The nuclear pore complex (NPC), a vital structure in eukaryotic cells, facilitates molecular transport between the nucleus and cytoplasm. It exhibits remarkable structural complexity, comprised of approximately 30 different proteins known as nucleoporins (Nups) arranged in multiple copies with eight-fold rotational symmetry. While Nup conservation is well-established between yeast, vertebrates, and plants, their presence and composition in other eukaryotic groups remained less clear. A comparative genomic analysis across 60 eukaryotic genomes, spanning all major supergroups, reveals striking evidence for a common ancestor when comparing the composition of the NPC.
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Universal Presence of Core NPC Subcomplexes Points to a Common Ancestor
This comprehensive analysis identified homologs for 19 of 31 known Nups in all five eukaryotic supergroups: Opisthokonts, Amoebozoa, Viridiplantae, Chromalveolates, and Excavates. These universally present Nups represent all major NPC subcomplexes, including the cytoplasmic fibrils, central core scaffold, anchoring system, nuclear ring, central channel, and nuclear basket. This widespread conservation strongly supports the presence of a fully functional and complex NPC in the Last Eukaryotic Common Ancestor (LECA). A Common Ancestor Is Evident When Comparing the remarkable similarity in the core NPC structure across such diverse eukaryotic lineages.
Anchoring System Conservation Challenges Previous Hypotheses
Previous studies suggested that the NPC anchoring system, responsible for securing the NPC to the nuclear envelope, might have evolved independently multiple times due to the seemingly limited distribution of anchoring Nups. However, this study identified Gp210, a key anchoring Nup, across all five supergroups, suggesting its presence in LECA. While Ndc1, another anchoring Nup, showed a more restricted distribution, its presence in key lineages still points to its likely presence in LECA. A common ancestor is evident when comparing the anchoring mechanisms, further reinforcing the concept of a complex NPC in LECA. This challenges previous hypotheses of convergent evolution for the anchoring system.
Implications for the Evolution of Mitosis
The distribution of integral membrane Nups, particularly Pom34, Pom121, and Pom152, provides intriguing insights into the evolution of open and closed mitosis. Pom121 appears restricted to vertebrates, while Pom34 is specific to Ascomycetes, a group of fungi characterized by closed mitosis. This correlation suggests that Pom34 may play a role in the evolution of closed mitosis in this fungal lineage. A common ancestor is evident when comparing the distribution of these Nups with the type of mitosis observed in different lineages, highlighting the potential link between NPC components and the evolution of cell division mechanisms. The absence of Pom34 in Basidiomycetes, which undergo open mitosis, strengthens this association.
Coatomer Complex Conservation Reinforces Ancient Origins
The protocoatomer hypothesis proposes a shared evolutionary origin between the NPC and vesicle-coating complexes based on shared protein architecture. This study examined the conservation of COPI, COPII, and clathrin complex components and found them to be remarkably conserved across eukaryotes. This high degree of conservation across all major eukaryotic supergroups further supports the ancient origin of these complexes and their likely presence in LECA. A common ancestor is evident when comparing the components of vesicle-coating complexes, lending further credence to the protocoatomer hypothesis and the interconnected evolution of intracellular trafficking machinery.
Conclusion: A Complex LECA Revealed Through Comparative Genomics
The extensive conservation of both NPC and vesicle-coating complex components across diverse eukaryotic lineages provides compelling evidence for a complex LECA. A common ancestor is evident when comparing the intricate machinery responsible for nucleocytoplasmic transport and vesicle trafficking, revealing a sophisticated level of cellular organization already present in the early stages of eukaryotic evolution. This study underscores the power of comparative genomics in reconstructing ancestral states and illuminating the evolutionary history of complex cellular structures. The findings solidify the concept of a complex LECA equipped with sophisticated mechanisms for intracellular transport and compartmentalization. Further research into the structural and functional details of these complexes across diverse eukaryotic lineages promises to further refine our understanding of LECA and the early evolution of eukaryotes.
