Rice virus release from the planthopper salivary gland is independent of plant tissue recognition by the stylet

Abstract

BackgroundThe transmission of plant viruses by arthropod vectors is closely related to feeding behavior. For persistently transmitted viruses, virus release means that virus moves through the salivary gland microvillus barriers of insects into plant via the stylet. However, whether virus release is dependent on plant tissue and component recognition by the stylet is unclear.ResultsIn this study, the small brown planthopper (SBPH) and two rice viruses transmitted by it were used as a model to explore this question. After the viruliferous insects penetrated a stretched membrane without plant tissue structure and ingested liquid food (rice sap, nutrient solution or water), both viruses were detected in the liquid food after only a 6 min inoculation access period, suggesting that the viruses were released from SBPH salivary gland independent of plant tissue and component recognition by the stylet. In subsequent electrical penetration graph (EPG) analysis, N4a‐like and N4b‐like waveforms, similar to N4a (phloem salivation before ingestion) and N4b (sieve element ingestion), were observed during SBPH penetrating the membrane, exhibiting normal feeding activity of planthopper on membrane, which further demonstrated that virus release from salivary gland was along with feeding activity, without the stylet sensing plant tissue. EPG analysis and identification of salivary proteins indicated more active feeding behavior and efficient salivation in viruliferous planthoppers.ConclusionThese results suggest that the rice virus is released from insect salivary gland independent of plant tissue and component recognition by the stylet, and the simple virus release mode facilitates virus transmission by vectors. © 2020 Society of Chemical Industry

Identification of Riptortus pedestris Salivary Proteins and Their Roles in Inducing Plant Defenses

“…To identify the salivary proteins commonly identified in R. pedestris and other pierce-sucking insects, comparative analysis was performed by local BLAST alignment. The salivary proteins used as queries were collected from Sternorrhyncha species [ 6 , 7 , 8 , 12 , 36 , 37 , 38 , 39 ], Auchenorrhyncha species [ 9 , 10 , 40 , 41 ], Heteroptera species [ 42 , 43 , 44 , 45 ], and Lepidopteran species [ 46 , 47 , 48 ]. The proteins with high sequence homology (an E-value cut-off of 10 −5 ) were further BLAST searched against the NCBI database.…”

“…The identification of saliva components is the first step in understanding their functions. In recent decades, with the development of omic technology, salivary proteins from some agriculturally important pests have been reported, including aphids [ 6 , 7 , 8 ], planthoppers [ 9 , 10 ], leafhoppers [ 11 ], whiteflies [ 12 ], and spider mites [ 13 , 14 , 15 ]. However, the current knowledge on the salivary components of herbivores in true bugs is still limited.…”

Hemipteran-Transmitted Plant Viruses: Research Progress and Control Strategies

“…In vector insects, when the virus is secreted along with saliva the interaction between the saliva and plants not only regulates the plant defense but also affects the virus spread [55] . In L. striatellus, RSV and RBSDV infection stimulate the insect to secrete more salivary proteins [56] . As an example of salivary mucin, which is an important component of the salivary sheath that accounts for continual insect feeding [57][58][59] , RSV infection significantly induces the expression of mucin, which might promote insect performance and virus transmission [56,60] .…”

“…In L. striatellus, RSV and RBSDV infection stimulate the insect to secrete more salivary proteins [56] . As an example of salivary mucin, which is an important component of the salivary sheath that accounts for continual insect feeding [57][58][59] , RSV infection significantly induces the expression of mucin, which might promote insect performance and virus transmission [56,60] . The regulation of salivary secretion by viruses was also reported in TYLCVinfected B. tabaci [61] .…”

Membrane association of importin α facilitates viral entry into salivary gland cells of vector insects

“…Many plant viruses are transmitted by vector insects in a persistent, circulative mode, which is characterized by systemic invasion of diverse tissues prior to entering salivary glands and release in saliva (9)(10)(11)(12)(13). The salivary glands are the last barriers for viral transmission to overcome (14)(15)(16)(17)(18). Unfortunately, the molecular mechanisms underlying viral entry into salivary-gland cells are not well known.…”