The evolution of the nuclear envelope

Abstract: The nucleus is one of the defining features of eukaryotes and the question of its origin is intimately linked to the evolution of the eukaryotic cell. It is delimited by a double lipid bilayer called the nuclear envelope, which separates the nuclear interior from the cytoplasm. The inner and outer membranes of the nucleus are continuous with one another creating a single folded envelope, interrupted by nuclear pore complexes (NPCs), which enable transport of proteins and RNA between nucleoplasm and cytoplasm.A combination of proteomic and bioinformatic analyses has shown that numerous Nups are conserved between yeast and vertebrates. As this only describes a subset of eukaryotic diversity, comparative genomic analyses were used to establish the extent to which the NPC is conserved across the eukaryotic tree. NPCs have been suggested to share a common origin with vesicle coat proteins of the endomembrane system. An additional goal of this work was therefore to establish the distribution of three complexes involved in vesicle transport between organelles of the secretory pathway, called COPI, COPII and Clathrin.Using profile hidden Markov models in combination with BLAST resulted in identification of nucleoporins and coat protein homologs across all five eukaryotic supergroups for which sequence data is available, indicating both were already present in the Last Eukaryotic Common Ancestor (LECA).Nup homologs were shown to be definitively absent from vestigial nucleomorph nuclei, resultant from secondary endosymbioses, suggesting that Nup genes have either been relocated to the host nuclear genome or that the same set of Nups are used for constructing both the NPC of the main nucleus and nucleomorph.´We also tested the proposal that transmembrane Nups in vertebrates and yeasts may account for their variant forms of mitosis (‘open’ in vertebrates, ‘closed’ among yeasts). Consistent with this suggestion, the distribution of fungal Pom34 fits a scenario wherein it was integral to the evolution of 'closed’ mitosis in ascomycetes.A unique arrangement for the chromosomes occurs during early meiosis, where the telomeres cluster at the nuclear envelope, forming a distinct ‘bouquet’ arrangement. This forms prior to homolog pairing and recombination in meiosis I. Hypotheses concerning the antiquity of the bouquet were tested by examining the extent of conservation of proteins involved in this stage of meiosis. Distribution appeared patchy, so its presence in LECA could not be unequivocally established and is discussed together with a model aimed at explaining the functional role of the bouquet.