A virus capsid component mediates virion retention and transmission by its insect vector

Chen, Angel Y.S.; Walker, G. P.; Carter, David; Ng, Jillian

doi:10.1073/pnas.1109384108

Cited by 101 publications

(123 citation statements)

References 36 publications

(53 reference statements)

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“…The molecular determinants of transmission have been explored for only a few phytopathosystems (compared to mammalian systems), with virus-vector interactions being the most extensively studied. Surface entities, such as virion capsid components, have been shown to be important for the retention and transmission of plant viruses (2), indicating the importance of pathogen surface properties in mediating these interactions. However, we have much less information regarding the molecular mechanisms of insect transmission of bacterial pathogens, specifically those infecting plants.…”

mentioning

confidence: 99%

O Antigen Modulates Insect Vector Acquisition of the Bacterial Plant Pathogen Xylella fastidiosa

Rapicavoli

Kinsinger

Perring

et al. 2015

Appl Environ Microbiol

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e Hemipteran insect vectors transmit the majority of plant pathogens. Acquisition of pathogenic bacteria by these piercing/sucking insects requires intimate associations between the bacterial cells and insect surfaces. Lipopolysaccharide (LPS) is the predominant macromolecule displayed on the cell surface of Gram-negative bacteria and thus mediates bacterial interactions with the environment and potential hosts. We hypothesized that bacterial cell surface properties mediated by LPS would be important in modulating vector-pathogen interactions required for acquisition of the bacterial plant pathogen Xylella fastidiosa, the causative agent of Pierce's disease of grapevines. Utilizing a mutant that produces truncated O antigen (the terminal portion of the LPS molecule), we present results that link this LPS structural alteration to a significant decrease in the attachment of X. fastidiosa to blue-green sharpshooter foreguts. Scanning electron microscopy confirmed that this defect in initial attachment compromised subsequent biofilm formation within vector foreguts, thus impairing pathogen acquisition. We also establish a relationship between O antigen truncation and significant changes in the physiochemical properties of the cell, which in turn affect the dynamics of X. fastidiosa adhesion to the vector foregut. Lastly, we couple measurements of the physiochemical properties of the cell with hydrodynamic fluid shear rates to produce a Comsol model that predicts primary areas of bacterial colonization within blue-green sharpshooter foreguts, and we present experimental data that support the model. These results demonstrate that, in addition to reported protein adhesin-ligand interactions, O antigen is crucial for vector-pathogen interactions, specifically in the acquisition of this destructive agricultural pathogen. Insect vectors transmit numerous pathogens to a wide range of animal and plant hosts. Hemipteran vectors, such as aphids, leafhoppers, and whiteflies, are an economically important group of insects because they are the dominant vectors of plant pathogens (1). The molecular determinants of transmission have been explored for only a few phytopathosystems (compared to mammalian systems), with virus-vector interactions being the most extensively studied. Surface entities, such as virion capsid components, have been shown to be important for the retention and transmission of plant viruses (2), indicating the importance of pathogen surface properties in mediating these interactions. However, we have much less information regarding the molecular mechanisms of insect transmission of bacterial pathogens, specifically those infecting plants.Xylella fastidiosa is a Gram-negative bacterium that causes diseases in several economically important crops, including Pierce's disease (PD) of grapevines, citrus variegated chlorosis, and almond leaf scorch. X. fastidiosa forms biofilms within the xylem vessels of plant hosts, which occludes vessels and impedes water flow within the vine (3). Symptoms of PD include marginal l...

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mentioning

confidence: 99%

O Antigen Modulates Insect Vector Acquisition of the Bacterial Plant Pathogen Xylella fastidiosa

Rapicavoli

Kinsinger

Perring

et al. 2015

Appl Environ Microbiol

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“…In contrast, persistent viruses circulate in the vector body and have developed intimate interactions with internal organs and components of vectors (1)(2)(3)(4)(5). Recent studies showed that the noncirculative Cauliflower mosaic virus (CaMV) and Lettuce infectious yellows virus (LIYV) were specifically retained in the stylet of an aphid and the foregut of a whitefly vector, respectively, and specific viral proteins bound to these retention sites correlated with virus transmission (6,7). These studies provided a better understanding of the transmission of noncirculative viruses by insect vectors.…”

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confidence: 99%

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Wei

Zhao

Zhang

et al. 2014

J Virol

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The majority of plant viruses are vectored by arthropods via persistent-circulative or noncirculative transmission. Previous studies have shown that specific binding sites for noncirculative viruses reside within the stylet or foregut of insect vectors, whereas the transmission mechanisms of circulative viruses remain ambiguous. Here we report the critical roles of whitefly primary salivary glands (PSGs) in the circulative transmission of two begomoviruses. The Middle East Asia Minor 1 (MEAM1) species of the whitefly Bemisia tabaci complex efficiently transmits both Tomato yellow leaf curl China virus (TYLCCNV) and Tomato yellow leaf curl virus (TYLCV), whereas the Mediterranean (MED) species transmits TYLCV but not TYLCCNV. PCR and fluorescence in situ hybridization experiments showed that TYLCCNV efficiently penetrates the PSGs of MEAM1 but not MED whiteflies. When a fragment of the coat protein of TYLCCNV was exchanged with that of TYLCV, mutated TYLCCNV accumulated in the PSGs of MED whiteflies, while mutant TYLCV was nearly undetectable. Confocal microscopy revealed that virion transport in PSGs follows specific paths to reach secretory cells in the central region, and the accumulation of virions in the secretory region of PSGs was correlated with successful virus transmission. Our findings demonstrate that whitefly PSGs, in particular the cells around the secretory region, control the specificity of begomovirus transmission. IMPORTANCEOver 75% of plant viruses are transmitted by insects. However, the mechanisms of virus transmission by insect vectors remain largely unknown. Begomoviruses and whiteflies are a complex of viruses and vectors which threaten many crops worldwide. We investigated the transmission of two begomoviruses by two whitefly species. We show that specific cells of the whitefly primary salivary glands control viral transmission specificity and that virion transport in the glands follows specific paths to reach secretory cells in the central region and then to reach the salivary duct. Our results indicate that the secretory cells in the central region of primary salivary glands determine the recognition and transmission of begomoviruses. These findings set a foundation for future research not only on circulative plant virus transmission but also on other human and animal viruses transmitted by arthropod vectors.

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“…Despite this diversity of both species and vectors, only the mechanism of whitefly transmission of lettuce infectious yellows virus (LIYV) has been studied in detail, and it was found that the minor coat protein, which encapsidates one end of the virion, binds directly to the cibarium of the insect foregut (2,8). CTV is one of the most destructive diseases in citrus (14).…”

Section: Importancementioning

confidence: 99%

“…The mechanisms by which viruses are transmitted by these insects have been classified into two general groups: circulative and noncirculative. More than half of the viruses with a described mode of transmission fall into the latter category and are defined by attachment to sites within the vector's stylet, cibarium, or foregut (2,3). There are also differences in both the acquisition and retention of noncirculative viruses (4), previously described as nonpersistent versus semipersistent.…”

mentioning

confidence: 99%

Minor Coat and Heat Shock Proteins Are Involved in the Binding of Citrus Tristeza Virus to the Foregut of Its Aphid Vector, Toxoptera citricida

Killiny

Harper

Alfaress

et al. 2016

Appl Environ Microbiol

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Vector transmission is a critical stage in the viral life cycle, yet for most plant viruses how they interact with their vector is unknown or is explained by analogy with previously described relatives. Here we examined the mechanism underlying the transmission of citrus tristeza virus (CTV) by its aphid vector, Toxoptera citricida, with the objective of identifying what virus-encoded proteins it uses to interact with the vector. Using fluorescently labeled virions, we demonstrated that CTV binds specifically to the lining of the cibarium of the aphid. Through in vitro competitive binding assays between fluorescent virions and free viral proteins, we determined that the minor coat protein is involved in vector interaction. We also found that the presence of two heat shock-like proteins, p61 and p65, reduces virion binding in vitro. Additionally, treating the dissected mouthparts with proteases did not affect the binding of CTV virions. In contrast, chitinase treatment reduced CTV binding to the foregut. Finally, competition with glucose, N-acetyl-␤-D-glucosamine, chitobiose, and chitotriose reduced the binding. These findings together suggest that CTV binds to the sugar moieties of the cuticular surface of the aphid cibarium, and the binding involves the concerted activity of three virus-encoded proteins. IMPORTANCELimited information is known about the specific interactions between citrus tristeza virus and its aphid vectors. These interactions are important for the process of successful transmission. In this study, we localized the CTV retention site as the cibarium of the aphid foregut. Moreover, we demonstrated that the nature of these interactions is protein-carbohydrate binding. The viral proteins, including the minor coat protein and two heat shock proteins, bind to sugar moieties on the surface of the foregut. These findings will help in understanding the transmission mechanism of CTV by the aphid vector and may help in developing control strategies which interfere with the CTV binding to its insect vector to block the transmission.T he survival of a virus is dependent on its ability to move from host to host, which for many plant viruses requires an insect vector (1). The mechanisms by which viruses are transmitted by these insects have been classified into two general groups: circulative and noncirculative. More than half of the viruses with a described mode of transmission fall into the latter category and are defined by attachment to sites within the vector's stylet, cibarium, or foregut (2, 3). There are also differences in both the acquisition and retention of noncirculative viruses (4), previously described as nonpersistent versus semipersistent. While there is no clear demarcation between the two, nonpersistent viruses can be acquired and disseminated through probing and salivation within a matter of minutes, while most semipersistent viruses may only be acquired and subsequently transmitted through deep phloem feeding, which generally requires hours for acquisition, and vectors remain vi...

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A virus capsid component mediates virion retention and transmission by its insect vector

Cited by 101 publications

References 36 publications

O Antigen Modulates Insect Vector Acquisition of the Bacterial Plant Pathogen Xylella fastidiosa

O Antigen Modulates Insect Vector Acquisition of the Bacterial Plant Pathogen Xylella fastidiosa

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Minor Coat and Heat Shock Proteins Are Involved in the Binding of Citrus Tristeza Virus to the Foregut of Its Aphid Vector, Toxoptera citricida

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