Plant endosomal trafficking pathways
Highlights
► Endosomes control multiple signaling pathways and cellular processes in plants. ► Trans-Golgi networks and multivesicular bodies are the best characterized plant endosomal compartments. ► The ESCRT and retromer complexes have both conserved and specialized functions in plants. ► Post-translational modifications of plasma proteins are important for endosomal trafficking.
Introduction
Endosomes traffic membrane and proteins from both the endocytic and biosynthetic pathways. Endosomal sorting of signaling receptors, transporters, and other plasma membrane (PM) proteins is a key regulatory process that controls the protein composition of the PM and therefore, the ability of the cells to respond to extracellular stimuli. PM proteins are continuously internalized by endocytosis and delivered to endosomes for sorting either back to the PM (recycling) or to degradation in vacuoles/lysosomes. Animal endosomes are classified in early, recycling, intermediate, and late endosomes/multivesicular bodies (MVBs). The main function of early and recycling endosomes is to receive and recycle both endocytosed membrane proteins back to the PM and vacuolar cargo receptors back to the trans-Golgi network (TGN). Intermediate and late endosomes/MVBs sort membrane proteins into endosomal intraluminal vesicles (ILVs) to be degraded by vacuolar/lysosomal hydrolases upon fusion between late endosomes and vacuoles/lysosomes. In addition, late endosomes/MVBs also carry newly synthesized vacuolar proteins from the Golgi to lysosomes/vacuoles (Figure 1).
Endosomes can regulate multiple trafficking pathways by coordinating the recognition, concentration, and packaging of cargo proteins by different molecular coat complexes such as the Endosomal Sorting Complex Required for Transport (ESCRTs) for degradative sorting and the retromer for recycling. How are cargo proteins recognized by the different endosomal complexes? In some cases, the mechanism of recognition depends on direct interactions between the cargo proteins and the sorting complexes whereas in other cases it relies on post-translational modifications of cargo proteins. Plants have conserved eukaryote endosomal functions but they have also evolved specific variations on the organization of their endosomal system and the molecular machinery that controls endosomal sorting. Here we discuss recent advances in our understanding of how endosomal sorting mechanisms operate in plants.
Section snippets
General organization of the endosomal system in plants
Only two endosomal organelles have been clearly identified and characterized in plants: the TGN/TGN-derived compartments that act as recycling/early endosomes and the late endosomes or MVBs, also called prevacuolar compartments. The typical tubulo-vesicular early endosomes found in mammals have not been described in plants.
Multivesicular bodies and ESCRT-mediated degradative sorting
In most cases, the ubiquitination of PM proteins acts as a signal for their internalization and degradation. At the endosomal membranes, the ESCRTs bind and concentrate the ubiquitinated cargo and mediate their sorting into ILVs.
In fungi and metazoans, five multimeric ESCRT-related complexes have been identified. ESCRT-0 binds PI3P and clathrin on the endosomal membranes, recognizes the ubiquitinated membrane proteins, and interacts with ESCRT-I. In an in vitro study using giant unilamellar
Conclusions
Endosomal trafficking pathways are emerging as central regulators of PM protein homeostasis, controlling multiple signaling pathways and developmental processes in eukaryotic cells. In the last few years, we have learned a great deal on how the plant endosomal system is organized and started to gain insights on how the major endosomal sorting machineries regulate the trafficking of transmembrane protein cargo. There are still many unanswered questions in the field. How are the biosynthetic and
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgement
The research conducted in the Otegui Laboratory on plant endosomal trafficking is supported by NSF grants MCB-0843151 and MCB-1048847.
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