scholarly journals Activation of Toll Immune Pathway in an Insect Vector Induced by a Plant Virus

2021 ◽  
Vol 11 ◽  
Author(s):  
Yu-Juan He ◽  
Gang Lu ◽  
Yu-Hua Qi ◽  
Yan Zhang ◽  
Xiao-Di Zhang ◽  
...  

The Toll pathway plays an important role in defense against infection of various pathogenic microorganisms, including viruses. However, current understanding of Toll pathway was mainly restricted in mammal and some model insects such as Drosophila and mosquitoes. Whether plant viruses can also activate the Toll signaling pathway in vector insects is still unknown. In this study, using rice stripe virus (RSV) and its insect vector (small brown planthopper, Laodelphax striatellus) as a model, we found that the Toll pathway was activated upon RSV infection. In comparison of viruliferous and non-viruliferous planthoppers, we found that four Toll pathway core genes (Toll, Tube, MyD88, and Dorsal) were upregulated in viruliferous planthoppers. When the planthoppers infected with RSV, the expressions of Toll and MyD88 were rapidly upregulated at the early stage (1 and 3 days post-infection), whereas Dorsal was upregulated at the late stage (9 days post-infection). Furthermore, induction of Toll pathway was initiated by interaction between a Toll receptor and RSV nucleocapsid protein (NP). Knockdown of Toll increased the proliferation of RSV in vector insect, and the dsToll-treated insects exhibited higher mortality than that of dsGFP-treated ones. Our results provide the first evidence that the Toll signaling pathway of an insect vector is potentially activated through the direct interaction between Toll receptor and a protein encoded by a plant virus, indicating that Toll immune pathway is an important strategy against plant virus infection in an insect vector.

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Wei Wang ◽  
Wan Zhao ◽  
Jing Li ◽  
Lan Luo ◽  
Le Kang ◽  
...  

No evidence has shown whether insect-borne viruses manipulate the c-Jun N-terminal kinase (JNK) signaling pathway of vector insects. Using a system comprising the plant virus Rice stripe virus (RSV) and its vector insect, the small brown planthopper, we have studied the response of the vector insect’s JNK pathway to plant virus infection. We found that RSV increased the level of Tumor Necrosis Factor-α and decreased the level of G protein Pathway Suppressor 2 (GPS2) in the insect vector. The virus capsid protein competitively bound GPS2 to release it from inhibiting the JNK activation machinery. We confirmed that JNK activation promoted RSV replication in the vector, whereas JNK inhibition caused a significant reduction in virus production and thus delayed the disease incidence of plants. These findings suggest that inhibition of insect vector JNK may be a useful strategy for controling the transmission of plant viruses.


2018 ◽  
Author(s):  
Gang Lu ◽  
Shuo Li ◽  
Changwei Zhou ◽  
Xin Qian ◽  
Qing Xiang ◽  
...  

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.


2014 ◽  
Vol 104 (7) ◽  
pp. 794-799 ◽  
Author(s):  
Shu Li ◽  
Han Wang ◽  
Guohui Zhou

Southern rice black-streaked dwarf virus (SRBSDV), a tentative species in the genus Fijivirus, family Reoviridae, is a novel rice virus transmitted by the white-backed planthopper (Sogatella furcifera). Since its discovery in 2001, SRBSDV has spread rapidly throughout eastern and southeastern Asia and caused large rice losses in China and Vietnam. Rice ragged stunt virus (RRSV) (genus Oryzavirus, family Reoviridae) is a common rice virus vectored by the brown planthopper (Nilaparvata lugens). RRSV is also widely distributed in eastern and southeastern Asia but has not previously caused serious problems in China owing to its low incidence. With SRBSDV's spread, however, RRSV has become increasingly common in China, and is frequently found in co-infection with SRBSDV. In this study, we show that SRBSDV and RRSV interact synergistically, the first example of synergism between plant viruses in the family Reoviridae. Rice plants co-infected with both viruses displayed enhanced stunting, earlier symptoms, and higher virus titers compared with singly infected plants. Furthermore, white-backed and brown planthoppers acquired SRBSDV and RRSV, respectively, from co-infected plants at higher rates. We propose that increased RRSV incidence in Chinese fields is partly due to synergism between SRBSDV and RRSV.


2004 ◽  
Vol 78 (10) ◽  
pp. 4976-4982 ◽  
Author(s):  
Ricardo B. Medeiros ◽  
Renato de O. Resende ◽  
Antonio Carlos de Ávila

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.


Life ◽  
2020 ◽  
Vol 10 (8) ◽  
pp. 143
Author(s):  
Priyanka Mittapelly ◽  
Swapna Priya Rajarapu

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.


Viruses ◽  
2020 ◽  
Vol 12 (2) ◽  
pp. 148 ◽  
Author(s):  
Xiujuan Wu ◽  
Jian Ye

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.


mBio ◽  
2020 ◽  
Vol 11 (4) ◽  
Author(s):  
Xiaofang Chen ◽  
Jinting Yu ◽  
Wei Wang ◽  
Hong Lu ◽  
Le Kang ◽  
...  

ABSTRACT Most plant viruses require vector insects for transmission. Viral stability in the hemolymph of vector insects is a prerequisite for successful transmission of persistent plant viruses. However, knowledge of whether the proteolytic activation of prophenoloxidase (PPO) affects the stability of persistent plant viruses remains elusive. Here, we explored the interplay between rice stripe virus (RSV) and the PPO cascade of the vector small brown planthopper. Phenoloxidase (PO) activity was suppressed by RSV by approximately 60%. When the PPO cascade was activated, we found distinct melanization around RSV particles and serious damage to viral stability in the hemolymph. Viral suppression of PO activity was derived from obstruction of proteolytic cleavage of PPOs by binding of the viral nonstructural protein NS3. These results indicate that RSV attenuates the PPO response to ensure viral stability in the hemolymph of vector insects. Our research provides enlightening cues for controlling the transmission of vector-borne viruses. IMPORTANCE Large ratios of vector-borne plant viruses circulate in the hemolymph of their vector insects before entering the salivary glands to be transmitted to plants. The stability of virions in the hemolymph is vital in this process. Activation of the proteolytic prophenoloxidase (PPO) to produce active phenoloxidase (PO) is one of the major innate immune pathways in insect hemolymph. How a plant virus copes with the PPO immune reaction in its vector insect remains unclear. Here, we report that the PPO affects the stability of rice stripe virus (RSV), a notorious rice virus, in the hemolymph of a vector insect, the small brown planthopper. RSV suppresses PPO activation using viral nonstructural protein. Once the level of PO activity is elevated, RSV is melanized and eliminated from the hemolymph. Our work gives valuable clues for developing novel strategies for controlling the transmission of vector-borne plant viruses.


Viruses ◽  
2021 ◽  
Vol 13 (6) ◽  
pp. 1121
Author(s):  
Marcia Beatriz Moya Fernández ◽  
Wenwen Liu ◽  
Lu Zhang ◽  
Jamal-U-Ddin Hajano ◽  
Xifeng Wang

Plant viruses transmitted by hemipteran vectors commonly cause losses to crop production. Rice stripe virus (RSV) and rice black streaked dwarf virus (RBSDV) are transmitted to rice plants by the same vector, the small brown planthopper (SBPH), Laodelphax striatellus Fallén, in a persistent propagative manner. However, rarely do the respective diseases they cause occur simultaneously in a field. Here, we determined the acquisition efficiency of RSV and RBSDV when acquired in succession or simultaneously by SBPH. When RBSDV was acquired first, RSV acquisition efficiency was significantly lower than when only acquiring RSV. However, RBSDV acquisition efficiency from insects that acquired RSV first was not significantly different between the insects only acquiring RBSDV. Immunofluorescence assays showed that the acquisition of RBSDV first might inhibit RSV entry into midgut epithelial cells, but RSV did not affect RBSDV entry. SBPHs were more likely to acquire RBSDV when they were feeding on plants coinfected with the two viruses. When RBSDV was acquired before RSV, RBSDV titer was significantly higher and RSV titer first declined, then increased compared to when only acquiring RBSDV or RSV. Only 5% of the SBPHs acquired both viruses when feeding on plants coinfected with RSV and RBSDV. These results provide a better understanding of the interaction between two persistent viruses when present in the same vector insect and explain why RSV and RBSDV occur in intermittent epidemics.


Agronomy ◽  
2021 ◽  
Vol 11 (8) ◽  
pp. 1451
Author(s):  
Anne-Katrin Kersten ◽  
Sabrina Scharf ◽  
Martina Bandte ◽  
Peer Martin ◽  
Peter Meurer ◽  
...  

Texture softening of pickled cucumbers does not meet consumers’ quality expectations and leads to economic losses. The factor(s) triggering this phenomenon is still unknown. We investigated the importance of plant viruses such as Cucumber green mottle mosaic tobamovirus (CGMMV) and Zucchini yellow mosaic potyvirus (ZYMV) in the context of softening of pickles. Cucumber plants (Cucumis sativus) were infected by mechanical inoculation, grown under greenhouse conditions and tested positive for the viral infection by ELISA. The severity of virus infection was reflected in yield and symptom expression. Histological and morphological alterations were observed. All fruits were pasteurized, separately stored in jars and subjected to texture measurements after four, six and 12 months. CGMMV-infections were asymptomatic or caused mild symptoms on leaves and fruit, and texture quality was comparable to control. At the same time, fruits of ZYMV-infected plants showed severe symptoms like deformations and discoloration, as well as a reduction in firmness and crunchiness after pasteurization. In addition, histological alterations were detected in such fruits, possibly causing textural changes. We conclude that plant viruses could have a considerable influence on the firmness and crunchiness of pickled cucumbers after pasteurization. It is possible that the severity of symptom expression has an influence on texture properties.


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