Plant endosomal trafficking pathways

https://doi.org/10.1016/j.pbi.2011.07.009Get rights and content

Endosomes regulate both the recycling and degradation of plasma membrane (PM) proteins, thereby modulating many cellular responses triggered at the cell surface. Endosomes also play a role in the biosynthetic pathway by taking proteins to the vacuole and recycling vacuolar cargo receptors. In plants, the trans-Golgi network (TGN) acts as an early/recycling endosome whereas prevacuolar compartments/multivesicular bodies (MVBs) take PM proteins to the vacuole for degradation. Recent studies have demonstrated that some of the molecular complexes that mediate endosomal trafficking, such as the retromer, the ADP-ribosylation factor (ARF) machinery, and the Endosomal Sorting Complexes Required for Transport (ESCRTs) have both conserved and specialized functions in plants. Whereas there is disagreement on the subcellular localization of the plant retromer, its function in recycling vacuolar sorting receptors (VSRs) and modulating the trafficking of PM proteins has been well established. Studies on Arabidopsis ESCRT components highlight the essential role of this complex in cytokinesis, plant development, and vacuolar organization. In addition, post-translational modifications of plant PM proteins, such as phosphorylation and ubiquitination, have been demonstrated to act as sorting signals for endosomal trafficking.

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.

References (65)

  • B.H. Kang et al.

    Electron tomography of RabA4b- and PI-4Kbeta1-labeled trans Golgi network compartments in Arabidopsis

    Traffic

    (2011)
  • C.-M. Chow et al.

    Rab-A2 and Rab-A3 GTPases define a trans-Golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate

    Plant Cell

    (2008)
  • M.S. Otegui et al.

    The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies

    Plant Cell

    (2006)
  • S. Hanton et al.

    Post-Golgi protein traffic in the plant secretory pathway

    Plant Cell Rep

    (2007)
  • A. Brüx et al.

    Reduced V-ATPase activity in the trans-Golgi network causes oxylipin-dependent hypocotyl growth inhibition in Arabidopsis

    Plant Cell

    (2008)
  • D. Gendre et al.

    Conserved Arabidopsis ECHIDNA protein mediates trans-Golgi-network trafficking and cell elongation

    Proc Natl Acad Sci U S A

    (2011)
  • D.C. Bassham et al.

    AtVPS45 complex formation at the trans-Golgi network

    Mol Biol Cell

    (2000)
  • K. Toyooka et al.

    A mobile secretory vesicle cluster involved in mass transport from the Golgi to the plant cell exterior

    Plant Cell

    (2009)
  • I.J. McGough et al.

    Recent advances in retromer biology

    Traffic

    (2011)
  • S. Niemes et al.

    Retromer recycles vacuolar sorting receptors from the trans-Golgi network

    Plant J

    (2010)
  • M. Yamazaki et al.

    Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence

    Plant Cell Physiol

    (2008)
  • T. Shimada et al.

    AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins

    Plant Cell Physiol

    (2006)
  • Y. Jaillais et al.

    AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis

    Nature

    (2006)
  • Y. Jaillais et al.

    The retromer protein VPS29 links cell polarity and organ initiation in plants

    Cell

    (2007)
  • J. Kleine-Vehn et al.

    Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting

    Proc Natl Acad Sci U S A

    (2008)
  • Y. Hashiguchi et al.

    Loss-of-function mutations of retromer large subunit genes suppress the phenotype of an Arabidopsis zig mutant that lacks Qb-SNARE VTI11

    Plant Cell

    (2010)
  • M. Pourcher et al.

    Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana

    Plant Cell

    (2010)
  • V. Vanoosthuyse et al.

    Interaction of calmodulin, a sorting nexin and kinase-associated protein phosphatase with the Brassica oleracea S locus receptor kinase

    Plant Physiol

    (2003)
  • H. Zheng et al.

    The plant vesicle-associated SNARE AtVTI1a likely mediates vesicle transport from the trans-Golgi network to the prevacuolar compartment

    Mol Biol Cell

    (1999)
  • R. Rojas et al.

    Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7

    J Cell Biol

    (2008)
  • P. Oliviusson et al.

    Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors

    Plant Cell

    (2006)
  • Y. Jaillais et al.

    Evidence for a sorting endosome in Arabidopsis root cells

    Plant J

    (2008)
  • Cited by (0)

    View full text