Pepino mosaic virus antagonizes plant m(6)A modification by promoting the autophagic degradation of the m(6)A writer HAKAI

Autophagy plays an active anti-viral role in plants. Increasing evidence suggests that viruses can inhibit or manipulate autophagy, thereby winning the arms race between plants and viruses. Here, we demonstrate that overexpression of an m(6)A writer from Solanum lycopersicum, SlHAKAI, could negatively regulate pepino mosaic virus (PepMV) infection, inhibit viral RNA and protein accumulations by affecting viral m(6)A levels in tomato plants and vice versa. The PepMV-encoded RNA-dependent RNA polymerase (RdRP) directly interacts with SlHAKAI and reduces its protein accumulation. The RdRP-mediated decreased protein accumulation of SlHAKAI is sensitive to the autophagy inhibitor 3-methyladenine and is compromised by knocking down a core autophagy gene. Furthermore, PepMV RdRP could interact with an essential autophagy-related protein, SlBeclin1. RdRP, SlHAKAI, and SlBeclin1 interaction complexes form bright granules in the cytoplasm. Silencing of Beclin1 in Nicotiana benthamiana plants abolishes the RdRP-mediated degradation of SlHAKAI, indicating the requirement of Beclin1 in this process. This study uncovers that the PepMV RdRP exploits the autophagy pathway by interacting with SlBeclin1 to promote the autophagic degradation of the SlHAKAI protein, thereby inhibiting the m(6)A modification-mediated plant defense responses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s42994-023-00097-6.