Eukaryotic nuclear structure explains the evolutionary rate difference of ribosome export factors

Abstract

Because the nucleus is the cellular structure essentially differentiating eukaryotes from prokaryotes, the formation of the nuclear membrane should have been a key event in eukaryotic evolution. Although an evolutionary cause of formation of the nucleus such as symbiosis has been speculated but still not clarified, evolutionary establishment of the transport system across the nuclear membrane must have been prerequisite for survival of the then-emerging eukaryotes. In particular, export of ribosomes, one of the largest complexes in a eukaryotic cell, from the nucleus to the cytoplasm must have been crucial for retaining the translation system of proteins. As discovered in recent years, kinetic steps in this nucleocytoplasmic transport pathway are stimulated by proteins called ribosome export factors (REFs). Hence, evolution of REFs is of particular interest, and description of the evolutionary features of REFs is of immediate value. However, even the evolutionary rates of REFs are still poorly understood compared with those of ribosomal components. With the aim of understanding the evolutionary features of REFs, we estimated the rates of amino acid substitutions of REFs for two related species of yeast, Saccharomyces cerevisiae and Saccharomyces paradoxus, and compared them with those of ribosomal components. We found that the average rate of amino acid substitutions for REFs was somewhat higher than that of ribosomal components, although the former was much lower than the grand average of other 5527 proteins. Moreover, we also found that the REFs were clearly classified into two classes; the slowly evolving REFs and the rapidly evolving REFs. Interestingly, we found that the slowly and rapidly evolving REFs correspond to the membranous REFs (mREFs) and the non-membranous REFs (non-mREFs), respectively. Further analyses with 112 REFs from 16 eukaryotic species also showed clear differences in the evolutionary rates between these two classes. Because the non-mREFs are involved in non-membranous transport from the nucleolus to nucleoplasm and the mREFs are committed to membranous transport from the nucleoplasm to the cytoplasm, the mREFs appear to have much stronger functional constraints than the non-mREFs. Thus, we conclude that the evolutionary appearance of mREFs may be one of the crucial factors for ensuring the transport from the nucleus to the cytoplasm when the nucleus was formed in the process of eukaryotic evolution.