Origin of Eukaryotic Endomembranes: A Critical Evaluation of Different Model Scenarios

Abstract

All cells can be assigned to one of two categories based on the complexity of cellular organization, eukaryotes and prokaryotes. Eukaryotes possess, among other distinguishing features, an intracellular dynamic membrane system through which there is a constant flow of membranes scaffolded by an internal cytoskeleton. Prokaryotes, however, can have internal membranes, entirely lack a system that resembles eukaryotic endomembranes in terms of dynamics, complexity and the multitude of functions. How and why did the complex endomembrane system of eukaryotes arise? Here I give a critical overview of the different cell biological model scenarios that have been proposed to explain endomembrane origins. I argue that the widely held symbiotic models for the origin of the nuclear envelope and other endomembranes are cell biologically and evolutionarily highly implausible. Recent findings about the origin of nuclear pore complexes also severely challenge such models. I also criticize a scenario of de novo vesicle formation at the origin of the endomembrane system. I contrast these scenarios to traditional and revised autogenous models according to which eukaryotic endomembranes evolved by the inward budding of a prokaryotic cell’s plasma membrane. I argue that such models can best satisfy the major constraints of membrane topology, membrane heredity and straightforwardly account for selection pressures while being consistent with genomic findings.