Abstract

Arthropod-borne viruses cause serious threats to human health and global agriculture by rapidly spreading via insect vectors. Southern rice black-streaked dwarf virus (SRBSDV) is the most damaging rice-infecting virus that is frequently transmitted by planthoppers. However, the molecular mechanisms underlying its propagation in the host plants and epidemics in the field are largely unknown. Here, we showed that the SRBSDV-encoded P6 protein is a key effector that regulates rice ethylene signaling to coordinate viral infection and transmission. In early SRBSDV infection, P6 interacts with OsRTH2 in the cytoplasm to activate ethylene signaling and enhance SRBSDV proliferation; this also repels the insect vector to reduce infestation. In late infection, P6 enters the nucleus, where it interacts with OsEIL2, a key transcription factor of ethylene signaling. The P6-OsEIL2 interaction suppresses ethylene signaling by preventing the dimerization of OsEIL2, thereby facilitating viral transmission by attracting the insect vector. Collectively, these findings reveal a novel molecular mechanism by which an arbovirus modulates the host defense system to promote viral infection and transmission.