The evolution of the ribosome biogenesis pathway from a yeast perspective

Ingo Ebersberger,Markus T Bohnsack,Matthias S Leisegang,Oliver Mirus,Arndt Von Haeseler,Enrico Schleiff,Stefan Simm,Peter Schmitzberger

doi:10.1093/nar/gkt1137

Ingo Ebersberger, Markus T Bohnsack + Show 6 more

Open Access

https://doi.org/10.1093/nar/gkt1137

Copy DOI

Abstract

Ribosome biogenesis is fundamental for cellular life, but surprisingly little is known about the underlying pathway. In eukaryotes a comprehensive collection of experimentally verified ribosome biogenesis factors (RBFs) exists only for Saccharomyces cerevisiae. Far less is known for other fungi, animals or plants, and insights are even more limited for archaea. Starting from 255 yeast RBFs, we integrated ortholog searches, domain architecture comparisons and, in part, manual curation to investigate the inventories of RBF candidates in 261 eukaryotes, 26 archaea and 57 bacteria. The resulting phylogenetic profiles reveal the evolutionary ancestry of the yeast pathway. The oldest core comprising 20 RBF lineages dates back to the last universal common ancestor, while the youngest 20 factors are confined to the Saccharomycotina. On this basis, we outline similarities and differences of ribosome biogenesis across contemporary species. Archaea, so far a rather uncharted domain, possess 38 well-supported RBF candidates of which some are known to form functional sub-complexes in yeast. This provides initial evidence that ribosome biogenesis in eukaryotes and archaea follows similar principles. Within eukaryotes, RBF repertoires vary considerably. A comparison of yeast and human reveals that lineage-specific adaptation via RBF exclusion and addition characterizes the evolution of this ancient pathway.

Highlights

Ribosomes mediate the translation of messenger RNAs into the corresponding amino acid sequences
A literature screen identified 255 accessory proteins confirmed or proposed to play a role in this pathway (Figure 1A; Supplementary Table S1). Starting from this set we investigated the evolutionary ancestry of ribosome biogenesis in yeast
Saccharomyces paradoxus exhibits almost the full inventory of 254 ribosome biogenesis factors (RBFs), in the microsporidium Antonospora locustae, which is still considerably closely related to the fungi we detected orthologs to only 65 RBFs, and in humans we found again counterparts to 200 yeast RBFs

Summary

Introduction

Ribosomes mediate the translation of messenger RNAs into the corresponding amino acid sequences. Ribosome synthesis is initiated by the transcription of a ribosomal RNA precursor (pre-rRNA; 35S pre-rRNA in yeast) in the nucleolus followed by the assembly of the 90S pre-ribosome (Figure 1A). The biogenesis pathways of the small and the large ribosomal subunits are separated upon cleavage of the pre-rRNA transcript (at the site A2 in yeast). The resulting pre-40S and pre-60S ribosome subunits are exported into the cytoplasm where the final rRNA processing takes place [for yeast, see [5,6]]. Both ribosomal subunits undergo final maturation to become functional for translation [1,6]

Methods

Results

Conclusion