Vitellogenin from planthopper oral secretion acts as a novel effector to impair plant defenses

Abstract

Vitellogenin (Vg) is a well-known nutritious protein involved in reproduction in nearly all oviparous animals, including insects. Recently, Vg has been detected in saliva proteomes of several piercing–sucking herbivorous arthropods, including the small brown planthopper (Laodelphax striatellus, SBPH). Its function, however, remains unexplored. We investigated the molecular mechanism underlying SBPH orally secreted Vg-mediated manipulation of plant–insect interaction by RNA interference, phytohormone and H2O2 profiling, protein–protein interaction studies and herbivore bioassays. A C-terminal polypeptide of Vg (VgC) in SBPH, when secreted into rice plants, acted as a novel effector to attenuate host rice defenses, which in turn improved insect feeding performance. Silencing Vg reduced insect feeding and survival on rice. Vg-silenced SBPH nymphs consistently elicited higher H2O2 production, a well-established defense mechanism in rice, whereas expression of VgC in planta significantly hindered hydrogen peroxide (H2O2) accumulation and promoted insect performance. VgC interacted directly with the rice transcription factor OsWRKY71, a protein which is involved in induction of H2O2 accumulation and plant resistance to SBPH. These findings indicate a novel effector function of Vg: when secreted into host rice plants, this protein effectively weakened H2O2-mediated plant defense through its association with a plant immunity regulator.