Restriction of viral dissemination from the midgut determines incompetence of small brown planthopper as a vector of Southern rice black-streaked dwarf virus

Jia, Dongsheng; Chen, Hongyan; Mao, Qianzhuo; Liu, Qifei; Wèi, Tàiyún

doi:10.1016/j.virusres.2012.05.023

Cited by 47 publications

(51 citation statements)

References 14 publications

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“…Although the data obtained here are not direct evidence, the greater ability of SRBSDV to multiply in insect vector cells than of RDV may be attributed to the assembly of progeny virions within the filamentous viroplasm matrix. Because a persistent-propagative plant virus must encounter multiple tissues barriers in the path from the alimentary canal to the salivary glands in the vector insect (1,2,14), the highly efficient propagation of SRBSDV in WBPH vectors may confer a greater ability for the virus to overcome these barriers, consistent with the fact that SRBSDV can be transmitted by WBPH vectors with high efficiency (14,16). These analyses suggest that SRBSDV, the first WBPH-borne reovirus, has evolved to be well adapted for persistent infection and maintenance in its WBPH vectors.…”

Section: Discussionmentioning

confidence: 99%

“…Cells were incubated with a 100-fold-diluted solution of the directly conjugated IgG. Cells were visualized with a Leica TCS SP5 confocal microscope as described previously (10,14).…”

Section: Methodsmentioning

confidence: 99%

“…Recombinant baculovirus vectors containing P5, P6, and P9-1 were introduced into DH10Bac (Invitrogen) for transposition into the bacmid. Sf9 cells were transfected with recombinant bacmids in the presence of Cellfectin (Invitrogen), incubated for 72 h, and then fixed in 4% paraformaldehyde and processed for immunofluorescence microscopy as described previously (10,14,24).…”

Section: Methodsmentioning

confidence: 99%

“…SRBSDV, transmitted by WBPH vectors in a persistent-propagative manner, has spread rapidly throughout southern China, northern Vietnam, and western Japan (10,(13)(14)(15)(16)(17)(18). SRBSDV virions are double shelled, spherical, and 65 to 70 nm in diameter (13,17,18).…”

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confidence: 99%

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New Model for the Genesis and Maturation of Viroplasms Induced by Fijiviruses in Insect Vector Cells

Mao

Zheng

Han

et al. 2013

J Virol

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Plant reoviruses are thought to replicate and assemble within cytoplasmic, nonmembranous structures called viroplasms. Here, we established continuous cell cultures of the white-backed planthopper (Sogatella furcifera Horváth) to investigate the mechanisms for the genesis and maturation of the viroplasm induced by Southern rice black-streaked dwarf virus (SRBSDV), a fijivirus in the family Reoviridae, during infection of its insect vector. Electron and confocal microscopy revealed that the viroplasm consisted of a granular region, where viral RNAs and nonstructural proteins P6 and P9-1 accumulated, and a filamentous region, where viral RNAs, progeny cores, viral particles, as well as nonstructural proteins P5 and P6 accumulated. Our results suggested that the filamentous viroplasm matrix was the site for the assembly of progeny virions. Because viral RNAs were produced by assembled core particles within the filamentous viroplasm matrix, we propose that these viral RNAs might be transported to the granular viroplasm matrix. P5 formed filamentous inclusions and P9-1 formed granular inclusions in the absence of viral infection, suggesting that the filamentous and granular viroplasm matrices were formed primarily by P5 and P9-1, respectively. P6 was apparently recruited in the whole viroplasm matrix by direct interaction with P9-1 and P5. Thus, the present results suggested that P5, P6, and P9-1 are collectively required for the genesis and maturation of the filamentous and granular viroplasm matrix induced by SRBSDV infection. Based on these results, we propose a new model to explain the genesis and maturation of the viroplasms induced by fijiviruses in insect vector cells.

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Section: Discussionmentioning

confidence: 99%

“…Cells were incubated with a 100-fold-diluted solution of the directly conjugated IgG. Cells were visualized with a Leica TCS SP5 confocal microscope as described previously (10,14).…”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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New Model for the Genesis and Maturation of Viroplasms Induced by Fijiviruses in Insect Vector Cells

Mao

Zheng

Han

et al. 2013

J Virol

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“…For many years, the midgut barrier has been believed to be the principal determinant of vector competence (1)(2)(3)(4)(5)(6)(7)(8)(9). For example, infection of the incompetent insect vectors of Rice dwarf virus and SRBSDV, two plant reoviruses, and Tomato spotted wilt virus (TSWV), a tospovirus, is restricted to the midgut epithelium (7)(8)(9)(10). The inability of incompetent insect vectors to transmit these viruses may be caused by a failure of the virus to efficiently replicate in or disseminate from the midgut epithelium (1)(2)(3)(4)(5).…”

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confidence: 99%

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Lan

Chen

Liu

et al. 2016

J Virol

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IMPORTANCE Many viral pathogens that cause significant global health and agricultural problems are transmitted via insect vectors. The first bottleneck in viral infection, the midgut epithelium, is a principal determinant of the ability of an insect species to transmit a virus. Southern rice black streaked dwarf virus (SRBSDV) is restricted exclusively to the midgut epithelium of an incompetent vector, the small brown planthopper (SBPH).Here, we show that silencing of the core component Dicer-2 of the small interfering RNA (siRNA) pathway increases viral titers in the midgut epithelium past the threshold (1.99 ؋ 10 9 copies of the SRBSDV P10 gene/g of midgut RNA) for viral dissemination into the midgut muscles and then into the salivary glands, allowing the SBPH to become a competent vector of SRBSDV. This result is the first evidence that the siRNA antiviral pathway has a direct role in the control of viral dissemination from the midgut epithelium and that it affects the competence of the virus's vector. Many viral pathogens that cause significant global health and agricultural problems are arthropod borne and transmitted via an insect vector. Many plant viruses are transmitted in a persistent manner by sap-sucking insects, including planthoppers, leafhoppers, thrips, and aphids (1-3). Plant viruses, when ingested by their insect vectors, establish their initial infection in the midgut epithelium, from where they disseminate to the midgut visceral muscles (1-3). The viruses then move from the midgut muscles into the hemolymph and finally into the salivary glands, from where they can be introduced into plant hosts (1-3). Efficient viral infection of the midgut epithelium, where initial infection is established, is thus a determinative factor in the ability of an insect species to transmit a certain plant virus.This ability of an insect species to transmit a virus, which has been described as vector competence, is common in nature (4, 5). For many years, the midgut barrier has been believed to be the principal determinant of vector competence (1-9). For example, infection of the incompetent insect vectors of Rice dwarf virus and SRBSDV, two plant reoviruses, and Tomato spotted wilt virus (TSWV), a tospovirus, is restricted to the midgut epithelium (7-10). The inability of incompetent insect vectors to transmit these viruses may be caused by a failure of the virus to efficiently replicate in or disseminate from the midgut epithelium (1-5). It is possible that viral titers in the midgut epithelium of incompetent vectors are unable to reach the threshold needed for viral dissemination. The innate immune response in the midgut epithelium may effectively control viral accumulation, thus blocking viral transmission by incompetent vectors. However, whether the initial antiviral immune pathway(s) in the insect midgut can modulate the competence of plant virus vectors is not unknown.Several mosquito and Drosophila innate immune responses have been reported to have an antiviral effect. These responses include RNA interfere...

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A systematic review of southern rice black‐streaked dwarf virus in the age of omics

Luo

Zhang

et al. 2023

Pest Management Science

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Southern rice black‐streaked dwarf virus (SRBSDV) is one of the most damaging rice viruses. The virus decreases rice quality and yield, and poses a serious threat to food security. From this perspective, this review performed a survey of published studies in recent years to understand the current status of SRBSDV and white‐backed planthopper (WBPH, Sogatella furcifera) transmission processes in rice. Recent studies have shown that the interactions between viral virulence proteins and rice susceptibility factors shape the transmission of SRBSDV. Moreover, the transmission of SRBSDV is influenced by the interactions between viral virulence proteins and S. furcifera susceptibility factors. This review focused on the molecular mechanisms of key genes or proteins associated with SRBSDV infection in rice via the S. furcifera vector, and the host defense response mechanisms against viral infection. A sustainable control strategy using RNAi was summarized to address this pest. Finally, we also present a model for screening anti‐SRBSDV inhibitors using viral proteins as targets. © 2023 Society of Chemical Industry.

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Restriction of viral dissemination from the midgut determines incompetence of small brown planthopper as a vector of Southern rice black-streaked dwarf virus

Cited by 47 publications

References 14 publications

New Model for the Genesis and Maturation of Viroplasms Induced by Fijiviruses in Insect Vector Cells

New Model for the Genesis and Maturation of Viroplasms Induced by Fijiviruses in Insect Vector Cells

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

A systematic review of southern rice black‐streaked dwarf virus in the age of omics

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