Evolution of factors shaping the endoplasmic reticulum. (17th August 2022)

• Record Type: Journal Article
• Authors: Kontou, Aspasia; Herman, Emily K.; Field, Mark C.; Dacks, Joel B.; Koumandou, V. Lila
• Is Part Of: Traffic. Volume 23:Number 9(2022)
• Page Start: 462
• Page End: 473
• Publication Date: 2022-08-17
• Subjects: comparative genomics -- endomembrane system -- endoplasmic reticulum -- eukaryogenesis -- evolution -- last eukaryotic common ancestor -- phylogeny -- reticulons -- vesicular traffic; Biological transport -- Periodicals; 571.6
• DOI: 10.1111/tra.12863
• Languages: English
• ISSNs: 1398-9219

Abstract

Abstract: Endomembrane system compartments are significant elements in virtually all eukaryotic cells, supporting functions including protein synthesis, post‐translational modifications and protein/lipid targeting. In terms of membrane area the endoplasmic reticulum (ER) is the largest intracellular organelle, but the origins of proteins defining the organelle and the nature of lineage‐specific modifications remain poorly studied. To understand the evolution of factors mediating ER morphology and function we report a comparative genomics analysis of experimentally characterized ER‐associated proteins involved in maintaining ER structure. We find that reticulons, REEPs, atlastins, Ufe1p, Use1p, Dsl1p, TBC1D20, Yip3p and VAPs are highly conserved, suggesting an origin at least as early as the last eukaryotic common ancestor (LECA), although many of these proteins possess additional non‐ER functions in modern eukaryotes. Secondary losses are common in individual species and in certain lineages, for example lunapark is missing from the Stramenopiles and the Alveolata. Lineage‐specific innovations include protrudin, Caspr1, Arl6IP1, p180, NogoR, kinectin and CLIMP‐63, which are restricted to the Opisthokonta. Hence, much of the machinery required to build and maintain the ER predates the LECA, but alternative strategies for the maintenance and elaboration of ER shape and function are present in modern eukaryotes. Moreover, experimental investigations for ER maintenance factors in diverse eukaryotes are expected to uncover novel mechanisms. Abstract : More than 15 proteins have a role in shaping the endoplasmic reticulum (ER) but studies on the evolution of these factors are lacking. Now, a molecular evolutionary analysis indicates that reticulons, REEPs, atlastin, spastin, lunapark, TMEM33, STIM1 and VAPs likely evolved as early as the last eukaryotic common ancestor (LECA). Secondary losses are common, while more recent innovations are evident in the Opisthokonta. Future experimental investigations for these ER maintenance factors in diverse eukaryotes are expected to uncover novel mechanisms.