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

Inmaculada Ramirez-Macias,Joel B Dacks,Lael D Barlow,Carlos Anton,Cesar Roncero,Anne Spang

doi:10.1038/s41598-018-29416-4

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.

Highlights

Trafficking through an elaborate set of endomembrane organelles allows for spatially distributed and compartmentalized chemical microenvironments that are required for proper tissue and cellular function in eukaryotes
We find that Bch[1] and Bud[7] are the result of a specific duplication very near the divergence of the Saccharomyces, as are Bch[2] and Chs[6]
In S. cerevisiae, the exomer complex serves as a potential adaptor complex for the export of cargo from the trans-Golgi Network (TGN) to the plasma membrane

Summary

Introduction

Trafficking through an elaborate set of endomembrane organelles allows for spatially distributed and compartmentalized chemical microenvironments that are required for proper tissue and cellular function in eukaryotes. Such internalization is undertaken by the endocytic pathway, while release of material and presentation on the cell surface is mediated by the secretory pathway[4] This secretory pathway consists of distinct steps for anterograde and retrograde transport between the membrane compartments. It can go directly from the TGN to the PM (with or without endosomal intermediates) mediated by AP-1 or AP-4 complex binding[9] Besides these pathways, cargo can be exported from the TGN to the PM in an AP-independent manner. The ChAPs are homologous proteins, they vary in their contribution to exomer assembly[14]

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Conclusion