Evolution and Natural History of Membrane Trafficking in Eukaryotes

Abstract

The membrane-trafficking system is a defining facet of eukaryotic cells. The best-known organelles and major protein families of this system are largely conserved across the vast diversity of eukaryotes, implying both ancient organization and functional unity. Nonetheless, intriguing variation exists that speaks to the evolutionary forces that have shaped the endomembrane system in eukaryotes and highlights ways in which membrane trafficking in protists differs from that in our well-understood models of mammalian and yeast cells. Both parasites and free-living protists possess specialized trafficking organelles, some lineage specific, others more widely distributed -the evolution and function of these organelles begs exploration. Novel members of protein families are present across eukaryotes but have been lost in humans. These proteins may well hold clues to understanding differences in cellular function in organisms that are of pressing importance for planetary health.

The liverwort oil body is formed by redirection of the secretory pathway

“…Thus, the redirection of the secretory pathway is a common strategy for plants to acquire novel organelles/cellular structures that have resulted in maximizing fitness for land plants during evolution. A lineage-specific acquisition of secretion-related organelles associated with duplication and neofunctionalization of trafficking machineries, such as RAB GTPase, was also reported in protozoa 6,44 . Thus, acquisition of new organelles by redirection of the secretory pathway through the paralogous expansion of trafficking machinery components followed by their neofunctionalization would be a commonly adopted evolutionary path, concordant with the organelle paralogy hypothesis.…”

“…Comparative genomics has proposed that the emergence of a novel membranebounded organelle was accompanied by the development of a novel membrane trafficking pathway, which was accomplished by expansion and functional differentiation of machinery components through gene duplication followed by neo-and/or subfunctionalization of those machineries by accumulated mutations 5 . For example, coat-protein complexes, RAB GTPases, and SNARE proteins, which act in transport vesicle formation, tethering of the vesicles to target membranes, and membrane fusion between the two membranes, respectively, were shown to expand and functionally differentiate during evolution to develop the specialized membrane trafficking system in each organism 6,7 . However, empirical support for this hypothesis, i.e.…”

A eukaryote-wide perspective on the diversity and evolution of the ARF GTPase protein family

“…Only a single study addressing the function of Arl16 has been published, reporting that the mammalian Arl16 inhibits the function of the RIG-I protein, involved in the defence against RNA viruses (Yang et al, 2011), but more specific functional insights are lacking. Functions for of the newly discovered paralogs Sar1L, Arl17, and Arl18 are completely unknown, as these paralogs are missing from all common model eukaryotes and thus represent examples of “jotnarlogs”, proteins that are present across eukaryotes, but missing in well-studied cell biological models (More et al, 2020). This adds further credence to the proposal that this is a substantial evolutionary cell biological phenomenon and highlights the gap in our understanding of the cell biology of the ARF family in eukaryotes.…”

Evolution and diversification of the nuclear envelope

“…Several distinct modes underpinning the evolution of compartments and organellar diversity have been proposed. These are based largely on analysis of the membrane trafficking system, which features large paralogous protein families with organelle-specific members such as GTPase and SNARE families, kinesins and others [8][9][10]. Some of these modes can be considered to be 'expansive', in the sense that they lead to an increase in the number of compartments.…”