ER-to-Golgi traffickingviaa dynamic intermediatecis-Golgi tubular network in Arabidopsis

Abstract

Endoplasmic Reticulum (ER)-to-Golgi trafficking is a central process of the secretory system of eukaryotic cells that ensures proper spatiotemporal sorting of proteins and lipids. However, the nature of the ER-Golgi Intermediate Compartments (ERGIC) and the molecular mechanisms mediating the transition between the ERGIC and the Golgi, as well as the universality of these processes amongst Eukaryotes, remain undiscovered. Here, we took advantage of the plant cell system in which the Golgi is highly dynamic and in close vicinity to the ER. We discovered that the ERGIC is composed from at least two distinct subpopulations of cis-Golgi. A subpopulation is a reticulated tubulo-vesicular network mostly independent from the Golgi, highly dynamic at the ER-Golgi interface and crossed by ER-induced release of luminal cargos at early stage. Another subpopulation is more stable, cisterna-like and mostly associated to the Golgi. Our results identified that the generation and dynamics of the ER-Golgi intermediate tubulo-vesicular network is regulated by the acyl-chain length of sphingolipids as well as the contacts it establishes with existing Golgi cisternae. Our study is a major twist in the understanding of the Golgi by identifying that the ERGIC in plants is a Golgi-independent highly dynamic tubular network from which arise more stable cisternae-like Golgi structures. This novel model presents a mechanism for early secretory trafficking adapted to respond to developmental and environmental stimuli, including susceptibility or resistance to diseases, autophagy or cell-reprograming.

Neosynthesized polarized and non-polarized plasma membrane cargoes follow distinct trafficking routes inAspergillus nidulans

“…The establishment of distinct trafficking routes at a very early secretory compartment has also been recently supported by findings showing the existence of two types of ERGIC subpopulations in plants. One subpopulation forms a dynamic reticulated tubulovesicular network, generated independently from Golgi maturation, while the other subpopulation is more stable, more cisterna-like, and dependent on Golgi (Fougère et al, 2023). Apparently, the generation of two types of ERGIC serves the trafficking of structurally and functionally different cargoes.…”

“…Proper integration into the ER membrane is followed by partitioning of membrane cargoes into ER-exit sites (ERes), which define distinct microdomains promoting the bud-off of vesicles (Zanetti et al, 2013;D'Arcangelo et al, 2013;Feyder et al, 2015;Gomez-Navarro & Miller, 2016) or tubules (Shomron et al, 2021;Weigel et al, 2021;Raote & Malhotra, 2021;Phuyal & Farhan, 2021). Vesicles or tubules loaded with membrane cargoes are directed to and fuse with the early-or cis-Golgi, seemingly via a dynamic pre-Golgi compartment, known as ERGIC (ER-to-Golgi Intermediate Compartment) in mammals and yeast, or the Golgi entry core compartment (GECCO) in plant cells (Peotter et al, 2019;Aridor, 2018;Wong-Dilworth et al, 2023;Tojima et al, 2023;Fougère et al, 2023). Once in the early-Golgi, cargoes 'advance' towards the medial-and late-Golgi to the trans-Golgi and the trans-Golgi Network (TGN), through Golgi maturation (Glick & Luini, 2011;Suda & Nakano, 2012;Day et al;Pantazopoulou & Glick, 2019;Lujan & Campelo, 2021;Tojima et al, 2023).…”