Areca palm velarivirus 1 encoded P25 hijacks host eIF4E and enhances viral translation through strengthening the interaction of eIF4E with 3′ cap-independent translation enhancer

Abstract Plant viruses employ diverse strategies to hijack host machinery for viral translation initiation. Cap-independent translation enhancers located in the 3′ untranslated region (3′-CITEs) have been identified in many members of the families Tombusviridae and Luteoviridae . However, viral proteins that regulate 3′-CITE-mediated translation remain unreported, and the underlying mechanisms are still poorly understood. Closteroviruses are important pathogens that infect many economically significant crops, yet their translation initiation mechanisms remain largely unexplored. Areca palm velarivirus 1 (APV1), a member of the family Closteroviridae , is the causative agent of yellow leaf disease (YLD) in areca palms. Here, we demonstrate that eukaryotic initiation factor 4E (eIF4E) specifically binds to the 3′-UTR of APV1. The APV1-encoded protein P25 interacts with eIF4E, enhances its stability, alters its subcellular localization, and promotes its recruitment to APV1 virions. Notably, P25 significantly enhances cap-independent viral translation. Knockout of eIF4E in Nicotiana benthamiana or mutation of key residues in APV1-P25 required for eIF4E interaction impairs APV1 infection. We identify the 3′-UTR of APV1 as the first reported 3′-CITE in the family Closteroviridae . Our study reveals P25 as the first viral regulator of 3′-CITE-mediated translation initiation, providing new insights into the molecular mechanisms underlying viral infection.