Nucleolar fibrillarin methyltransferase regulates systemic trafficking of a plant virus satellite RNA

RNA trafficking is crucial in almost every phase of plant development. Fibrillarin (FIB), a highly conserved nucleolar protein with methyltransferase (MTase) activity, functions in methylation and rRNA processing and facilitates the transport of several RNA viruses in plants. Previously, we demonstrated that bamboo mosaic virus satellite RNA (satBaMV) traffics autonomously and systemically in a helper virus-independent but FIB-dependent manner by forming a mobile ribonucleoprotein (RNP) complex comprising satBaMV, FIB, and satBaMV-encoded P20 movement protein. Here, we show that FIB methylates the arginine-rich motif (ARM) of P20 and relies on its MTase activity for the systemic movement of satBaMV. FIB MTase-defective mutants failed to complement long-distance satBaMV transport in FIBi plants, despite still binding to satBaMV in vivo. We also demonstrate that the ARM of P20 guides its nucleolar localization for FIB-mediated methylation. P20 methylation not only contributes to its plasmodesmata (PD) targeting but also triggers nucleocytoplasmic shuttling of FIB with P20 as the RNP complex to PD. A satBaMV mutant harboring a non-methylated P20, but not a methylation-mimic P20, exhibited disrupted PD targeting and impaired P20-assisted satBaMV trafficking. Our findings provide mechanistic insights into how FIB-mediated P20 methylation positively regulates systemic trafficking of a subviral agent in plants.