Disruption of Vector Transmission by a Plant-Expressed Viral Glycoprotein

Vector-borne viruses are a threat to human, animal, and plant health worldwide, requiring the development of novel strategies for their control. Tomato spotted wilt virus (TSWV) is one of the 10 most economically significant plant viruses and, together with other tospoviruses, is a threat to global food security. TSWV is transmitted by thrips, including the western flower thrips, Frankliniella occidentalis. Previously, we demonstrated that the TSWV glycoprotein GN binds to thrips vector midguts. We report here the development of transgenic plants that interfere with TSWV acquisition and transmission by the insect vector. Tomato plants expressing GN-S protein supported virus accumulation and symptom expression comparable with nontransgenic plants. However, virus titers in larval insects exposed to the infected transgenic plants were three-log lower than insects exposed to infected nontransgenic control plants. The negative effect of the GN-S transgenics on insect virus titers persisted to adulthood, as shown by four-log lower virus titers in adults and an average reduction of 87% in transmission efficiencies. These results demonstrate that an initial reduction in virus infection of the insect can result in a significant decrease in virus titer and transmission over the lifespan of the vector, supportive of a dose-dependent relationship in the virus–vector interaction. These findings demonstrate that plant expression of a viral protein can be an effective way to block virus transmission by insect vectors.

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Tomato spotted wilt virusmanipulates the reproduction of its insect vector, western flower thrips (Frankliniella occidentalis), to facilitate transmission

10.1101/598920 ◽

2019 ◽

Author(s):

Yanran Wan ◽

Sabir Hussain ◽

Baoyun Xu ◽

Wen Xie ◽

Shaoli Wang ◽

...

Keyword(s):

Frankliniella Occidentalis ◽

Mating Behaviour ◽

Monitoring Program ◽

Virus Transmission ◽

Western Flower Thrips ◽

Reproductive Behaviour ◽

Insect Vector ◽

Vegetable Crops ◽

Flower Thrips ◽

Tomato Spotted Wilt

ABSTRACTBACKGROUNDTomato spotted wilt virus(TSWV), one of the most devastating viruses of ornamental plants and vegetable crops worldwide, is transmitted by the western flower thrips,Frankliniella occidentalis(Pergande), in a persistent-propagative manner. How TSWV manipulates the reproduction of its vector to enhance transmission and whether infection with TSWV changes the mating behaviour of this thrips vector are not fully understood.RESULTSIn this study, we found that TSWV-exposed thrips, in general, had a significantly longer developmental time than did non-exposed individuals. Such an increase was predominantly seen in adults, a stage associated with dispersal and virus transmission. TSWV-exposedF. occidentalis produced substantially more progeny than did non-exposed thrips. Interestingly, most of the increase in progeny came from an increase in males, a sex with a greater dispersal and virus transmission capability. Specifically, the sex ratio of progeny shifted from female biased (2-7:1) to evenly split or male biased. Regarding mating behaviour, compared to virus-free controls, TSWV-exposedF. occidentalis had significantly longer copulation duration, were more active in males, and remated less often in females.CONCLUSIONThese combined results suggest that TSWV alters the reproductive behaviour of its insect vector,F. occidentalis, to promote virus transmission. Consequently, a monitoring program capable of earlier detection of the virus and a reduced economic threshold for vector (thrips) control should be in consideration for the long-term, sustainable management of TSWV.

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Tenuivirususes a molecular bridge strategy to overcome insect midgut barriers for virus persistent transmission

10.1101/404657 ◽

2018 ◽

Author(s):

Gang Lu ◽

Shuo Li ◽

Changwei Zhou ◽

Xin Qian ◽

Qing Xiang ◽

...

Keyword(s):

Brown Planthopper ◽

Specific Interaction ◽

Virus Transmission ◽

Plant Viruses ◽

Insect Vector ◽

Terminal Protein ◽

Insect Midgut ◽

Helper Component ◽

Vector Interaction ◽

Molecular Bridge

AbstractMany persistent transmitted plant viruses, includingRice stripe tenuivirus(RSV), cause serious damages to crop productions in China and worldwide. Although many reports have indicated that successful insect-mediated virus transmission depends on proper virus–insect vector interactions, the mechanism(s) controlling interactions between viruses and insect vectors for virus persistent transmission remained poorly understood. In this study, we used RSV and its small brown planthopper (SBPH) vector as a working model to elucidate the molecular mechanism controlling RSV virion entrance into SBPH midgut for persistent transmission. We have now demonstrated that this non-envelopedTenuivirususes its non-structural glycoprotein NSvc2 as a helper component to bridge the specific interaction between virion and SBPH midgut cells, leading to overcome SBPH midgut barriers for virus persistent transmission. In the absence of this glycoprotein, purified RSV virion is not capable of entering SBPH midgut cells. In RSV-infected cells, glycoprotein NSvc2 is processed into two mature proteins: an amino-terminal protein NSvc2-N and a carboxyl-terminal protein NSvc2-C. We determined that NSvc2-N interacted with RSV virion and bound directly to midgut lumen surface via its N-glycosylation sites. Upon recognition by midgut cells, the midgut cells underwent endocytosis followed by compartmentalizing RSV virion and NSvc2 into early and then late endosomes. The acidic condition inside the late endosome triggered conformation change of NSvc2-C and caused cell membrane fusion via its highly conserved fusion loop motifs, leading to the release of RSV virion from endosome into cytosol. In summary, our results showed for the first time that a riceTenuivirususes a molecular bridge strategy to ensure proper interactions between virus and insect midgut for successful persistent transmission.Author summaryOver 75% of the known plant viruses are insect transmitted. Understanding how plant viruses interacted with their insect vectors during virus transmission is one of the key steps to manage virus diseases worldwide. Both the direct and indirect virus–insect vector interaction models have been proposed for virus non-persistent and semi-persistent transmission. However, the indirect virus–vector interaction mechanism during virus persistent transmission has not been reported previously. In this study, we developed a new reverse genetics technology and demonstrated that the circulative and propagative transmittedRice stripe tenuivirusutilizes a glycoprotein NSvc2 as a helper component to ensure a specific interaction betweenTenuivirusvirion and midgut cells of small brown planthopper (SBPH), leading to conquering the midgut barrier of SBPH. This is the first report of a helper component mediated-molecular bridge mechanism for virus persistent transmission. These new findings and our new model on persistent transmission expand our understanding of molecular mechanism(s) controlling virus–insect vector interactions during virus transmission in nature.

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Two-year Grower Survey of Western Flower Thrips and Tospovirus Incidence and Management in Maine Greenhouses

HortScience ◽

10.21273/hortsci.31.4.569e ◽

1996 ◽

Vol 31 (4) ◽

pp. 569e-570 ◽

Cited By ~ 1

Author(s):

P.A. Stack ◽

L.B. Stack ◽

F.A. Drummond

Keyword(s):

Pest Management ◽

Frankliniella Occidentalis ◽

Management Strategies ◽

Mail Survey ◽

Western Flower Thrips ◽

Plant Viruses ◽

Future Research ◽

Flower Thrips ◽

Greenhouse Growers ◽

Grower Survey

A mail survey of greenhouse growers was conducted in 1994 and 1995 to determine the presence and importance of western flower thrips (WFT), Frankliniella occidentalis Pergande, in Maine greenhouses in growing years 1993 and 1994. Respondents were licensed growers with at least 1000 ft2 (93 m2) of greenhouse growing area. The survey objectives were to develop a grower demographic profile; determine the incidence of WFT and two WFT-vectored plant viruses, tomato spotted wilt (TSWV) and impatiens necrotic spot (INSV); and identify current WFT management strategies. The survey shows that Maine greenhouse growers are seasonal, experienced and retail oriented. Their growing area averages less than 10,000 ft2 (929 m2) and they produce a diverse crop mix and choose to import production stock as much as propagate it themselves. Both WFT and TSWV/INSV have increased in severity in Maine greenhouses over the past 10 years. Larger, year-round greenhouses are more likely to experience infestations of WFT and higher virus incidence. An integrated pest management (IPM) strategy is employed by the majority of growers surveyed. Insecticide application is the primary tactic used to control WFT. Fewer than 4% of the growers use natural enemies to control thrips. However, 63% responded that future research in pest management should focus on biological control.

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Comparative plant transcriptome profiling of Arabidopsis and Camelina infested with Myzus persicae aphids acquiring circulative and non-circulative viruses reveals virus- and plant-specific alterations relevant to aphid feeding behavior and transmission

10.1101/2022.01.04.474350 ◽

2022 ◽

Author(s):

Quentin Chesnais ◽

Victor Golyaev ◽

Amadine Velt ◽

Camille Rustenholz ◽

Véronique Brault ◽

...

Keyword(s):

Feeding Behavior ◽

Myzus Persicae ◽

Virus Transmission ◽

Transcriptome Profiling ◽

Defense Responses ◽

Plant Viruses ◽

Transmission Mode ◽

Insect Vector ◽

Plant Host ◽

Aphid Vector

Background: Evidence accumulates that plant viruses alter host-plant traits in ways that modify their insect vectors' behavior. These alterations often enhance virus transmission, which has led to the hypothesis that these effects are manipulations caused by viral adaptation. However, the genetic basis of these indirect, plant-mediated effects on vectors and their dependence on the plant host and the mode of virus transmission is hardly known. Results: Transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with turnip yellows virus (TuYV) or cauliflower mosaic virus (CaMV) and infested with the common aphid vector Myzus persicae revealed strong virus- and host-specific differences in the gene expression patterns. CaMV infection caused more severe effects on the phenotype of both plant hosts than did TuYV infection, and the severity of symptoms correlated strongly with the proportion of differentially expressed genes, especially photosynthesis genes. Accordingly, CaMV infection modified aphid behavior and fecundity stronger than did infection with TuYV. Conclusions: Overall, infection with CaMV — relying on the non-circulative transmission mode — tends to have effects on metabolic pathways with strong potential implications for insect-vector / plant-host interactions (e.g. photosynthesis, jasmonic acid, ethylene and glucosinolate biosynthetic processes), while TuYV — using the circulative transmission mode — alters these pathways only weakly. These virus-induced deregulations of genes that are related to plant physiology and defense responses might impact aphid probing and feeding behavior on both infected host plants, with potentially distinct effects on virus transmission. Keywords: Caulimovirus, polerovirus, aphid vector, transmission, feeding behavior, insect-plant interactions, transcriptome profiling, RNA-seq.

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The Plant Virus Tomato Spotted Wilt Tospovirus Activates the Immune System of Its Main Insect Vector, Frankliniella occidentalis

Journal of Virology ◽

10.1128/jvi.78.10.4976-4982.2004 ◽

2004 ◽

Vol 78 (10) ◽

pp. 4976-4982 ◽

Cited By ~ 56

Author(s):

Ricardo B. Medeiros ◽

Renato de O. Resende ◽

Antonio Carlos de Ávila

Keyword(s):

Immune Response ◽

Immune System ◽

Plant Virus ◽

Frankliniella Occidentalis ◽

Plant Viruses ◽

Cdna Libraries ◽

Northern Analysis ◽

Insect Vector ◽

Insect Vectors ◽

Tomato Spotted Wilt

ABSTRACT Tospoviruses have the ability to infect plants and their insect vectors. Tomato spotted wilt virus (TSWV), the type species in the Tospovirus genus, infects its most important insect vector, Frankliniella occidentalis, the western flower thrips (WFT). However, no detrimental effects on the life cycle or cytopathological changes have been reported in the WFT after TSWV infection, and relatively few viral particles can be observed even several days after infection. We hypothesized that TSWV infection triggers an immune response in the WFT. Using subtractive cDNA libraries to probe WFT DNA macroarrays, we found that the WFT's immune system is activated by TSWV infection. The activated genes included (i) those encoding antimicrobial peptides, such as defensin and cecropin; (ii) genes involved in pathogen recognition, such as those encoding lectins; (iii) those encoding receptors that activate the innate immune response, such as Toll-3; and (iv) those encoding members of signal transduction pathways activated by Toll-like receptors, such as JNK kinase. Transcriptional upregulation of these genes after TSWV infection was confirmed by Northern analysis, and the kinetics of the immune response was measured over time. Several of the detected genes were activated at the same time that viral replication was first detected by reverse transcription-PCR. To our knowledge, this is the first report of the activation of an insect vector immune response by a plant virus. The results may lead to a better understanding of insects' immune responses against viruses and may help in the future development of novel control strategies against plant viruses, as well as human and animal viruses transmitted by insect vectors.

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Application of Genomics for Understanding Plant Virus-Insect Vector Interactions and Insect Vector Control

Phytopathology ◽

10.1094/phyto-02-16-0111-fi ◽

2016 ◽

Vol 106 (10) ◽

pp. 1213-1222 ◽

Cited By ~ 10

Author(s):

Navneet Kaur ◽

Daniel K. Hasegawa ◽

Kai-Shu Ling ◽

William M. Wintermantel

Keyword(s):

Gene Expression ◽

Molecular Mechanisms ◽

Virus Transmission ◽

Plant Viruses ◽

Significant Shift ◽

Insect Vector ◽

Insect Vectors ◽

Genomic Technologies ◽

Potential Applications ◽

Generation Sequencing

The relationships between plant viruses and their vectors have evolved over the millennia, and yet, studies on viruses began <150 years ago and investigations into the virus and vector interactions even more recently. The advent of next generation sequencing, including rapid genome and transcriptome analysis, methods for evaluation of small RNAs, and the related disciplines of proteomics and metabolomics offer a significant shift in the ability to elucidate molecular mechanisms involved in virus infection and transmission by insect vectors. Genomic technologies offer an unprecedented opportunity to examine the response of insect vectors to the presence of ingested viruses through gene expression changes and altered biochemical pathways. This review focuses on the interactions between viruses and their whitefly or thrips vectors and on potential applications of genomics-driven control of the insect vectors. Recent studies have evaluated gene expression in vectors during feeding on plants infected with begomoviruses, criniviruses, and tospoviruses, which exhibit very different types of virus-vector interactions. These studies demonstrate the advantages of genomics and the potential complementary studies that rapidly advance our understanding of the biology of virus transmission by insect vectors and offer additional opportunities to design novel genetic strategies to manage insect vectors and the viruses they transmit.

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Laboratory and Greenhouse Evaluation of a Granular Formulation of Beauveria bassiana for Control of Western Flower Thrips, Frankliniella occidentalis

Insects ◽

10.3390/insects10020058 ◽

2019 ◽

Vol 10 (2) ◽

pp. 58 ◽

Cited By ~ 6

Author(s):

Xingrui Zhang ◽

Zhongren Lei ◽

Stuart Reitz ◽

Shengyong Wu ◽

Yulin Gao

Keyword(s):

Soil Moisture ◽

Beauveria Bassiana ◽

Entomopathogenic Fungi ◽

Frankliniella Occidentalis ◽

Western Flower Thrips ◽

Plant Viruses ◽

Infection Process ◽

The Body ◽

Plant Production ◽

Flower Thrips

Western flower thrips (WFT) is one of the most important pests of horticultural crops worldwide because it can damage many different crops and transmit various plant viruses. Given these significant impacts on plant production, novel methodologies are required to maximize regulation of WFT to minimize crop losses. One particular approach is to develop control strategies for the non-feeding, soil-dwelling stages of WFT. Control of these stages could be enhanced through the use of granules impregnated with entomopathogenic fungi mixed in the soil. The use of soil-applied fungi contrasts with existing approaches in which entomopathogenic fungi are formulated as oil-based suspensions or water-based wettable powders for foliar applications against the feeding stages of WFT. To examine the efficacy of this approach, we evaluated the effects of a granular formulation of Beauveria bassiana on the soil-dwelling, pupal phases of Frankliniella occidentalis in laboratory bioassays and greenhouse experiments. Based on micromorphological observations of fungal conidia during the infection process after treatment of WFT with a B. bassiana suspension, fungal conidia complete the process of surface attachment, germination, and penetration of the body wall of the WFT pupa and enter the host within 60 h of treatment. Given these results, we undertook a controlled greenhouse experiment and applied B. bassiana granules to soil used to cultivate eggplants. Populations of F. occidentalis on eggplants grown in treated soil were 70% lower than those on plants grown in the untreated soil after 8 weeks. Furthermore, when measuring the survival and growth of B. bassiana on granules under different soil moisture conditions, survival was greatest when the soil moisture content was kept at 20%. These results indicate that the application of B. bassiana-impregnated granules could prove to be an effective biological control strategy for use against F. occidentalis under greenhouse conditions.

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A Soluble Form of the Tomato spotted wilt virus (TSWV) Glycoprotein GN (GN-S) Inhibits Transmission of TSWV by Frankliniella occidentalis

Phytopathology ◽

10.1094/phyto-98-1-0045 ◽

2008 ◽

Vol 98 (1) ◽

pp. 45-50 ◽

Cited By ~ 45

Author(s):

A. E. Whitfield ◽

N. K. K. Kumar ◽

D. Rotenberg ◽

D. E. Ullman ◽

E. A. Wyman ◽

...

Keyword(s):

Time Course ◽

Tomato Spotted Wilt Virus ◽

Frankliniella Occidentalis ◽

Infected Plant ◽

Virus Titer ◽

Soluble Form ◽

Viral Glycoprotein ◽

S Protein ◽

Tomato Spotted Wilt ◽

Wilt Virus

Tomato spotted wilt virus (TSWV) is an economically important virus that is transmitted in a persistent propagative manner by its thrips vector, Frankliniella occidentalis. Previously, we found that a soluble form of the envelope glycoprotein GN (GN-S) specifically bound thrips midguts and reduced the amount of detectable virus inside midgut tissues. The aim of this research was to (i) determine if GN-S alters TSWV transmission by thrips and, if so, (ii) determine the duration of this effect. In one study, insects were given an acquisition access period (AAP) with GN-S mixed with purified virus and individual insects were assayed for transmission. We found that GN-S reduced the percent of transmitting adults by eightfold. In a second study, thrips were given an AAP on GN-S protein and then placed on TSWV-infected plant material. Individual insects were assayed for transmission over three time intervals of 2 to 3, 4 to 5, and 6 to 7 days post-adult eclosion. We observed a significant reduction in virus transmission that persisted to the same degree throughout the time course. Real-time reverse transcription polymerase chain reaction analysis of virus titer in individual insects revealed that the proportion of thrips infected with virus was reduced threefold when insects were preexposed to the GN-S protein as compared to no exposure to protein, and nontransmitters were not infected with virus. These results demonstrate that thrips transmission of a tospovirus can be reduced by exogenous viral glycoprotein.

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Deep Sequencing of Small RNAs in the Whitefly Bemisia tabaci Reveals Novel MicroRNAs Potentially Associated with Begomovirus Acquisition and Transmission

Insects ◽

10.3390/insects11090562 ◽

2020 ◽

Vol 11 (9) ◽

pp. 562

Author(s):

Daniel K. Hasegawa ◽

Md Shamimuzzaman ◽

Wenbo Chen ◽

Alvin M. Simmons ◽

Zhangjun Fei ◽

...

Keyword(s):

Bemisia Tabaci ◽

Deep Sequencing ◽

Small Rnas ◽

Target Genes ◽

Expression Profiles ◽

Virus Transmission ◽

Plant Viruses ◽

Insect Vector ◽

Regulatory Effects ◽

Leaf Curl Virus

The whitefly Bemisia tabaci (Gennadius) is a notorious insect vector that transmits hundreds of plant viruses, affecting food and fiber crops worldwide, and results in the equivalent of billions of U.S. dollars in crop loss annually. To gain a better understanding of the mechanism in virus transmission, we conducted deep sequencing of small RNAs on the whitefly B. tabaci MEAM1 (Middle East-Asia Minor 1) that fed on tomato plants infected with tomato yellow leaf curl virus (TYLCV). Overall, 160 miRNAs were identified, 66 of which were conserved and 94 were B. tabaci-specific. Among the B. tabaci-specific miRNAs, 67 were newly described in the present study. Two miRNAs, with predicted targets encoding a nuclear receptor (Bta05482) and a very-long-chain (3R)-3-hydroxyacyl-CoA dehydratase 2 (Bta10702), respectively, were differentially expressed in whiteflies that fed on TYLCV-infected versus uninfected plants. To better understand the regulatory effects of identified miRNAs and their target genes, we correlated expression profiles of miRNAs and their target transcripts and found that, interestingly, miRNA expression was inversely correlated with the expression of ~50% of the predicted target genes. These analyses could serve as a model to study gene regulation in other systems involving arthropod transmission of viruses to plants and animals.

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