Abstract
BackgroundThe establishment of the nuclear membrane resulted in the physical separation of transcription and translation, and presented early eukaryotes with a formidable challenge: how to shuttle RNA from the nucleus to the locus of protein synthesis. In prokaryotes, mRNA is translated as it is being synthesized, whereas in eukaryotes mRNA is synthesized and processed in the nucleus, and it is then exported to the cytoplasm. In metazoa and fungi, the different RNA species are exported from the nucleus by specialized pathways. For example, tRNA is exported by exportin-t in a RanGTP-dependent fashion. By contrast, mRNAs are associated to ribonucleoproteins (RNPs) and exported by an essential shuttling complex (TAP-p15 in human, Mex67-mtr2 in yeast) that transports them through the nuclear pore. The different RNA export pathways appear to be well conserved among members of Opisthokonta, the eukaryotic supergroup that includes Fungi and Metazoa. However, it is not known whether RNA export in the other eukaryotic supergroups follows the same export routes as in opisthokonts.MethodsOur objective was to reconstruct the evolutionary history of the different RNA export pathways across eukaryotes. To do so, we screened an array of eukaryotic genomes for the presence of homologs of the proteins involved in RNA export in Metazoa and Fungi, using human and yeast proteins as queries.ResultsOur genomic comparisons indicate that the basic components of the RanGTP-dependent RNA pathways are conserved across eukaryotes, and thus we infer that these are traceable to the last eukaryotic common ancestor (LECA). On the other hand, several of the proteins involved in RanGTP-independent mRNA export pathways are less conserved, which would suggest that they represent innovations that appeared later in the evolution of eukaryotes.ConclusionsOur analyses suggest that the LECA possessed the basic components of the different RNA export mechanisms found today in opisthokonts, and that these mechanisms became more specialized throughout eukaryotic evolution.
Highlights
The establishment of the nuclear membrane resulted in the physical separation of transcription and translation, and presented early eukaryotes with a formidable challenge: how to shuttle RNA from the nucleus to the locus of protein synthesis
We examined conservation of the proteins involved in the different RNA export pathways across eukaryotes, with special focus on distinguishing components that are traceable to the last eukaryotic common ancestor (LECA) from those that derive from lineage-specific innovations
Results from our genomic comparisons indicate that several of the key proteins involved in the different RanGTPdependent RNA export pathways are conserved across most eukaryotic lineages, and we infer that orthologs of them were highly likely to have been already present in the LECA
Summary
The establishment of the nuclear membrane resulted in the physical separation of transcription and translation, and presented early eukaryotes with a formidable challenge: how to shuttle RNA from the nucleus to the locus of protein synthesis. The mRNA export machinery is highly integrated with mRNA processing, and it includes a different set of nuclear transport adaptors plus other mRNA binding proteins, RNA helicases, and NPC associated proteins [4,5,6]. It is not known whether the proteins involved in the different RNA export pathways are conserved among the different eukaryotic supergroups, and which components of the nucleocytoplasmic export of RNA are traceable to the last eukaryotic common ancestor (LECA). Results from our bioinformatic comparisons suggest that the basic components of the RanGTP-dependent RNA pathways are conserved across eukaryotes, whereas proteins involved in RanGTP-independent mRNA export are less conserved
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