Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution

Abstract

The process by which some eukaryotic organelles, for example the endomembrane system, evolved without endosymbiotic input remains poorly understood. This problem largely arises because many major cellular systems predate the last common eukaryotic ancestor (LCEA) and thus do not provide examples of organellogenesis in progress. A model is emerging whereby gene duplication and divergence of multiple ''specificity-'' or ''identity-'' encoding proteins for the various endomembranous organelles produced the diversity of nonendosymbiotically derived cellular compartments present in modern eukaryotes. To address this possibility, we analyzed three molecular components of the endocytic membrane-trafficking machinery. Phylogenetic analyses of the endocytic syntaxins, Rab 5, and the ␤-adaptins each reveal a pattern of ancestral, undifferentiated endocytic homologues in the LCEA. Subsequently, these undifferentiated progenitors independently duplicated in widely divergent lineages, convergently producing components with similar endocytic roles, e.g., ␤1 and ␤2-adaptin. In contrast, ␤3, ␤4, and all other adaptin complex subunits, as well as paralogues of the syntaxins and Rabs specific for the other membrane-trafficking organelles, all evolved before the LCEA. Thus, the process giving rise to the differentiated organelles of the endocytic system appears to have been interrupted by the major speciation event that produced the extant eukaryotic lineages. These results suggest that although many endocytic components evolved before the LCEA, other major features evolved independently and convergently after diversification into the primary eukaryotic supergroups. This finding provides an example of a basic cellular system that was simpler in the LCEA than in many extant eukaryotes and yields insight into nonendosymbiotic organelle evolution.adaptin ͉ Rab ͉ SNARE ͉ trafficking ͉ autogenous

Identification and Dynamics of Arabidopsis Adaptor Protein-2 Complex and Its Involvement in Floral Organ Development

“…Detection of the a-and b-subunit isoforms in the mass spectrometry ( Figure 3C) implies they are functionally equivalent to each other. Our recent study revealed that both AP1/2B1 and AP1/2B2 also interact with the m-subunit of AP-1 complex (ADAPTOR PROTEIN-1 MU-ADAPTIN2 [AP1M2]) (Teh et al, 2013), indicating a common use of the b-subunit isoforms by AP-1 and AP-2 as predicted (Boehm and Bonifacino, 2001;Bassham et al, 2008;Dacks et al, 2008). Coimmunoprecipitation assays demonstrated the weak interaction between AP-2 and CHC ( Figure 3D), implying that the AP-2 complex is transiently associated with clathrin during CCV formation.…”

“…The Arabidopsis genome contains two homologous genes for each of the a and b subunits (Boehm and Bonifacino, 2001;Bassham et al, 2008;Dacks et al, 2008). This suggests that multiple sets of the different gene products are used to assemble the Arabidopsis AP-2 complex.…”

Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus

“…Endocytosis is known as a eukaryote-specific process by which cells internalize molecules from the plasma membrane and recycle them back to the surface or sort them to lysosomes for degradation (2). There is evidence that endocytosis must have been present in cells as far back as the last eukaryotic common ancestor (LECA) (3,4), but it has never been reported to occur in members of the domains Bacteria and Archaea. Recent hypotheses have placed the origin of endocytosis-like mechanisms as a primary step toward evolution of compartmentalization (3,4).…”

“…There is evidence that endocytosis must have been present in cells as far back as the last eukaryotic common ancestor (LECA) (3,4), but it has never been reported to occur in members of the domains Bacteria and Archaea. Recent hypotheses have placed the origin of endocytosis-like mechanisms as a primary step toward evolution of compartmentalization (3,4). Surprisingly, subcellular compartmentalization is not a unique feature of the eukaryote cell: it has been discovered that a restricted group of bacteria belonging to the phyla Planctomycetes and Verrucomicrobia possess such compartmentalization (5)(6)(7)(8).…”

Expanding Proteostasis by Membrane Trafficking Networks

“…3) Dacks et al 2008) as a quinary feature of proteostasis folding biology is used by the eukaryotic cell to manage when and where a protein folds, when the fold should or should not be functional, and when it should be removed through degradation. The invention of the TPN as a unifying theme for eukaryotic membrane biology was a pivotal advance accelerating the evolability of unicelluar and multicellular Eukarya to not only optimize and integrate cell and organismal function for a particular niche, but to promote survival and fitness through natural selection (Darwin 1856(Darwin , 1867.…”