The c-Jun N-terminal kinase pathway of a vector insect is activated by virus capsid protein and promotes viral replication

Wang, Wei; Zhao, Wan; Li, Jing; Li, Luo; Kang, Le; Cui, Feng

doi:10.7554/elife.26591

Cited by 47 publications

(56 citation statements)

References 32 publications

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“…One interaction consists of LsST6-CP binding, which mediates viral entry into midgut epithelial cells [18]. Another is GPS2-CP binding, an interaction that activates the SBPH JNK signaling pathway in the midgut, which is beneficial to viral replication [24]. With respect to the salivary gland barrier, only CPR1 or GPS2-CP binding were reported to facilitate viral movement in the salivary glands [23,24].…”

Section: Discussionmentioning

confidence: 99%

“…Another is GPS2-CP binding, an interaction that activates the SBPH JNK signaling pathway in the midgut, which is beneficial to viral replication [24]. With respect to the salivary gland barrier, only CPR1 or GPS2-CP binding were reported to facilitate viral movement in the salivary glands [23,24]. The spread of RSV in SBPH is obviously complex and requires multiple components.…”

Section: Discussionmentioning

confidence: 99%

“…We previously reported that RSV was horizontally transmitted to rice plants via salivation during the feeding of insect vectors [21]. A series of salivary-specific transcriptome and proteome analyses revealed numerous genes involved in RSV transmission [22,23]; however, only cuticular protein (CPR1) and a G protein pathway suppressor 2 (GPS2) impacted RSV transmission and replication in salivary glands [23,24]. Obviously, the mechanism that RSV uses to overcome the salivary gland barrier and then undergo horizontal transmission to the plant warrants further investigation.…”

Section: Introductionmentioning

confidence: 99%

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The α-tubulin of Laodelphax striatellus facilitates the passage of rice stripe virus (RSV) and enhances horizontal transmission

Chen

et al. 2018

Preprint

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14Rice stripe virus (RSV), causal agent of rice stripe disease, is transmitted by the small 15 brown planthopper (SBPH, Laodelphax striatellus) in a persistent manner. The midgut and 16 salivary glands of SBPH are the first and last barriers in viral circulation and transmission, 17 respectively; however, the precise mechanisms used by RSV to cross these organs and 18 re-inoculate rice have not been fully elucidated. We obtained full-length cDNA of L. 19 striatellus α-tubulin 2 (LsTUB) and found that RSV infection increased the level of LsTUB 20 in vivo. Furthermore, LsTUB was shown to bind the RSV nonstructural protein 3 (NS3) in 21 vitro. RNAi was used to reduce LsTUB expression, which caused a significant reduction in 22 RSV titer, NS3 expression, RSV inoculation rates, and transmission to healthy plants. 23 Electrical penetration graphs (EPG) showed that LsTUB knockdown by RNAi did not 24 impact SBPH feeding; therefore, the reduction in RSV inoculation rate was likely caused 25 by the decrease in RSV transmission. These findings suggest that LsTUB mediates the 26 passage of RSV through midgut and salivary glands and leads to successful horizontal 27 transmission. 30The survival of plant viruses is largely dependent on the efficient transmission to plant 31 hosts by viral-specific vector(s) [1,2]. Insects transmit over 70% of all known plant viruses 32 [3]. Hemipteran insects (e.g. leafhoppers, planthoppers, aphids and whiteflies), transmit 33 approximately 55% of insect-vectored plant viruses; as these insects have distinctive 34 piercing-sucking mouthparts with needle-like stylet bundles that are comprised of two 35 maxillary and two mandibular stylets [3-5]. Four categories of insect vector -plant virus 36 transmission relationships have been described as follows: non-persistent; semi-persistent; 37 persistent: propagative and persistent: circulative [2,6]. Plant viruses with persistent 38 relationships enter vectors via the gut, pass through various tissues and ultimately reach the 39 salivary glands and ovaries. Viruses are transmitted horizontally from the salivary glands 40 of the vector into healthy plants and are vertically transmitted from female ovaries to 41 offspring [7]. Barriers to the persistent transmission of plant viruses in insect vectors 42 include the following: (i) midgut infection barriers; (ii) dissemination barriers, including 43 midgut escape and salivary gland infection barriers; (iii) salivary gland escape barriers; and 44 (iv) transovarial transmission barriers [8,9]. A deeper understanding of the mechanistic 45 basis of virus transmission through these four barriers will facilitate the development of 46 novel methods to control the systemic spread of plant viruses [10]. 47 Previous studies demonstrated that the persistent transmission of viruses in 48 different insect tissues requires specialized interactions between components of the virus 49 and vector. For example, in the aphid Myzus persicae, the coat protein read-through 50 domain (CP-RTD) of Beet western yellows virus...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The α-tubulin of Laodelphax striatellus facilitates the passage of rice stripe virus (RSV) and enhances horizontal transmission

Chen

et al. 2018

Preprint

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“…A 168 bp fragment of LsACE, 142 bp fragment of RdRp, 142 bp fragment of NS2, 148 bp fragment of NSvc2, 129 bp fragment of NS3, 60 bp fragment of CP, 152 bp fragment of SP, and 128 bp fragment of NSvc4 were amplified using real-time quantitative PCR (qPCR) to quantify the relative RNA levels of respective genes in planthoppers and rice plants. A 64 bp fragment of the planthopper elongation factor 2 gene (EF2, Wang et al, 2017) and a 185 bp fragment of the rice ubiquitin 5 gene (AK061988) were quantified to normalize the cDNA templates of insect and plant samples, respectively. The primers are listed in Table S1 qPCR was performed on a Light Cycler 480 II (Roche, Basel, Switzerland).…”

Section: Real-time Quantitative Pcrmentioning

confidence: 99%

Immune function of an angiotensin-converting enzyme against Rice stripe virus infection in a vector insect

Wang

Zhang

et al. 2019

Virology

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Angiotensin-converting enzyme (ACE) plays diverse roles in the animal kingdom. However, whether ACE plays an immune function against viral infection in vector insects is unclear. In this study, an ACE gene (LsACE) from the small brown planthopper was found to respond to Rice stripe virus (RSV) infection. The enzymatic activities of LsACE were characterized at different pH and temperature. Twenty planthopper proteins were found to interact with LsACE. RSV infection significantly upregulated LsACE expression in the testicle and fat body. When the expression of LsACE in viruliferous planthoppers was inhibited, the RNA level of the RSV SP gene was upregulated 2-fold in planthoppers, and all RSV genes showed higher RNA levels in the rice plants consumed by these planthoppers, leading to a higher viral infection rate and disease rating index. These results indicate that LsACE plays a role in the immune response against RSV transmission by planthoppers.

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“…Each RNA segment binds multiple copies of capsid protein (CP) to form ribonucleoprotein (RNP), the minimal infectious unit . Thus, the amount of CP protein or the RNA level of the CP gene is generally believed to reflect viral load and has been widely used to detect or quantify RSV virions in insect vectors and plant hosts . The disease‐specific protein (SP) plays a critical role in RSV spreading within planthoppers and is positively correlated with the rice stripe symptoms though damaging grana stacks of the chloroplast …”

Section: Introductionmentioning

confidence: 99%

Evaluation of Rice stripe virus transmission efficiency by quantification of viral load in the saliva of insect vector

Zhao

Wang

et al. 2019

Pest Management Science

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BACKGROUND: Persistent plant viruses transfer from insect gut to the hemolymph, and finally to the salivary glands before inoculation into the plant hosts with saliva during insect feeding. Virus accumulation in saliva is an important indicator for the transmission ability of an insect vector. In order to evaluate the transmission ability of the small brown planthopper to rice stripe virus (RSV), we successfully measured accumulation of RSV in the saliva of planthoppers via the absolute real-time quantitative polymerase chain reaction method by quantifying the copy numbers of viral genes. RESULTS: After feeding on an artificial diet for 24 h, the copy numbers of viral genes of capsid protein (CP) and disease-specific protein (SP) can be detected in the saliva collected from as few as ten viruliferous planthoppers and ten non-viruliferous planthoppers after infected with RSV for 7 days. When the expression of planthopper G protein pathway suppressor 2 or c-JunN-terminal kinase was knocked down, the copy numbers of CP and SP in the saliva varied accordingly. CONCLUSION: Our study provided an accurate and convenient detection system to evaluate the transmission efficiency of RSV by small brown planthoppers, and this method may also be suitable for other persistent plant viruses.

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The c-Jun N-terminal kinase pathway of a vector insect is activated by virus capsid protein and promotes viral replication

Cited by 47 publications

References 32 publications

The α-tubulin of Laodelphax striatellus facilitates the passage of rice stripe virus (RSV) and enhances horizontal transmission

The α-tubulin of Laodelphax striatellus facilitates the passage of rice stripe virus (RSV) and enhances horizontal transmission

Immune function of an angiotensin-converting enzyme against Rice stripe virus infection in a vector insect

Evaluation of Rice stripe virus transmission efficiency by quantification of viral load in the saliva of insect vector

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