The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid

Heuvel, J.F.J.M. van den; Bruyere, A.; Hogenhout, Saskia A.; Ziegler-Graff, Véronique; Brault, Véronique; Verbeek, M.; Wilk, F. van der; Richards, K.

doi:10.1128/jvi.71.10.7258-7265.1997

Cited by 147 publications

(65 citation statements)

References 68 publications

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“…Point mutations in the RTD impair transport of virions in the gut cells (15) and uptake by the accessory salivary glands (19)(20)(21)(22). Moreover, RTD interacts with GroEL produced by aphid endosymbionts, likely protecting the virus from destruction in the hemolymph (23). The specificity of poleroviruses with respect to their aphid vectors is determined by the N-terminal region of the RTD (18,23) and by its specificity in binding to the GroEL chaperonin of the aphid bacterial symbiont.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, RTD interacts with GroEL produced by aphid endosymbionts, likely protecting the virus from destruction in the hemolymph (23). The specificity of poleroviruses with respect to their aphid vectors is determined by the N-terminal region of the RTD (18,23) and by its specificity in binding to the GroEL chaperonin of the aphid bacterial symbiont. Despite the preexisting knowledge on polerovirus-aphid interactions, we cannot explain the nontransmissibil- ity of PeWBVYV by aphids.…”

Section: Discussionmentioning

confidence: 99%

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Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

Ghosh

Kanakala

Lebedev

et al. 2019

J Virol

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Many animal and plant viruses depend on arthropods for their transmission. Virus-vector interactions are highly specific, and only one vector or one of a group of vectors from the same family is able to transmit a given virus. Poleroviruses (Luteoviridae) are phloem-restricted RNA plant viruses that are exclusively transmitted by aphids. Multiple aphid-transmitted polerovirus species commonly infect pepper, causing vein yellowing, leaf rolling, and fruit discoloration. Despite low aphid populations, a recent outbreak with such severe symptoms in many bell pepper farms in Israel led to reinvestigation of the disease and its insect vector. Here we report that this outbreak was caused by a new whitefly (Bemisia tabaci)-transmitted polerovirus, which we named Pepper whitefly-borne vein yellows virus (PeWBVYV). PeWBVYV is highly (Ͼ95%) homologous to Pepper vein yellows virus (PeVYV) from Israel and Greece on its 5= end half, while it is homologous to African eggplant yellows virus (AeYV) on its 3= half. Koch's postulates were proven by constructing a PeWBVYV infectious clone causing the pepper disease, which was in turn transmitted to test pepper plants by B. tabaci but not by aphids. PeWBVYV represents the first report of a whitefly-transmitted polerovirus. IMPORTANCE The high specificity of virus-vector interactions limits the possibility of a given virus changing vectors. Our report describes a new virus from a family of viruses strictly transmitted by aphids which is now transmitted by whiteflies (Bemisia tabaci) and not by aphids. This report presents the first description of polerovirus transmission by whiteflies. Whiteflies are highly resistant to insecticides and disperse over long distances, carrying virus inoculum. Thus, the report of such unusual polerovirus transmission by a supervector has extensive implications for the epidemiology of the virus disease, with ramifications concerning the international trade of agricultural commodities.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

Ghosh

Kanakala

Lebedev

et al. 2019

J Virol

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“…Buchnera GroEL homologues are found in most aphid taxa and are immunologically closely related. Structural characteristics of Buchnera GroEL are highly similar to those of GroEL of E. coli, and a Ͼ80% sequence identity is present in functionally significant regions (Filichkin et al, 1997;Hogenhout et al, 1998;Ohtaka et al, 1992;van den Heuvel et al, 1994van den Heuvel et al, , 1997. However, unlike E. coli GroEL, Buchnera GroEL is not restricted to the cytosol of the bacteria.…”

Section: Introductionmentioning

confidence: 95%

“…Viruses from the genera Luteovirus, Polerovirus, and Enamovirus display a specific but differential affinity for this protein, which is produced by the primary endosymbiont (a Buchnera sp.) of aphids (van den Heuvel et al, 1994Heuvel et al, , 1997Filichkin et al, 1997). These gram-negative bacteria are harboured in the aphid's haemocoel by specialized polyploid cells, called mycetocytes (Buchner, 1965), and are distantly related to Escherichia coli (Unterman et al, 1989).…”

Section: Introductionmentioning

confidence: 99%

A GroEL Homologue from Endosymbiotic Bacteria of the WhiteflyBemisia tabaciIs Implicated in the Circulative Transmission of Tomato Yellow Leaf Curl Virus

et al. 1999

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Evidence for the involvement of a Bemisia tabaci GroEL homologue in the transmission of tomato yellow leaf curl geminivirus (TYLCV) is presented. A approximately 63-kDa protein was identified in B. tabaci whole-body extracts using an antiserum raised against aphid Buchnera GroEL. The GroEL homologue was immunolocalized to a coccoid-shaped whitefly endosymbiont. The 30 N-terminal amino acids of the whitefly GroEL homologue showed 80% homology with that from different aphid species and GroEL from Escherichia coli. Purified GroEL from B. tabaci exhibited ultrastructural similarities to that of the endosymbiont from aphids and E. coli. In vitro ligand assays showed that tomato yellow leaf curl virus (TYLCV) particles displayed a specific affinity for the B. tabaci 63-kDa GroEL homologue. Feeding whiteflies anti-Buchnera GroEL antiserum before the acquisition of virions reduced TYLCV transmission to tomato test plants by >80%. In the haemolymph of these whiteflies, TYLCV DNA was reduced to amounts below the threshold of detection by Southern blot hybridization. Active antibodies were recovered from the insect haemolymph suggesting that by complexing the GoEL homologue, the antibody disturbed interaction with TYLCV, leading to degradation of the virus. We propose that GroEL of B. tabaci protects the virus from destruction during its passage through the haemolymph.

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“…Experiments with the nonenveloped plant viruses Luteovirus and Begomovirus revealed that they interact with GroEL, a chaperone of a symbiotic bacterium in aphid vectors (94,95). This interaction is required for circulative transmission and protects against degradation in the vector (96,97). Chaperones are not only involved in protein folding but also in membrane translocation.…”

Section: The Viral Envelope As An Adaptation To Animal Cellsmentioning

confidence: 99%

Cell Walls and the Convergent Evolution of the Viral Envelope

Buchmann

Holmes

2015

Microbiol Mol Biol Rev

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SUMMARYWhy some viruses are enveloped while others lack an outer lipid bilayer is a major question in viral evolution but one that has received relatively little attention. The viral envelope serves several functions, including protecting the RNA or DNA molecule(s), evading recognition by the immune system, and facilitating virus entry. Despite these commonalities, viral envelopes come in a wide variety of shapes and configurations. The evolution of the viral envelope is made more puzzling by the fact that nonenveloped viruses are able to infect a diverse range of hosts across the tree of life. We reviewed the entry, transmission, and exit pathways of all (101) viral families on the 2013 International Committee on Taxonomy of Viruses (ICTV) list. By doing this, we revealed a strong association between the lack of a viral envelope and the presence of a cell wall in the hosts these viruses infect. We were able to propose a new hypothesis for the existence of enveloped and nonenveloped viruses, in which the latter represent an adaptation to cells surrounded by a cell wall, while the former are an adaptation to animal cells where cell walls are absent. In particular, cell walls inhibit viral entry and exit, as well as viral transport within an organism, all of which are critical waypoints for successful infection and spread. Finally, we discuss how this new model for the origin of the viral envelope impacts our overall understanding of virus evolution.

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The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid

Cited by 147 publications

References 68 publications

Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

A GroEL Homologue from Endosymbiotic Bacteria of the WhiteflyBemisia tabaciIs Implicated in the Circulative Transmission of Tomato Yellow Leaf Curl Virus

Cell Walls and the Convergent Evolution of the Viral Envelope

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