Extracellular vesicle-mediated plant miRNA trafficking regulates viral infection in insect vector

Extracellular vesicle (EV)-mediated small RNA trafficking plays an important role in intercellular and interspecies communication. Plant arboviruses keep homeostasis in insect vectors, thus ensuring vector survival and viral transmission. How plant EV-mediated cross-kingdom RNA interference participates in viral infection in insect vectors remains unknown. Here, we successfully isolate rice EVs and identify a batch of microRNAs (miRNAs) encapsulated in EVs. Two EV-enriched rice miRNAs, Osa-miR159a.1-1 and Osa-miR167a, are transported into midgut epithelial cells of small brown planthopper, which is a competent vector of rice stripe virus (RSV). Osa-miR159a.1-1 elevates the expression of a phospholipase C by enhancing its mRNA stability, inducing the downstream CSL expression to inhibit apoptosis for the benefit of RSV replication. On the other hand, Osa-miR167a directly binds RSV RdRp to suppress viral replication. This differential regulation of EV-mediated cross-kingdom RNA interference contributes to arbovirus homeostasis in insect vectors and the following efficient transmission.