Silencing the Autophagy-Related Genes ATG3 and ATG9 Promotes SRBSDV Propagation and Transmission in Sogatella furcifera

SIMPLE SUMMARY: Plant viruses are mostly transmitted by insects and cause severe damage to crops. The southern rice black-streaked dwarf virus is a rice virus exclusively transmitted by a planthopper, Sogatella furcifera. Autophagy is usually initiated as an adaptive response for cell survival in unfavorable conditions, such as pathogen invasion. The invasion of the virus in the vector may elicit autophagy and may subsequently function to suppress or promote virus propagation and transmission in the insect vector. Here, we annotated two key autophagy-related genes, SfATG3 and SfATG9, in the planthopper vector and found that the genes are conserved among various insects. Interestingly, exposure of the vector to the virus activated the expression of SfATG3 and SfATG9, and silencing SfATG3 or SfATG9 promoted propagation and transmission rates of the virus. These results indicate that the expression of autophagy-related genes is initiated in the vector following exposure to the virus and that autophagy-related genes functions to suppress SRBSDV propagation and transmission. ABSTRACT: Autophagy plays diverse roles in the interaction among pathogen, vector, and host. In the plant virus and insect vector system, autophagy can be an antiviral/pro-viral factor to suppress/promote virus propagation and transmission. Here, we report the antiviral role of autophagy-related genes ATG3 and ATG9 in the white-backed planthopper (Sogatella furcifera) during the process of transmitting the southern rice black-streaked dwarf virus (SRBSDV). In this study, we annotated two autophagy-related genes, SfATG3 and SfATG9, from the female S. furcifera transcriptome. The cDNA of SfATG3 and SfATG9 comprised an open reading frame (ORF) of 999 bp and 2295 bp that encodes a protein of 332 and 764 amino acid residues, respectively. SfATG3 has two conserved domains and SfATG9 has one conserved domain. In S. furcifera females exposed to SRBSDV, expression of autophagy-related genes was significantly activated and shared similar temporal patterns to those of SRBSDV S9-1 and S10, all peaking at 4 d post viral exposure. Silencing the expression of SfATG3 and SfATG9 promoted SRBSDV propagation and transmission. This study provides evidence for the first time that S. furcifera autophagy-related genes ATG3 and ATG9 play an antiviral role to suppress SRBSDV propagation and transmission.