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

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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Investigations of the mechanism of the transmission of plant viruses by insect vectors III. The insect’s saliva

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1939.0038 ◽

1939 ◽

Vol 127 (849) ◽

pp. 526-543 ◽

Cited By ~ 18

Keyword(s):

Direct Evidence ◽

Virus Transmission ◽

Plant Viruses ◽

Convincing Evidence ◽

Transmission Characteristic ◽

Insect Vectors ◽

Leaf Hopper

For the type of virus transmission characteristic of leaf hopper vectors, there is convincing evidence that the virus passes through the insect's body. The manner in which it emerges from the insect and comes to be inoculated into a plant is much less certainly known. It has generally been assumed that the saliva is the vehicle of the inoculation. For this assumption there is even now little direct evidence. I now describe observations on the excretion of saliva by a leafhopper and attempts to demonstrate experimentally in this saliva the virus of which this insect is a specific vector.

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Structural Insights into the Molecular Mechanisms of Cauliflower Mosaic Virus Transmission by Its Insect Vector

Journal of Virology ◽

10.1128/jvi.02662-09 ◽

2010 ◽

Vol 84 (9) ◽

pp. 4706-4713 ◽

Cited By ~ 32

Author(s):

François Hoh ◽

Marilyne Uzest ◽

Martin Drucker ◽

Célia Plisson-Chastang ◽

Patrick Bron ◽

...

Keyword(s):

Mosaic Virus ◽

Molecular Mechanisms ◽

Structural Model ◽

Coiled Coil ◽

Virus Transmission ◽

Cauliflower Mosaic Virus ◽

Insect Vector ◽

Virus Surface ◽

X Ray Crystallography ◽

Coil Structure

ABSTRACT Cauliflower mosaic virus (CaMV) is transmitted from plant to plant through a seemingly simple interaction with insect vectors. This process involves an aphid receptor and two viral proteins, P2 and P3. P2 binds to both the aphid receptor and P3, itself tightly associated with the virus particle, with the ensemble forming a transmissible viral complex. Here, we describe the conformations of both unliganded CaMV P3 protein and its virion-associated form. X-ray crystallography revealed that the N-terminal domain of unliganded P3 is a tetrameric parallel coiled coil with a unique organization showing two successive four-stranded subdomains with opposite supercoiling handedness stabilized by a ring of interchain disulfide bridges. A structural model of virus-liganded P3 proteins, folding as an antiparallel coiled-coil network coating the virus surface, was derived from molecular modeling. Our results highlight the structural and biological versatility of this coiled-coil structure and provide new insights into the molecular mechanisms involved in CaMV acquisition and transmission by the insect vector.

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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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Insights Into Insect Vector Transmission and Epidemiology of Plant-Infecting Fijiviruses

Frontiers in Microbiology ◽

10.3389/fmicb.2021.628262 ◽

2021 ◽

Vol 12 ◽

Author(s):

Lu Zhang ◽

Nan Wu ◽

Yingdang Ren ◽

Xifeng Wang

Keyword(s):

Plant Disease ◽

Virus Transmission ◽

Insect Vector ◽

Insect Vectors ◽

System Research ◽

Transmission Characteristics ◽

Complex Interactions ◽

Transmission Mechanisms ◽

Vector Insect ◽

Efficient Transmission

Viruses in genus Fijivirus (family Reoviridae) have caused serious damage to rice, maize and sugarcane in American, Asian, European and Oceanian countries, where seven plant-infecting and two insect-specific viruses have been reported. Because the planthopper vectors are the only means of virus spread in nature, their migration and efficient transmission of these viruses among different crops or gramineous weeds in a persistent propagative manner are obligatory for virus epidemics. Understanding the mechanisms of virus transmission by these insect vectors is thus key for managing the spread of virus. This review describes current understandings of main fijiviruses and their insect vectors, transmission characteristics, effects of viruses on the behavior and physiology of vector insects, molecular transmission mechanisms. The relationships among transmission, virus epidemics and management are also discussed. To better understand fijivirus-plant disease system, research needs to focus on the complex interactions among the virus, insect vector, insect microbes, and plants.

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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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Feeding Behavior and Virus-transmission Ability of Insect Vectors Exposed to Systemic Insecticides

Plants ◽

10.3390/plants9070895 ◽

2020 ◽

Vol 9 (7) ◽

pp. 895 ◽

Cited By ~ 3

Author(s):

Elisa Garzo ◽

Aránzazu Moreno ◽

María Plaza ◽

Alberto Fereres

Keyword(s):

Feeding Behavior ◽

Virus Transmission ◽

Plant Viruses ◽

Crop Damage ◽

Insect Vectors ◽

Vector Borne Diseases ◽

Systemic Insecticides ◽

Turnip Yellows Virus ◽

Vector Borne ◽

Leaf Curl Virus

The majority of plant viruses depend on Hemipteran vectors for their survival and spread. Effective management of these insect vectors is crucial to minimize the spread of vector-borne diseases, and to reduce crop damage. The aim of the present study was to evaluate the effect of various systemic insecticides on the feeding behavior of Bemisia tabaci and Myzus persicae, as well as their ability to interfere with the transmission of circulative viruses. The obtained results indicated that some systemic insecticides have antifeeding properties that disrupt virus transmission by their insect vectors. We found that some of the tested insecticides significantly reduced phloem contact and sap ingestion by aphids and whiteflies, activities that are closely linked to the transmission of phloem-limited viruses. These systemic insecticides may play an important role in reducing the primary and secondary spread of tomato yellow leaf curl virus (TYLCV) and turnip yellows virus (TuYV), transmitted by B. tabaci and M. persicae, respectively.

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Applications of Proteomic Tools to Study Insect Vector–Plant Virus Interactions

Life ◽

10.3390/life10080143 ◽

2020 ◽

Vol 10 (8) ◽

pp. 143

Author(s):

Priyanka Mittapelly ◽

Swapna Priya Rajarapu

Keyword(s):

Protein Interactions ◽

Plant Virus ◽

Management Strategies ◽

Viral Disease ◽

Plant Viruses ◽

Global Changes ◽

Insect Vector ◽

Insect Vectors ◽

Biological Interactions ◽

Bioinformatic Tools

Proteins are crucial players of biological interactions within and between the organisms and thus it is important to understand the role of proteins in successful partnerships, such as insect vectors and their plant viruses. Proteomic approaches have identified several proteins at the interface of virus acquisition and transmission by their insect vectors which could be potential molecular targets for sustainable pest and viral disease management strategies. Here we review the proteomic techniques used to study the interactions of insect vector and plant virus. Our review will focus on the techniques available to identify the infection, global changes at the proteome level in insect vectors, and protein-protein interactions of insect vectors and plant viruses. Furthermore, we also review the integration of other techniques with proteomics and the available bioinformatic tools to analyze the proteomic data.

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Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

Viruses ◽

10.3390/v12020148 ◽

2020 ◽

Vol 12 (2) ◽

pp. 148 ◽

Cited By ~ 6

Author(s):

Xiujuan Wu ◽

Jian Ye

Keyword(s):

Crop Yield ◽

Plant Virus ◽

Plant Viruses ◽

Insect Vector ◽

Insect Vectors ◽

Plant Host ◽

Effective Strategies ◽

Secondary Damage ◽

Molecular And Biochemical Mechanisms ◽

Ja Signaling

Plant viruses pose serious threats to stable crop yield. The majority of them are transmitted by insects, which cause secondary damage to the plant host from the herbivore-vector’s infestation. What is worse, a successful plant virus evolves multiple strategies to manipulate host defenses to promote the population of the insect vector and thereby furthers the disease pandemic. Jasmonate (JA) and its derivatives (JAs) are lipid-based phytohormones with similar structures to animal prostaglandins, conferring plant defenses against various biotic and abiotic challenges, especially pathogens and herbivores. For survival, plant viruses and herbivores have evolved strategies to convergently target JA signaling. Here, we review the roles of JA signaling in the tripartite interactions among plant, virus, and insect vectors, with a focus on the molecular and biochemical mechanisms that drive vector-borne plant viral diseases. This knowledge is essential for the further design and development of effective strategies to protect viral damages, thereby increasing crop yield and food security.

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Next generation sequencing (NGS) as a multipurpose method for detection and differentiation of plant viruses

Progress in Plant Protection ◽

10.14199/ppp-2021-029 ◽

2021 ◽

Vol 61 (4) ◽

pp. 269-277

Keyword(s):

Next Generation Sequencing ◽

Molecular Mechanisms ◽

Environmental Changes ◽

Simultaneous Detection ◽

Disease Outbreaks ◽

Plant Viruses ◽

Next Generation ◽

Early Detection Of Disease ◽

Next Generation Sequencing Ngs ◽

Generation Sequencing

This paper describes the application of next generation sequencing (NGS) in plant virus research. Although NGS has not been routinely used yet, it is increasingly adopted in diagnostics and genomics of phytopathogens. NGS technics enable the simultaneous detection of multiple viruses present in infected material. This makes it possible not only to determine which viruses are present in a single sample but also to determine their concentration and genetic diversity. The simultaneous identification of many viruses, the possibility of early detection of disease outbreaks as well as tracking and monitoring of epidemic development, make NGS a universal research tool that enables not only the detection but also the understanding of molecular mechanisms allowing viruses to adapt to environmental changes (host plant genotype, vector, presence of other pathogens).

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