Evolutionary cell biology traces the rise of the exomer complex in Fungi from an ancient eukaryotic component

Abstract

Cargo is transported from the trans-Golgi Network to the plasma membrane by adaptor complexes, which are pan-eukaryotic components. However, in yeast, cargo can also be exported by the exomer complex, a heterotetrameric protein complex consisting of two copies of Chs5, and any two members of four paralogous proteins (ChAPs). To understand the larger relevance of exomer, its phylogenetic distribution and function outside of yeast need to be explored. We find that the four ChAP proteins are derived from gene duplications after the divergence of Yarrowia from the remaining Saccharomycotina, with BC8 paralogues (Bch2 and Chs6) being more diverged relative to the BB8 paralogues (Bch1 and Bud7), suggesting neofunctionalization. Outside Ascomycota, a single preduplicate ChAP is present in nearly all Fungi and in diverse eukaryotes, but has been repeatedly lost. Chs5, however, is a fungal specific feature, appearing coincidentally with the loss of AP-4. In contrast, the ChAP protein is a wide-spread, yet uncharacterized, membrane-trafficking component, adding one more piece to the increasingly complex machinery deduced as being present in our ancient eukaryotic ancestor.

Exomer complex regulates protein traffic at the TGN through differential interactions with cargos and clathrin adaptor complexes

“…Thus, we sought to analyze whether these relationships have been conserved along evolution. Considering the evolutionary distribution of the exomer complex, 71 we decided to analyze this relationship in Candida albicans where both complexes exist. Given the effect of exomer on polarized exocytosis in Saccharomyces cerevisiae , we examined filamentous growth which strongly depends on polarized exocytosis.…”

“…These subunits lack the cargo binding activity of the Chs6/Bch2, 22,23 suggesting that exomer may also contribute to the transport of proteins through its action in coat assembly in addition to its direct role as cargo adaptor. Since Bch1/Bud7 are less divergent from the ChAP representative found in the root of the fungal evolutionary tree, this may suggest that this coat function is the ancestral role of the complex 29,71 …”

Paralogous gene modules derived from ancient hybridization drive vesicle traffic evolution in yeast

“…A disproportionate number of paralogous gene modules have been retained in the yeast vesicle traffic system, 100 million years after they arose by hybridization. Though duplicate vesicle traffic modules have been described previously [49,50], the fact many of these have a common origin has not been appreciated. It is only when these instances are identified and analyzed together that we truly see the scale and long-term impact of this ancient genome doubling event.…”

Exomer Is Part of a Hub Where Polarized Secretion and Ionic Stress Connect

“…Exomer is present in Fungi and absent from Metazoa ( Trautwein et al, 2006 ; Anton et al, 2018 ; Ramirez-Macias et al, 2018 ). All fungi bear one Chs5 homolog and one, two, or four ChAPs, with a Bch1 homolog always present.…”