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Evolution of the eukaryotic membrane trafficking system as revealed by comparative genomic and phylogenetic analysis of adaptin, golgin, and SNARE proteins
- Author / Creator
- Barlow, Lael D.
All eukaryotic cells possess a complex system of endomembranes that functions in trafficking molecular cargo within the cell, which is not observed in prokaryotic cells. This membrane trafficking system is fundamental to the cellular physiology of extant eukaryotes, and includes organelles such as the endoplasmic reticulum, Golgi apparatus, and endosomes as well as the plasma membrane. The evolutionary history of this system offers an over-arching framework for research on membrane trafficking in the field of cell biology. However, the evolutionary origins of this system in the evolution from a prokaryotic ancestor to the most recent common ancestor of extant eukaryotes is a major evolutionary transition that remains poorly understood. A leading paradigm is described by the previously proposed Organelle Paralogy Hypothesis, which posits that coordinated duplication and divergence of genes encoding organelle-specific membrane trafficking proteins underlies a corresponding evolutionary history of organelle differentiation that produced the complex sets of membrane trafficking organelles found in extant eukaryotes. This thesis focuses on investigating the evolution of families of proteins that sustain membrane traffic by organizing vesicle transport between specific compartments.
Comparative genomics and phylogenetic analysis methods were applied to trace the evolution of subunits of the Adaptor Protein complexes, which function in vesicle formation, revealing that losses of genes encoding these subunits in Fungi and duplications in plants are relatively recent events, consistent with a highly conserved role of members of this protein family in organizing the membrane trafficking system. Similar methods were applied to the golgin proteins, which extend from membranes of the Golgi apparatus to recognize and tether specific vesicles. This revealed considerable conservation of golgins specific to different regions of the Golgi, consistent with ancestral complexity of the Golgi inferred from conservation of morphological complexity
among eukaryotes. The Soluble N-ethylmaleimide sensitive factor Attachment protein REceptor (SNARE) protein superfamily comprises numerous proteins forming complexes that mediate vesicle fusion at specific locations in the cell. An extensive analysis of the SNAREs revealed evidence for additional SNARE proteins present in the last common ancestor of eukaryotes. Finally, the evolution of the four constituent families within the SNARE superfamily was explored and relevance to various potential scenarios of early evolution of the membrane trafficking system are discussed.
Taken together, the results of this work shed light on the connections between protein evolution and organelle evolution, and provide novel evidence for distinguishing between alternative scenarios for the evolution of the membrane trafficking system.
- Graduation date
- Spring 2020
- Type of Item
- Doctor of Philosophy
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