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

The structural and functional unit of the Golgi apparatus is the stack, formed by piled membranous cisternae ^1,2 . Among eukaryotes the number of stacks ranges from one to several copies per cell ³ . When present in multiple copies, the Golgi is observed in two arrangements: stacks either remain separated or link into a centralized structure referred to as the “ribbon”, after its description by Camillo Golgi ⁴ . This Golgi architecture is considered to be restricted to vertebrate cells and its biological functions remain unclear ^3,5–9 .

Here we show that the ribbon-like Golgi organization is instead present in the cells of several animals belonging to the cnidarian and bilaterian clades, implying its appearance in their common ancestor. We hypothesize a possible scenario driving this structural innovation. The Golgi Reassembly and Stacking Proteins, GRASPs, are central to the formation of the mammalian Golgi ribbon by mediating stack tethering ^10–15 . To link the stacks, GRASPs must be correctly oriented on Golgi membranes through dual anchoring including myristoylation and interaction with a protein partner of the Golgin class ^16,17 . We propose that the evolution of binding of Golgin-45 to GRASP led to Golgi stack tethering and the appearance of the ribbon-like organization. This hypothesis is supported by AlphaFold2 modelling of Golgin-45/GRASP complexes of animals and their closest unicellular relatives. Early evolution and broad conservation of the ribbon-like Golgi architecture imply its functional importance in animal cellular physiology. We anticipate that our findings will stimulate a wave of new studies on the so far elusive biological roles of this Golgi arrangement.