Salivary gland morphology, tissue tropism and the progression of tospovirus infection in Frankliniella occidentalis

Montero-Astúa, Mauricio; Ullman, Diane E.; Whitfield, Anna E.

doi:10.1016/j.virol.2016.03.003

Cited by 53 publications

(55 citation statements)

References 71 publications

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“…With the creation of transcriptome sequence resources for F. occidentalis and improved proteomics technologies, we have identified the first thrips proteins that bind directly to the TSWV attachment protein, G N . With particular relevance to viral attachment to and internalization in epithelia, two TIPs (endocuticle structural glycoprotein, endoCP-G N and cyclophilin) were confirmed to interact directly with G N and were abundant in midgut and salivary gland tissues (21). These data may be the first indication of a protein(s) that serves ‘receptor-like’ roles in transmission biology of the tospoviruses.…”

Section: Discussionmentioning

confidence: 99%

“…For the virus and G N treatments, 25 μg/mL and 3.5 μg/mL of purified TSWV virions and recombinant G N glycoprotein, respectively, were incubated with membranes in blocking buffer at 4°C overnight with gentle rotating motion. Membranes were washed three times using PBST and were incubated with polyclonal rabbit anti-TSWV G N antiserum at 1:2,000 dilution in blocking buffer for 2 hours at room temperature (9, 21). After washing with PBST, membranes were incubated with HRP-conjugated goat-anti rabbit antiserum at 1:5,000 dilution in blocking buffer for 1 hour at room temperature.…”

Section: Methodsmentioning

confidence: 99%

“…Protein spots that were consistently identified in the 2-D gel overlays were selected and manually picked for analysis. The picked proteins were processed and subjected to ESI mass spectrometry as previously described (21). Protein spots (peptides) that had Mascot scores (Mascot v2.2) with significant matches ( P ≤ 0.05) to translated de novo -assembled contigs (all six frames) derived from mixed stages of F. occidentalis (“Fo Seq” 454-Sanger hybrid) (45) were identified and NCBI Blastx was performed on the contigs to provisionally annotate ( E < 10 −10 ) the protein and to predict conserved motifs using the contig as the query and the NCBI non-redundant protein database as the subject.…”

Section: Methodsmentioning

confidence: 99%

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Discovery of novel thrips vector proteins that bind to the viral attachment protein of the plant bunyavirus, tomato spotted wilt virus

Badillo-Vargas¹,

Chen

Martin

et al. 2018

Preprint

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16The plant-pathogenic virus, tomato spotted wilt virus (TSWV), encodes a structural 17 glycoprotein (G N ) that, like with other bunyavirus/vector interactions, serves a role in viral 18 attachment and possibly entry into arthropod vector host cells. It is well documented that 19Frankliniella occidentalis is one of seven competent thrips vectors of TSWV transmission to 20 plant hosts, however, the insect molecules that interact with viral proteins, such as G N , during 21 infection and dissemination in thrips vector tissues are unknown. The goals of this project 22 Importance Statement 37 Thrips-transmitted viruses cause devastating losses to numerous food crops worldwide. For 38 negative-sense RNA viruses that infect plants, the arthropod serves as a host as well by 39 supporting virus replication in specific tissues and organs of the vector. The goal of this work 40 was to identify vector/host proteins that bind directly to the viral attachment protein and thus 41 may play a role in the infection cycle in the insect. Using the model plant bunyavirus, tomato 42 spotted wilt virus (TSWV), and the most efficient thrips vector, we identified and validated 43 six TSWV-interacting proteins from Frankliniella occidentalis first instar larvae. Two 44 proteins, an endocuticle structural glycoprotein and cyclophilin, were able to interact directly 45 with the TSWV attachment protein, G N, in insect cells. The TSWV G N -interacting proteins 46 3 provide new targets for disrupting the virus-vector interaction and could be putative 47 determinants of vector competence. 48 49Vector-borne diseases caused by animal-and plant-infecting viruses are some of the 50 most important medical, veterinary, and agricultural problems worldwide (1, 2). The majority 51 of viruses infecting plants and animals are transmitted by arthropods. Understanding the viral 52 and arthropod determinants of vector competence is important for basic knowledge of virus-53 vector interactions and development of new interdiction strategies to control disease. 54Significant progress has been made towards identification of viral determinants of 55 transmission, but the interacting molecules in vectors remain largely elusive. For negative-56 sense RNA viruses, vector factors that mediate the transmission process have not been well 57 characterized. 58Bunyavirales is the largest order of negative-sense RNA viruses; twelve families are 59 described (http://www.ictvonline.org/virustaxonomy.asp). The Bunyavirales contains plant 60 and insect vector-infecting viruses that make up the Family Tospoviridae (3-5). Within this 61 family, there are eighteen species and several unassigned viruses that most likely will be 62 classified as unequivocal members of the Orthotospovirus genus. Tomato spotted wilt 63 orthotospovirus is the type species within this genus and has been best characterized in terms 64 of viral host range, genome organization and protein functions (6, 7). 65 Tomato spotted wilt virus (TSWV) infects both monocotyledonous and dicotyledonous 66 plants enc...

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Discovery of novel thrips vector proteins that bind to the viral attachment protein of the plant bunyavirus, tomato spotted wilt virus

Badillo-Vargas¹,

Chen

Martin

et al. 2018

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Saliva plays a crucial role in insect feeding behavior and virus transmission [91]. In thrips, the primary site of TSWV infections shifts from the midgut and tubular salivary glands in larvae to primary salivary glands in adult vectors [92]. This change in tissue tropism during insect development leads to virus accumulation ready for transmission.…”

Section: Critical Steps In Virus–insect Interactions As Potential mentioning

confidence: 99%

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Dietzgen

Mann

Johnson

2016

Viruses

191

142

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Acquisition and transmission by an insect vector is central to the infection cycle of the majority of plant pathogenic viruses. Plant viruses can interact with their insect host in a variety of ways including both non-persistent and circulative transmission; in some cases, the latter involves virus replication in cells of the insect host. Replicating viruses can also elicit both innate and specific defense responses in the insect host. A consistent feature is that the interaction of the virus with its insect host/vector requires specific molecular interactions between virus and host, commonly via proteins. Understanding the interactions between plant viruses and their insect host can underpin approaches to protect plants from infection by interfering with virus uptake and transmission. Here, we provide a perspective focused on identifying novel approaches and research directions to facilitate control of plant viruses by better understanding and targeting virus–insect molecular interactions. We also draw parallels with molecular interactions in insect vectors of animal viruses, and consider technical advances for their control that may be more broadly applicable to plant virus vectors.

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“…Generally, virions are secreted together with saliva to the salivary cavities and then to the canal in the stylet, to be ejected while insect vectors feed on susceptible hosts (1,4). Previous studies have focused on the routes for viral spread into the salivary glands of insect vectors (1,4,7,11). To be transmitted, persistent viruses must pass through the cavity apical plasmalemma of salivary gland cells, and thus, such plasmalemma represents the last membrane barrier for viral transmission by insect vectors (1,2,4,12).…”

mentioning

confidence: 99%

Filamentous Structures Induced by a Phytoreovirus Mediate Viral Release from Salivary Glands in Its Insect Vector

Mao

Liao

et al. 2017

J Virol

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Numerous viral pathogens are persistently transmitted by insect vectors and cause agricultural or health problems. These viruses circulate in the vector body, enter the salivary gland, and then are released into the apical plasmalemma-lined cavities, where saliva is stored. The cavity plasmalemma of vector salivary glands thus represents the last membrane barrier for viral transmission. Here, we report a novel mechanism used by a persistent virus to overcome this essential barrier. We observed that the infection by rice gall dwarf virus (RGDV), a species of the genus in the family, induced the formation of virus-associated filaments constructed by viral nonstructural protein Pns11 within the salivary glands of its leafhopper vector, Such filaments attached to actin-based apical plasmalemma and induced an exocytosis-like process for viral release into vector salivary gland cavities, through a direct interaction of Pns11 of RGDV and actin of Failure of virus-induced filaments assembly by RNA interference with synthesized double-stranded RNA targeting the Pns11 gene inhibited the dissemination of RGDV into salivary cavities, preventing viral transmission by For the first time, we show that a virus can exploit virus-induced inclusion as a vehicle to pass through the apical plasmalemma into vector salivary gland cavities, thus overcoming the last membrane barrier for viral transmission by insect vectors. Understanding how persistent viruses overcome multiple tissue and membrane barriers within the insect vectors until final transmission is the key for viral disease control. The apical plasmalemma of the cavities where saliva is stored in the salivary glands is the last barrier for viral transmission by insect vectors; however, the mechanism is still poorly understood. Here we show that a virus has evolved to exploit virus-induced filaments to perform an exocytosis-like process that enables viral passage through the apical plasmalemma into salivary cavities. This mechanism could be extensively exploited by other persistent viruses to overcome salivary gland release barriers in insect vectors, opening new perspectives for viral control.

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Salivary gland morphology, tissue tropism and the progression of tospovirus infection in Frankliniella occidentalis

Cited by 53 publications

References 71 publications

Discovery of novel thrips vector proteins that bind to the viral attachment protein of the plant bunyavirus, tomato spotted wilt virus

Discovery of novel thrips vector proteins that bind to the viral attachment protein of the plant bunyavirus, tomato spotted wilt virus

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Filamentous Structures Induced by a Phytoreovirus Mediate Viral Release from Salivary Glands in Its Insect Vector

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