A leafhopper saliva protein mediates horizontal transmission of viral pathogens from insect vectors into rice phloem

Abstract

Numerous insects transmit viruses together with saliva to plant phloem, but the roles of saliva components remain elusive. Here, we report that calcium-binding protein (CBP), a universal insect saliva protein, is modified to benefit horizontal transmission of a devastating rice reovirus into plant phloem. CBP effectively competes with virus-induced filaments to target and traverse actin-based apical plasmalemma into saliva-stored cavities in salivary glands of leafhopper vector. Thus, the inhibition of CBP expression by viral infection facilitates filament-mediated viral secretion into salivary cavities and then into plant phloem. Furthermore, virus-mediated reduction of CBP secretion causes an increase of cytosolic Ca2+ levels in rice, triggering substantial callose deposition and H2O2 production. Thus, viruliferous vectors encounter stronger feeding barriers, probe more frequently, and secrete more saliva into plants, ultimately enhancing viral transmission. We thus conclude that the inhibition of CBP secretion facilitates viral secretion and increases host defense response to benefit viral transmission.

Calcium Signaling in Plant-Insect Interactions

“…CBPs are also involved in the transmission of devastating viruses into plant phloem. Viral infection may inhibit CBP expression and this event facilitates filament-mediated viral secretion first into salivary cavities and then into plant phloem which in rice causes an increased [Ca 2+ ] cyt , followed by a substantial H 2 O 2 production [ 67 ].…”

Plant Arbovirus Mobilizes a Vector Salivary Protein to Initiate Plant Infection

“…A recent study on leafhoppers revealed that the expression of a saliva calcium-binding protein is inhibited by rice gall dwarf virus (RGDV), thus causing an increase of cytosolic Ca 2+ levels in rice and triggering callose deposition and H 2 O 2 production. This increases the frequency of insect probing, thereby enhancing viral horizontal transmission into the rice phloem (Wu et al, 2022). Direct saliva protein-pathogen interactions have been reported in animal pathogens.…”

“…During plant virus transmission by piercing-sucking insects, arboviruses are inoculated into the plant phloem via the secreted insect's saliva (Arca & Ribeiro, 2018;Conway et al, 2016;Wu, Yi, Lv, Mao, & Wei, 2022). Thus, insect saliva acts as an interface for the virus-insect-host tripartite interaction and it can directly promote pathogen transmission to, and infection of, the hosts (Sun et al, 2020;Wu et al, 2022). However, despite the importance of insect salivary proteins in the tripartite interaction, there is still much to learn about how these proteins enable successful viral infection.…”

“…Callose is a β-(1,3)-D-glucan polysaccharide that is synthesized by callose synthases and degraded by β-(1,3)-glucanases. Plants can defend themselves by depositing callose at the sieve tubes in response to virus infection, whereas viruses can counter this by activating β-(1,3)-glucanases to degrade callose and unplug the sieve tube occlusions (Bucher et al, 2001;Hao et al, 2008;Wu et al, 2022;Zavaliev et al, 2011).…”

The cauliflower mosaic virus transmission helper protein P2 modifies directly the probing behavior of the aphid vector Myzus persicae to facilitate transmission

“…Such viruses traverse the intestine, cycle through the hemocoel and accumulate in the salivary glands, before inoculation as a saliva component into new plant hosts. During their passage, they can interact with various host organs, for example the brain, the salivary glands or antenna and modify vector behavior in ways that are conducive to virus transmission [ 18 – 20 ]. Similar manipulations have also been described for other pathogens that replicate in their vectors [ 21 ].…”