Abstract

BACKGROUND Insect-borne viruses represent a major threat to global agriculture and public health. Rice ragged stunt virus (RRSV), a destructive pathogen transmitted by brown planthopper (Nilaparvata lugens Stå), lacks comprehensive understanding of the molecular mechanisms underlying its replication and transmission. RESULTS This study reveals that the RRSV P6 protein serves as a key regulator of vector-borne transmission by sequentially interacting with RTE1-HOMOLOG 2 (OsRTH2) and ETHYLENE-INSENSITIVE3-LIKE 2 (OsEIL2) in the host ethylene signaling pathway. This biphasic strategy manipulates brown planthopper (BPH) behavior, initially promoting viral replication and subsequently facilitating epidemic spread. Furthermore, the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) significantly impairs BPH fitness, reducing survival and fecundity. CONCLUSIONS Our study elucidates how a plant virus manipulates the host ethylene signaling pathway to promote its own replication and transmission. Moreover, we identify the ethylene biosynthesis precursor ACC as a potential, environmentally friendly control agent against brown planthoppers. © 2026 Society of Chemical Industry.