A Plant Virus Glycoprotein Induces Autophagy by Activating the Toll7 Immune Pathway in Its Insect Vector

The Toll7 pathway is crucial in defending against diverse pathogenic microorganisms, including viruses. This study reveals that a plant virus (rice stripe virus, RSV) infection activates Toll7-mediated antiviral response in the insect vector Laodelphax striatellus. We identified a specific interaction between the TIR domain of Toll7 and RSV glycoprotein (Gc). Furthermore, Toll7 silencing significantly enhanced RSV replication and acquisition, suggesting its antiviral role in L. striatellus. Transcriptomic analysis indicated that Toll7 negatively regulates the PI3K-Akt-mTOR pathway, a key autophagy regulator. Toll7 knockdown upregulated the expression of PI3K, Akt and mTOR; simultaneously, autophagy-related genes (Atg3, Atg5, Atg8, Atg9, Torc1 and ULK1) were downregulated and autophagy inhibitor Sqstm1 was upregulated. Conversely, silencing PI3K, Akt or mTOR suppressed RSV replication, highlighting the essential role of this pathway in viral persistence within its vector. These findings demonstrate that Toll7-mediated inhibition of the PI3K-Akt-mTOR pathway activates autophagy, restricting RSV replication in L. striatellus. This study uncovers a conserved Toll7-dependent antiviral mechanism modulating autophagy to inhibit viral infection, offering new insights into the co-evolutionary dynamics between plant viruses and insect vectors.