A double-agent microRNA regulates viral cross-kingdom infection in animals and plants

Plant arbovirus infection is regulated by a delicate interplay between virus, vector, and host. While microRNAs are known to be transmitted across species, their role as cross-kingdom effectors in influencing arbovirus infectious cycles remains poorly understood. Our study reveals the dual role of miR-263a, a conserved insect microRNA, in governing rice stripe virus (RSV) infection within both insect vector, small brown planthopper, and rice host. In the planthopper, miR-263a facilitates rice stripe virus accumulation through targeting a cathepsin B-like gene to inhibit apoptosis in midgut epithelial cells. Upon insect saliva secretion, miR-263a is delivered into rice, where it proceeds to upregulate the transcription factor GATA19, triggering an antiviral response. The increase of GATA19 levels hinders JAZ1 from binding with MYC2, thus activating jasmonate signaling pathway. This study reveals the function of a microRNA as a dual agent in modulating viral cross-kingdom infection.