bacteria in their gut. A considerably lower proportion of adults that acquire the virus early in the second instar transmit virus and none of those exposed to virus late on in the second instar do so. The highest prevalence and total number of symbiotic bacteria are recorded in the guts of second instar thrips. This leads to the hypothesis that the build up of bacteria in the gut reduces the acquisition of TSWV, resulting in a lower capacity to transmit the virus. To test this hypothesis, the transmission of this virus by symbiotic and aposymbiotic adult thrips of the NL3 population was studied. Comparison of virus transmission by adult thrips, the larvae of which either had or lacked gut bacteria and were exposed to virus in either the first or second instar, revealed no difference in the ability of symbiotic and aposymbiotic adults to transmit this virus. We conclude that virus transmission is not affected by the number of the symbiotic bacteria Erwinia sp. present in the gut of thrips larvae.

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“…WFT transmits the virus in a circulative and propagative persistent manner (Ullman et al, 1993;. Transmission is unique in that TSWV can only be acquired by thrips larvae and transmitted by second larval instars or adults (Ullman et al, 1992a;. Adult thrips are considered to be the most important cause of virus dispersal because of their greater mobility (Cho et al, 1989;German et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

Comparative host reactions and Frankliniella occidentalis transmission of different isolates of tomato spotted wilt tospovirus from Spain

Roca¹,

Aramburu²,

Moriones³

1997

Plant Pathology

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The abilities of different isolates of tomato spotted wilt tospovirus (TSWV) collected from northeastern and eastern Spain to infect 10 host species, and to be acquired and transmitted by the western flower thrips (WFT), Frankliniella occidentalis were compared. Two isolates of TSWV from a single source plant could be separated according to the different type of local lesions they induced in Nicotiana glutinosa. Host ranges of the studied TSWV isolates were very similar, but differences were found in the symptoms induced and in their capacity to infect specific hosts systemically. Lycopersicon esculentum and Datura stramonium were evaluated for their potential as virus acquisition host species. The proportion of transmitter adult thrips obtained from WFT larvae fed on L. esculentum was greater than from D. stramonium. No differences were detected between TSWV isolates in their ability to be acquired and transmitted by WFT. No evidence was obtained of alterations in TSWV particles which could affect WFT transmissibility due to the repeated mechanical transfers used to clone the isolates. Our findings do not support the existence of pathological effects of TSWV on WFT.

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A Midgut Barrier to Tomato Spotted Wilt Virus Acquisition by Adult Western Flower Thrips

Cited by 154 publications

References 0 publications

Infection with a plant virus modifies vector feeding behavior

Infection with a plant virus modifies vector feeding behavior

Symbiotic bacteria (Erwinia sp.) in the gut of Frankliniella occidentalis (Thysanoptera: Thripidae) do not affect its ability to transmit tospovirus

Comparative host reactions and Frankliniella occidentalis transmission of different isolates of tomato spotted wilt tospovirus from Spain

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