Genome doubling enabled the expansion of yeast vesicle traffic pathways

Abstract

Vesicle budding and fusion in eukaryotes depend on a suite of protein types, such as Arfs, Rabs, coats and SNAREs. Distinct paralogs of these proteins act at distinct intracellular locations, suggesting a link between gene duplication and the expansion of vesicle traffic pathways. Genome doubling, a common source of paralogous genes in fungi, provides an ideal setting in which to explore this link. Here we trace the fates of paralog doublets derived from the 100-Ma-old hybridization event that gave rise to the whole genome duplication clade of budding yeast. We find that paralog doublets involved in specific vesicle traffic functions and pathways are convergently retained across the entire clade. Vesicle coats and adaptors involved in secretory and early-endocytic pathways are retained as doublets, at rates several-fold higher than expected by chance. Proteins involved in later endocytic steps and intra-Golgi traffic, including the entire set of multi-subunit and coiled-coil tethers, have reverted to singletons. These patterns demonstrate that selection has acted to expand and diversify the yeast vesicle traffic apparatus, across species and time.

An evolutionary perspective on Arf family GTPases

“…The final event in the genesis of the S. cerevisiae Arf family gene set was duplication of the ancestral Arf1 gene yielding a pair of lineage-specific paralogs (Arf1 and Arf2), which was part of the whole genome duplication (WGD) that occurred in the common ancestor of Saccharomyces and several related genera [24] (Figure 2). Although not the case for S. cerevisiae, taxon-specific expansions of the Arf family by gene duplication have been pervasive across eukaryotes in general.…”

Graphlet-based hyperbolic embeddings capture evolutionary dynamics in genetic networks

“…This domain is composed of GO-BPs such as 'export from cell', 'secretion by cell' and 'exocytosis', which are all vesicle traffic related functions. It has been shown that, as paralogs can be differentially expressed or regulated, or can have different interaction partners, they contribute to the robustness and versatility of the vesicle traffic pathway (Purkanti and Thattai, 2022). In conclusion, GraCoal 2 captures functional redundancy and functional specialisation in GI networks of species with many paralogs.…”