Rice stripe mosaic virus M protein antagonizes G-protein-induced antiviral autophagy in insect vectors

• Published in: PLoS pathogens Vol. 21; no. 4; p. e1013070
• Main Authors: Zhang, Ruonan, Wang, Tengfei, Cheng, Yu, Qiu, Jiaxin, Jia, Dongsheng, Chen, Hongyan, Wei, Taiyun, Zhang, Xiao-Feng
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 29.04.2025; Public Library of Science (PLoS)
• Subjects: Agricultural pests; Animals; Antiviral agents; Autophagy (Cytology); Autophagy - immunology; Beclin-1; Biology and Life Sciences; Causes of; Diseases and pests; Genetic aspects; GTP-Binding Proteins - metabolism; Health aspects; Hemiptera - immunology; Hemiptera - virology; Immunity; Infection; Insect Proteins - metabolism; Insect Vectors - immunology; Insect Vectors - virology; Insects as carriers of disease; Medical research; Medicine and Health Sciences; Medicine, Experimental; Oryza - virology; Physiological aspects; Plant diseases; Plant Diseases - virology; Plant viruses; Research and Analysis Methods; Rice; Tenuivirus - immunology; Tenuivirus - metabolism; Tenuivirus - pathogenicity; Viral proteins; Virus diseases of plants; Virus research; China; South Dakota
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1013070

In the field, 80% of plant viruses are transmitted by insect vectors. When ingested by a sap-sucking insect such as Recilia dorsalis , persistently transmitted viruses such as rice stripe mosaic virus (RSMV) infect the gut epithelium and eventually pass to the salivary glands where they will be transmitted to the next rice ( Oryza sativa ) plant. To efficiently exploit insect vectors for transmission, plant viruses must overcome various immune mechanisms within the vectors, including autophagy. However, understanding how plant viruses overcome insect autophagic defenses remains limited. In this study, we provide evidence that infection with RSMV triggers an autophagic antiviral response in leafhopper cells. In this response, the G protein of RSMV binds to a leafhopper AMP-activated protein kinase (AMPK), leading to enhanced phosphorylation of Beclin-1 (BECN1), thereby inducing autophagy. Knockdown of AMPK and genes encoding members of the phosphoinositide 3-kinase (PI3K) complex composed of the autophagy-related protein 14 (ATG14), BECN1, and vacuolar protein sorting 34 (VPS34) facilitated viral infection in leafhoppers. To suppress leafhopper-induced autophagy, RSMV M protein specifically interacts with ATG14, resulting in the disintegration of PI3K complexes. This leads to reduced phosphatidylinositol-3-phosphate content and thus inhibits the G-protein- induced autophagy. Our study sheds light on the mechanism by which this rice virus evades insect autophagy antiviral defenses.