Riptortus pedestris effector induces autophagy through interaction with ATG8, enhancing insect feeding

Autophagy is an evolutionarily conserved pathway in eukaryotes that delivers cytoplasmic cargos for vacuolar/lysosomal degradation. Plant pathogens have evolved various strategies to regulate host autophagy for successful infections. However, whether herbivores modulate host autophagy to facilitate feeding remains unclear. Previously, we identified a salivary protein RP246 from Riptortus pedestris, which enhances Spodoptera litura feeding when transiently expressed in Nicotiana benthamiana. This study further revealed that RP246 protein is delivered into the soybean plant during R. pedestris infestation. Targeted gene silencing of RP246 significantly reduced insect feeding duration, honeydew excretion, and body weight, demonstrating that RP246 functions as a virulent effector. Our findings further demonstrated that RP246 interacts with NbATG8 and GmATG8c, the core autophagy protein, using its AIM2 (ATG8-interacting motif2), and subsequently promotes the formation of autophagosomes. RP246-induced insect feeding depends on NbATG8, and treatment with the autophagy inhibitor, 3-methyladenine (3-MA), significantly inhibits R. pedestris feeding on soybean plants. Collectively, these findings revealed that RP246 activates plant autophagy to facilitate R. pedestris feeding by interacting with ATG8. Our findings uncovered a mechanism utilized by herbivores to facilitate infestation through hijacking the autophagy machinery of the plant.