Cellular COPI components promote geminivirus infections by facilitating the chloroplast localization of viral C4/AC4 proteins

Abstract

Geminiviruses are a family of viruses that infect numerous crops and cause extensive agricultural losses worldwide. During viral infection, geminiviral C4/AC4 proteins relocate from the plasma membrane (PM) to chloroplasts, where they inhibit chloroplast-mediated host defense, including the biosynthesis of salicylic acid (SA). However, how are C4/AC4 proteins transported to chloroplasts is unknown. We report here that the Coat Protein I (COPI) components play a critical role in redistributing Tomato yellow leaf curl virus (TYLCV) C4 protein to chloroplasts. TYLCV C4 interacts with the β subunit of COPI, and the coexpression of both inNicotiana benthamianacells promotes the enrichment of C4 in chloroplasts, which also occurs during TYLCV infection and is blocked by an inhibitor of the COPI pathway. Overexpression of COPI components promotes but knockdown of gene expression inhibits TYLCV infection. The COPI pathway plays similar roles in C4/AC4 transport and infections of other geminiviruses, including Beet curly top virus and East African cassava mosaic virus. Our results identify an unconventional role of the COPI pathway in protein trafficking to chloroplasts during geminiviruses infections in plants, and suggest a broad-spectrum antiviral strategy in controlling geminiviruses by manipulating COPI components.