Plant Virus and Vector Insect Regulate the Dual Phosphorylation of ATG1–ATG13 To Maintain a Moderate Autophagy for Viral Persistent Propagation

Plant virus infection can trigger autophagy and remodel autophagosomes to benefit viral propagation in vector insects. Rice gall dwarf virus (RGDV) triggers the incomplete autophagy to promote viral spread in Recilia dorsalis, yet the autophagy initiation remains unclear. Here, we discovered that the dual-role ATG1–ATG13 complex acts as a crucial switch in initiating or inhibiting autophagy in RGDV-infected R. dorsalis. RGDV infection or microinjection of RGDV Pns11 reduces the accumulation of phosphorylated ATG1–ATG13 complex and stimulates autophagy in insects. Additionally, Pns11 interacts with ATG13 and recruits the phosphatase PP4C to effectively dephosphorylate ATG13 for stimulating autophagy in insects. However, p38 MAPK is dynamically upregulated to phosphorylate ATG1–ATG13 complex in RGDV-infected insects. Inhibiting the expression or kinase activity of p38 MAPK both promotes autophagosomes formation and viral propagation, but reduces the survival rate of insects. Taken together, these findings demonstrate how rice reoviruses and vector insects regulate the phosphorylation of the dual-role ATG1–ATG13 complex to maintain moderate autophagy for viral persistent propagation in insect vectors.