Leafhopper salivary vitellogenin mediates 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 how they facilitate plant virus transmission. Leafhopper Nephotettix cincticeps transmits important rice reovirus via virus-packaging exosomes released from salivary glands and then entering the rice phloem. Here, we report that intact salivary vitellogenin of N. cincticeps (NcVg) is associated with the GTPase Rab5 of N. cincticeps (NcRab5) for release from salivary glands. In virus-infected salivary glands, NcVg is upregulated and packaged into exosomes mediated by virus-induced NcRab5, subsequently entering the rice phloem. The released NcVg inherently suppresses H2O2 burst of rice plants by interacting with rice glutathione S-transferase F12, an enzyme catalyzing glutathione-dependent oxidation, thus facilitating leafhoppers feeding. When leafhoppers transmit virus, virus-upregulated NcVg thus promotes leafhoppers feeding and enhances viral transmission. Taken together, the findings provide evidence that viruses exploit insect exosomes to deliver virus-hijacked effectors for efficient transmission.