Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol Biol 7: 29

Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, UK. <>
BMC Evolutionary Biology (Impact Factor: 3.41). 02/2007; 7:29. DOI: 10.1186/1471-2148-7-29
Source: PubMed

ABSTRACT In membrane trafficking, the mechanisms ensuring vesicle fusion specificity remain to be fully elucidated. Early models proposed that specificity was encoded entirely by SNARE proteins; more recent models include contributions from Rab proteins, Syntaxin-binding (SM) proteins and tethering factors. Most information on membrane trafficking derives from an evolutionarily narrow sampling of model organisms. However, considering factors from a wider diversity of eukaryotes can provide both functional information on core systems and insight into the evolutionary history of the trafficking machinery. For example, the major Qa/syntaxin SNARE families are present in most eukaryotic genomes and likely each evolved via gene duplication from a single ancestral syntaxin before the existing eukaryotic groups diversified. This pattern is also likely for Rabs and various other components of the membrane trafficking machinery.
We performed comparative genomic and phylogenetic analyses, when relevant, on the SM proteins and components of the tethering complexes, both thought to contribute to vesicle fusion specificity. Despite evidence suggestive of secondary losses amongst many lineages, the tethering complexes are well represented across the eukaryotes, suggesting an origin predating the radiation of eukaryotic lineages. Further, whilst we detect distant sequence relations between GARP, COG, exocyst and DSL1 components, these similarities most likely reflect convergent evolution of similar secondary structural elements. No similarity is found between the TRAPP and HOPS complexes and the other tethering factors. Overall, our data favour independent origins for the various tethering complexes. The taxa examined possess at least one homologue of each of the four SM protein families; since the four monophyletic families each encompass a wide diversity of eukaryotes, the SM protein families very likely evolved before the last common eukaryotic ancestor (LCEA).
These data further support a highly complex LCEA and indicate that the basic architecture of the trafficking system is remarkably conserved and ancient, with the SM proteins and tethering factors having originated very early in eukaryotic evolution. However, the independent origin of the tethering complexes suggests a novel pattern for increasing complexity in the membrane trafficking system, in addition to the pattern of paralogous machinery elaboration seen thus far.

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Available from: Mark Field, Jul 17, 2015
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    • "As far as we are aware, there are four broadly distributed SM proteins, likely present in the LECA. The tether system is more complex, as these factors comprise several complexes of varying size, and in many taxa several subunits are lost, but most lineages have at least a representative of all examined tethering complexes, consistent with a complement of at least seven complexes in the LECA (Koumandou et al., 2007). Limited sequence similarity is apparent between the tether complex subunits, but structural biology has identified a similar ''CATCHR'' fold in subunits from multiple tether complexes, suggesting the presence of paralogous subunits (Bröcker et al., 2010; Spang, 2012). "
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    ABSTRACT: Abstract Eukaryogenesis, the origin of the eukaryotic cell, represents one of the fundamental evolutionary transitions in the history of life on earth. This event, which is estimated to have occurred over one billion years ago, remains rather poorly understood. While some well-validated examples of fossil microbial eukaryotes for this time frame have been described, these can provide only basic morphology and the molecular machinery present in these organisms has remained unknown. Complete and partial genomic information has begun to fill this gap, and is being used to trace proteins and cellular traits to their roots and to provide unprecedented levels of resolution of structures, metabolic pathways and capabilities of organisms at these earliest points within the eukaryotic lineage. This is essentially allowing a molecular paleontology. What has emerged from these studies is spectacular cellular complexity prior to expansion of the eukaryotic lineages. Multiple reconstructed cellular systems indicate a very sophisticated biology, which by implication arose following the initial eukaryogenesis event but prior to eukaryotic radiation and provides a challenge in terms of explaining how these early eukaryotes arose and in understanding how they lived. Here, we provide brief overviews of several cellular systems and the major emerging conclusions, together with predictions for subsequent directions in evolution leading to extant taxa. We also consider what these reconstructions suggest about the life styles and capabilities of these earliest eukaryotes and the period of evolution between the radiation of eukaryotes and the eukaryogenesis event itself.
    Critical Reviews in Biochemistry and Molecular Biology 07/2013; 48(4):373-396. DOI:10.3109/10409238.2013.821444 · 5.81 Impact Factor
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    • "Tethering factors have been divided into three functional classes: 1) oligomeric complexes that bind to SNAREs and typically act as Rab effectors, i.e., the DCGE group that includes Dsl1 complex, Conserved Oligomeric Golgi (COG) complex, Golgi-associated retrograde protein (GARP) complex, and Exocyst; 2) oligomeric complexes that function as GEFs for Rab proteins, i.e., Transport Protein Particle (TRAPP I and TRAPP II) and Heterohexameric homotypic fusion and vacuole protein sorting complex (HOPS), which works as a GEF and an effector; and 3) coiled-coil tethers (Sztul and Lupashin 2009). In Arabidopsis most of the tethering factor homologues have been identified (Table 4) (Koumandou et al. 2007; Latijnhouwers et al. 2005). "
    03/2013, Degree: PhD, Supervisor: Henrik Aronsson
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    • "Research in yeast suggests that Exo70 and Sec3 subunits serve as spatial PM landmarks for the assembly of the exocyst complex that interacts with, and might also be activated by, Rho GTPases to coordinate the tethering of incoming secretory vesicles before SNARE complex formation (Boyd et al., 2004; He et al., 2007; Zhang et al., 2008; Wu et al., 2010). Phylogenetic analyses indicate that all exocyst subunits are present in land plants (Cvr ckov a et al., 2001; Eli a s et al., 2003; Koumandou et al., 2007), and that the EXO70 gene has undergone a dramatic evolutionary expansion: e.g. in Angiosperms, with 22 presumably functional genes present in Arabidopsis thaliana (Eli a s et al., 2003; Synek et al., 2006). By contrast, only a single copy of EXO70 is present in yeast and animals, suggesting an elaboration of functional or tissue-specific specialization in plants ( Z arsk y et al., 2009). "
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    The Plant Journal 11/2012; 73(5). DOI:10.1111/tpj.12074 · 6.82 Impact Factor
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