A Novel Role for a Karyopherin-β Protein in Plant pre-60S Ribosome Biogenesis

Universally across cellular life, protein synthesis depends on proper ribosome biogenesis and assembly. Newly produced, individual ribosomal proteins are trafficked into the nucleus to associate into quaternary structures with ribosomal RNA. The formation of such premature ribosomal subunits is an extensive and complex process that starts in the nucleolus and concludes in the cytoplasm. Unlike in animals and yeast, the majority of ribosome biogenesis factors that determine the transition of subunits across subcellular spaces on their way towards maturation remain uncharacterized. Here, we show that the karyopherin-β protein IMPORTIN β-2 (IMB2) has a critical role in promoting the transition of pre-60S particles out of the nucleolus and into the nucleoplasm. Through proximity labeling proteomics, we report that IMB2 probes a plurality of ribosomal proteins from 40S and 60S subunits. We show that IMB2 associates with ribosomal subunits and that imb2/- mutants have pronounced defects in ribosome biogenesis and translation, along with severe developmental and reproductive defects. Mutants of IMB2 have stalled pre-60S particles at the nucleolus and IMB2 is required for the maturation and incorporation of 60S subunits into polysomes. Through ribosome profiling, we show that immature pre-60S particles lead to a severe alteration in translational efficiency in imb2/- mutants, and link this to specific disfunctions in ribosome-mRNA interactions. Our results suggest that IMB2 is a novel and fundamental factor in pre-60S ribosome biogenesis.