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First published online August 22, 2007
doi: 10.1242/10.1242/jcs.013250

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Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode

Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, UK

View larger version (33K): [in this window] [in a new window]   Fig. 1. Evolutionary origin and loss of endomembrane components across the major eukaryotic lineages. Current understanding of the relationships between major eukaryotic lineages suggests a rapid radiation early in evolution that gave rise to the six major groups. The stem of the tree represents the transition between prokaryotes and eukaryotes, and is a period of radical innovation. Red dots indicate presumed secondary loss of factors, because multiple sampled lineages above the internode lack the relevant gene. Blue dots indicate that most taxa above the symbol possess a given gene or gene complement, suggesting that the system/complex/factor arose at this point. The split dot represents the apparent secondary reduction of multiple trafficking components in the metamonad Giardia contrasted with the expansion of trafficking machinery in its sister lineage Trichomonas. Significantly, many of the major components are universal, indicating that the basic mechanisms for vesicle specificity and fusion arose very early, together with establishment of major landmarks of the endomembrane system (i.e. clathrin-dependent endocytosis, exocytosis and recycling pathways). In addition, there is evidence for the acquisition of lineage-specific components (e.g. caveolin by metazoa) and multiple secondary losses (e.g. the Rab4 recycling pathway). Sampling bias in choice of experimental taxa means that novel factors in most lineages have not been identified. Rhizaria are shown as a dotted line because, at present, there are no genome sequences for this group. Figure redrawn and modified from Field et al. (Field et al., 2006), with permission from Landes Bioscience and Springer Science + Business Media.

View larger version (23K): [in this window] [in a new window]   Fig. 2. Acquisition of organelle complexity and function by paralogous gene family expansion. (A) Gene duplication events lead to more than one copy of an open reading frame A (ORF A). This gene redundancy allows each member of the new family to accumulate sequence variation and, hence, potentially new functions. A clear example of this type of event would be the ancestor of the coatomer and adaptin complex subunits. (B) Model for compartment number expansion by gene duplication of protein factors implicated in vesicle identity, specificity and fusion. The progenitor compartment contains, at least, a member of the Rab family, a syntaxin and a coat system (grey). Duplications of the genes encoding these factors facilitate differentiation of function (red, purple), yielding discrete organelles. This process continues in some cases, so that the A1 compartment further is differentiated to A1a and A1b (light and dark blue, respectively), whereas A2 is not elaborated. This may yield a new organelle or differentiation of an organelle into sub-domains or pathways in the case of the coatomers and adaptins (which yielded the cis-Golgi and trans-Golgi network). This general process could eventually have given rise to the organellar complement and machinery reconstructed as present in the LCEA. (C) Paralogous expansion appears variable across the eukaryotes and across machinery; all of the gene families shown were probably present in the LCEA but exhibit different levels of expansion in modern eukaryotes. Specifically there is little evidence for multiple genes encoding tether complex factors in most genomes, while at the other extreme there are many Rab and SNARE genes. Intermediate situations are found for the coatomer, adaptins and syntaxin-binding (SM) proteins; in some lineages either entire complexes or specific subunit families are expanded.

View larger version (41K): [in this window] [in a new window]   Fig. 3. Major transitions in evolution of the endomembrane system. In prokaryotes, secretion is a comparatively simple matter of translocation of polypeptides across the plasma membrane. Although there are several distinct mechanisms for achieving this, all appear to require an unfolded substrate for translocation. The type I, SRP/SecY-mediated, pathway is homologous to the co-translational ER import pathways of eukaryotes. In the hypothesized LCEA, comparative genomic evidence suggests that the major structures and pathways constituting the endomembrane system were already present, including the ER, Golgi complex and the main features of the endocytosis and recycling systems. The paralogous relationship of the families of SNAREs, Rabs, SM proteins and GTPases, as well as the homology of many coat components to each other and also to components of the nuclear pore complex, provide a potential mechanism for how this system arose. Compartmentalization and gene family expansion led to establishment of multiple protein systems capable of deforming membranes (i.e. transport steps). Elaboration of this basic pattern has been a major driving force for subsequent diversification of the endomembrane system, giving rise to the array of systems present in extant taxa. Subsequent evolution yielded multiple modes of endocytosis, specialized exocytic pathways and increased complexity of post-Golgi pathways. The red ovals indicate a trans-membrane translocation system. Lys, lysosome or vacuole; LCEA, last common eukaryotic ancestor. Small numbers in red indicate an associated pathway-specific Rab protein. The grey structure in the prokaryote indicates the non-compartmentalized genome.

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