Leafhopper salivary vitellogenin mediates horizontal virus transmission to plant phloem

Abstract Salivary effectors of piercing-sucking insects can suppress plant defense to promote insect feeding, but it remains largely elusive that how they facilitate persistent plant virus transmission. Rice dwarf virus (RDV), an important rice reovirus, utilizes exosomes of the leafhopper vector, Nephotettix cincticeps, to release from salivary glands and enter the rice phloem for horizontal virus transmission. In this study, we report that the intact salivary vitellogenin (NcVg) of N. cincticeps associates with a small GTPase NcRab5 through interaction for release from salivary glands of leafhopper. When leafhoppers transmit RDV, NcVg is upregulated and packaged into exosomes mediated by the virus-induced NcRab5 in salivary glands, subsequently enters into the rice phloem. The released NcVg in rice phloem inherently suppresses H2O2 burst of rice plants by interacting with the rice glutathione S-transferase F12 (OsGSTF12), which catalyzes glutathione-dependent oxidation, thus facilitating leafhopper feeding. During viral transmission, virus-upregulated NcVg enhances suppression of H2O2 burst by improving the OsGSTF12 catalysis, promoting leafhopper feeding and viral transmission. We thus conclude that salivary NcVg mediates virus transmission from insect to plant phloem, via modulating insect resistance of plant hosts. Our findings provide the first evidence that viruses exploit insect exosomes to deliver virus-hijacked effectors, facilitating horizontal virus transmission.