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      Differentiation of Trafficking Pathways at Golgi Entry Core Compartments and Post-Golgi Subdomains

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          Abstract

          Eukaryotic cells have developed specialized membrane structures called organelles, which compartmentalize cellular functions and chemical reactions. Recent improvements in microscopy and membrane compartment isolation techniques are now sophisticating our view. Emerging evidences support that there are distinct sub-populations or subdomains, which are spatially and/or temporally segregated within one type of organelle, contributing to specify differential sorting of various cargos to distinct destinations of the cell. In plant cells, the Golgi apparatus represents a main trafficking hub in which entry occurs through a Golgi Entry Core Compartment (GECCO), that remains to be further characterized, and sorting of cargos is mediated through multiple transport pathways with different sets of regulator proteins at the post-Golgi compartment trans-Golgi network (TGN). Both GECCO and TGN are differentiated sub-populations as compared to the rest of Golgi, and moreover, further subdomain formation within TGN is suggested to play a key role for cargo sorting. In this review, we will summarize recent findings obtained on organelle subdomains, and their relationship with cargo entry at and exit from the Golgi apparatus.

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          Most cited references67

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          Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: Evidence for membrane cycling from Golgi to ER

          In cells treated with brefeldin A (BFA), movement of newly synthesized membrane proteins from the endoplasmic reticulum (ER) to the Golgi apparatus was blocked. Surprisingly, the glycoproteins retained in the ER were rapidly processed by cis/medial Golgi enzymes but not by trans Golgi enzymes. An explanation for these observations was provided from morphological studies at both the light and electron microscopic levels using markers for the cis/medial and trans Golgi. They revealed a rapid and dramatic redistribution to the ER of components of the cis/medial but not the trans Golgi in response to treatment with BFA. Upon removal of BFA, the morphology of the Golgi apparatus was rapidly reestablished and proteins normally transported out of the ER were efficiently and rapidly sorted to their final destinations. These results suggest that BFA disrupts a dynamic membrane-recycling pathway between the ER and cis/medial Golgi, effectively blocking membrane transport out of but not back to the ER.
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            Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis.

            In eukaryotic cells, compartments of the highly dynamic endomembrane system are acidified to varying degrees by the activity of vacuolar H(+)-ATPases (V-ATPases). In the Arabidopsis thaliana genome, most V-ATPase subunits are encoded by small gene families, thus offering potential for a multitude of enzyme complexes with different kinetic properties and localizations. We have determined the subcellular localization of the three Arabidopsis isoforms of the membrane-integral V-ATPase subunit VHA-a. Colocalization experiments as well as immunogold labeling showed that VHA-a1 is preferentially found in the trans-Golgi network (TGN), the main sorting compartment of the secretory pathway. Uptake experiments with the endocytic tracer FM4-64 revealed rapid colocalization with VHA-a1, indicating that the TGN may act as an early endosomal compartment. Concanamycin A, a specific V-ATPase inhibitor, blocks the endocytic transport of FM4-64 to the tonoplast, causes the accumulation of FM4-64 together with newly synthesized plasma membrane proteins, and interferes with the formation of brefeldin A compartments. Furthermore, nascent cell plates are rapidly stained by FM4-64, indicating that endocytosed material is redirected into the secretory flow after reaching the TGN. Together, our results suggest the convergence of the early endocytic and secretory trafficking pathways in the TGN.
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              Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle.

              Plants constantly adjust their repertoire of plasma membrane proteins that mediates transduction of environmental and developmental signals as well as transport of ions, nutrients, and hormones. The importance of regulated secretory and endocytic trafficking is becoming increasingly clear; however, our knowledge of the compartments and molecular machinery involved is still fragmentary. We used immunogold electron microscopy and confocal laser scanning microscopy to trace the route of cargo molecules, including the BRASSINOSTEROID INSENSITIVE1 receptor and the REQUIRES HIGH BORON1 boron exporter, throughout the plant endomembrane system. Our results provide evidence that both endocytic and secretory cargo pass through the trans-Golgi network/early endosome (TGN/EE) and demonstrate that cargo in late endosomes/multivesicular bodies is destined for vacuolar degradation. Moreover, using spinning disc microscopy, we show that TGN/EEs move independently and are only transiently associated with an individual Golgi stack.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                08 December 2020
                2020
                : 11
                : 609516
                Affiliations
                Laboratoire de Biogenèse Membranaire, Université de Bordeaux , Villenave d’Ornon, France
                Author notes

                Edited by: Eugenia Russinova, Ghent University, Belgium

                Reviewed by: Charlotte Kirchhelle, University of Oxford, United Kingdom; Georgia Drakakaki, University of California, Davis, United States

                *Correspondence: Yoko Ito, yoko.ito@ 123456u-bordeaux.fr

                This article was submitted to Plant Membrane Traffic and Transport, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.609516
                7752856
                33363561
                a4929e84-07f9-4fa2-8a54-877c904f6557
                Copyright © 2020 Ito and Boutté.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 23 September 2020
                : 23 November 2020
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 67, Pages: 8, Words: 6572
                Funding
                Funded by: the French National Research Agency
                Award ID: ANR-18-CE13-0025
                Funded by: Japan Society for Promotion of Science (JSPS)
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                membrane traffic,subdomains,secretion,endocytosis,lipids,trans-golgi network,golgi apparatus,protein sorting

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