Evolution of the ribbon-like organization of the Golgi apparatus in animal cells

• Published in: Cell reports (Cambridge) Vol. 43; no. 3; p. 113791
• Main Authors: Benvenuto, Giovanna, Leone, Serena, Astoricchio, Emanuele, Bormke, Sophia, Jasek, Sanja, D’Aniello, Enrico, Kittelmann, Maike, McDonald, Kent, Hartenstein, Volker, Baena, Valentina, Escrivà, Héctor, Bertrand, Stephanie, Schierwater, Bernd, Burkhardt, Pawel, Ruiz-Trillo, Iñaki, Jékely, Gáspár, Ullrich-Lüter, Jack, Lüter, Carsten, D’Aniello, Salvatore, Arnone, Maria Ina, Ferraro, Francesco
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 26.03.2024
• Subjects: AlphaFold2; Animals; Cytoskeleton - metabolism; development; evolution; GM130; Golgi Apparatus - metabolism; Golgi ribbon; Golgi structure; Golgin-45; GRASP; HeLa Cells; Humans; Life Sciences; Membrane Proteins - metabolism; metazoans; organelle; Vertebrates; metazoans; development; Golgi ribbon; Golgi structure; GM130; CP: Cell biology; organelle; AlphaFold2; CP: Evolution; evolution; GRASP; Golgin-45
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2024.113791

The “ribbon,” a structural arrangement in which Golgi stacks connect to each other, is considered to be restricted to vertebrate cells. Although ribbon disruption is linked to various human pathologies, its functional role in cellular processes remains unclear. In this study, we investigate the evolutionary origin of the Golgi ribbon. We observe a ribbon-like architecture in the cells of several metazoan taxa suggesting its early emergence in animal evolution predating the appearance of vertebrates. Supported by AlphaFold2 modeling, we propose that the evolution of Golgi reassembly and stacking protein (GRASP) binding by golgin tethers may have driven the joining of Golgi stacks resulting in the ribbon-like configuration. Additionally, we find that Golgi ribbon assembly is a shared developmental feature of deuterostomes, implying a role in embryogenesis. Overall, our study points to the functional significance of the Golgi ribbon beyond vertebrates and underscores the need for further investigations to unravel its elusive biological roles. [Display omitted] •The cells of several animal taxa have a ribbon-like Golgi configuration•Ribbon-like Golgi emergence may be explained by the evolution of a GRASP/golgin complex•Formation of the ribbon-like Golgi in early embryos suggests its role in development Benvenuto et al. challenge the current consensus by revealing the pre-vertebrate origin of ribbon-like Golgi architecture and suggest a molecular basis for its evolution supported by AlphaFold modeling. Observing its formation early in embryogenesis, the authors also propose that the ribbon-like Golgi configuration plays a role in development.