An Insect Effector Mimics Its Host Immune Regulator to Undermine Plant Immunity.

Abstract

Plants activate defense machinery when infested by herbivorous insects but avoid such costs in the absence of herbivory. However, the key signaling pathway regulators underlying such flexibility and the mechanisms that insects exploit these components to disarm plant defense systems remain elusive. Here, it is reported that immune repressor 14-3-3e in rice Oryza sativa (OsGF14e) regulates immune homeostasis. Infestation with brown planthopper (BPH) Nilaparvata lugens decreased OsGF14e expression; however, the level of downregulation is limited both by the short duration and the specific feeding location. OsGF14e interacts with Enhanced Disease Resistance 1-like (OsEDR1l), a Raf-like MAP kinase kinase kinase (MAPKKK), and repressed jasmonic acid, jasmonic acid-isoleucine, and H₂O₂ accumulation by enhancing OsEDR1l abundance and signaling ability. OsGF14e and OsEDR1l overexpression renders rice susceptible to BPH, whereas their knockout increases plant resistance but compromises rice growth and grain yield. Intriguingly, BPH 14-3-3e protein (Nl14) that shares high sequence homology and structural similarity with OsGF14e is identified from BPH saliva and egg-associated secretions. Mediated through BPH feeding and oviposition, Nl14, similar to OsGF14e, interacts with OsEDR1l and triggers the OsEDR1l signaling, thereby suppressing plant defenses and facilitating BPH infestation. Apparently, structural and functional mimicry makes it possible for this newly discovered BPH effector to exploit rice OsGF14e-EDR1l immune suppression module. The results reveal a novel mechanism deployed by herbivorous insects, in a manner similar to certain pathogen effectors, to evade host plant defenses by mimicking host immune regulators.