Pore timing: the evolutionary origins of the nucleus and nuclear pore complex

Abstract

The name "eukaryote" is derived from Greek, meaning "true kernel", and describes the domain of organisms whose cells have a nucleus. The nucleus is thus the defining feature of eukaryotes and distinguishes them from prokaryotes (Archaea and Bacteria), whose cells lack nuclei. Despite this, we discuss the intriguing possibility that organisms on the path from the first eukaryotic common ancestor to the last common ancestor of all eukaryotes did not possess a nucleus at all-at least not in a form we would recognize today-and that the nucleus in fact arrived relatively late in the evolution of eukaryotes. The clues to this alternative evolutionary path lie, most of all, in recent discoveries concerning the structure of the nuclear pore complex. We discuss the evidence for such a possibility and how this impacts our views of eukaryote origins and how eukaryotes have diversified subsequent to their last common ancestor.

Keywords: eukaryogenesis; molecular evolution; nuclear pore complex; vesicle coats.

Figure 1.. Diversity within modern nuclear pore complex (NPC) structures.

( A) Four NPC examples are shown from different taxa, metazoa, fungi, green alga, and kinetoplastids (some elements speculative in the latter), and approximate evolutionary relationships are shown at the far left. ( B) A schematic of a generic NPC, based on the Saccharomyces cerevisiae structure, is shown at the top right. ( C) Variations in the scaffold structure, export platform, cytoplasmic face remodeling complex, and the nuclear basket structures are indicated. The outer and inner ring nucleoporin (Nup) complex subunit arrangements are shown at the bottom right, emphasizing the distinct coat architectures present. Type I coats are red and type II are blue. FG, phenylalanine-glycine.

Figure 2.. Type I and type II coat protein architectures and locations within the nuclear pore complex.

( A) Examples of type I and type II architectures are shown. Type I coats are red and type II are blue. Idealized structures appear above, and examples of structures determined by x-ray (COPI subunits pdf:5A1U and COPII subunits pdf:4BZJ as representatives of type I and type II, respectively) appear below. Note the characteristic β-propeller head and α-solenoid tail in both type I subunits, the α-solenoid adaptin-like subunit in type I, and the clear presence of a discontinuity and loop in the α-solenoid following the β-propellers in type II. ( B) A section of the Saccharomyces cerevisiae nuclear pore complex structure is shown at the bottom, illustrating only the type I– and type II–related subunits. Note the intermixing of types within the overall structure.

Figure 3.. Timeline for evolution of coat complexes, mitochondrial enslavement, and nuclear pore complex (NPC) elaboration.

( A) The top system illustrates acquisition and gradual enslavement of the mitochondrion by transfer of genes from the original bacterial genome to the genome of the host cell. Dotted lines indicate uncertainty concerning both the point of endosymbiont acquisition and duration of the overall process. ( B) The top middle system depicts hypothetical general structures of transitional eukaryotic cellular forms at various stages during the process of eukaryogenesis. The location and type of protocoatomer are indicated by colored crescents. Note the amalgam coat of the NPC. ( C) The lower middle system is a proposed timeline for the evolution of vesicular coat complexes, colored to correspond with the cellular diagrams. The earliest proto-eukaryote is suggested to have a single ancestral coat (protocoatomer), which is derived from Archaeal genes. In many prokaryotes, such genes are present, but the β-propellers and α-solenoids are not fused to encode a single protein. Examples of type I and type II architectures are shown at the right, together with examples of specific complexes present in modern eukaryotes. ( D) The lower system illustrates a possible route for the evolution of the NPC, placing emphasis on the duplication of subunits and merging of protocoatomer type I and type II to create the modern NPC structure. Ovals represent subunits in the evolving NPC and are differently shaded to indicate duplications. Type I coats are red, type II are blue, and protocoatomer is purple. Putative archaeal lineages and proteins are shown in gray. FECA, first eukaryotic common ancestor; LECA, last eukaryotic common ancestor.