Exocytosis, Endocytosis and Membrane Recycling in Plant Cells

Abstract

In plants, cell growth is dependent on vacuole enlargement, cell wall deposition and plasma membrane extension. Secretion (exocytosis) and uptake (endocytosis) of materials are two vital processes for cell function and cell–cell communication. The fusion of secretory vesicles with the plasma membrane (PM) during exocytosis is essential for proper cell function because it delivers proteins and lipids to the PM as well as proteins and polysaccharides to the cell wall. Basically, secretory proteins can be transported to the PM through the Golgi apparatus (conventional protein secretion) or bypassing the Golgi (unconventional protein secretion) via vesicle‐mediated pathways. In mature, nongrowing cells, the anterograde flow of materials is balanced by endocytosis, which retrieves excess membrane and recycles PM receptors and transporters. Clathrin‐mediated endocytosis (CME) and membrane microdomain‐associated endocytosis (MME) are the major well‐characterised routes. The balance of exocytosis and endocytosis is tightly regulated, which is crucial to both plant development and signalling processes.

Key Concepts

  • Conventional protein secretion (CPS) is the trafficking route for secretory proteins that are transported through the endoplasmic reticulum (ER), Golgi apparatus and (plasma membrane) PM via secretory vesicles.
  • Unconventional protein secretion (UPS) is the process by which proteins are secreted by‐passing the Golgi apparatus.
  • Endocytosis in plants shares conserved features with those in animals but also possesses some evolutionarily unique components.
  • Clathrin‐mediated endocytosis (CME) and membrane microdomain‐associated endocytosis (MME) have been recognised to mediate the internalisation of cargo proteins.
  • The balance of exocytosis and endocytosis regulates proteins and lipids in the PM and mediates signalling transduction and plant adaptation to an ever‐changing environment.

Keywords: exocytosis; endocytosis; vesicle trafficking; plasma membrane; clathrin‐coated vesicle

Figure 1. Endosomal trafficking routes in plant cells. In the plant secretory pathway, proteins are translocated into the ER and then transported to the Golgi apparatus. Sorting events happen at the TGN/EE: proteins are either sorted to PVC/MVB/LE and later deposited into LV (black solid arrow) or secreted outside of the cell from the TGN to the PM via the conventional secretion pathway, which is also called exocytosis (purple dashed arrow). Protein secretion can also be mediated by unconventional protein secretion routes, such as Golgi bypassing route, PVC/MVB or EXPO mediated secretion (dark blue dashed arrow). In the endocytic pathways (purple solid arrow), proteins are internalised from the PM or extracellular space and first reach the TGN/EEs, where the exocytic and endocytic routes intersect. The abundance of PM‐resident proteins can be regulated by endocytosis and endosomal trafficking through the PVC/MVB/LE and eventually the LV, where proteins are degraded. Proteins can be recycled from either (1) MVB/PVC/LE, (2) TGN/EE or (3) Golgi as retrograde protein transport (green dashed arrow). ER, endoplasmic reticulum; EXPO, exocyst‐positive organelle; PVC/MVB/LE, prevacuolar compartment/multivesicular body/late endosome; LV, lytic vacuole; PM, plasma membrane; TGN/EE, trans‐Golgi network/early endosome.
Figure 2. Organelle‐mediated unconventional protein secretory pathway in plants. Various mechanisms are proposed for the exocytic protein secretion, including vacuole–PM fusion for the secretion of vacuolar contents (a), PVC/MVB–PM fusion for exosome formation (b) and EXPO mediated secretion, which are subsequently burst to release their contents to the apoplast (c).
Figure 3. Clathrin‐mediated endocytosis and membrane microsome‐associated endocytosis in plants. Clathrin‐mediated endocytosis (CME) is the major route to uptake extracellular materials and internalise PM‐localised proteins (black solid arrow). The conserved AP2 complex and plant‐specific TPLATE complex (TPC) perform overlapping but distinct functions during CME, especially the early stage. Membrane microsome‐associated endocytosis (MME) is independent of clathrin (Red solid arrow). Plant flotillins have been identified as a membrane microdomain marker and shown to play a crucial role in clathrin‐independent endocytosis. CW, cell wall; PM, plasma membrane; TGN/EE, trans‐Golgi network/early endosome; TPC, the TPLATE complex.
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Further Reading

Narasimhan M, Johnson A, Prizak R, et al. (2020) Evolutionarily unique mechanistic framework of clathrin‐mediated endocytosis in plants. eLife 9: e52067.

Robinson DG (2020) Plant Golgi ultrastructure. Journal of Microscopy. DOI: 10.1111/jmi.12899.

Shimada T, Takagi J, Ichino T, Shirakawa M and Hara‐Nishimura I (2018) Plant vacuoles. Annual Review of Plant Biology 69: 123–145.

Wang L, Xue Y, Xing J, Song K and Lin J (2018) Exploring the spatiotemporal organization of membrane proteins in living plant cells. Annual Review of Plant Biology 69: 525–551.

Zeng Y, Li B, Lin Y and Jiang L (2019) The interplay between endomembranes and autophagy in plants. Current Opinion in Plant Biology 52: 14–22.

Zhang L, Xing J and Lin J (2019) At the intersection of exocytosis and endocytosis in plants. The New Phytologist 224: 1479–1489.

Zhu D, Zhang M, Gao C and Shen J (2020) Protein trafficking in plant cells: tools and markers. Science China. Life Sciences 63: 343–363.

Zhuang X, Cui Y, Gao C and Jiang L (2015) Endocytic and autophagic pathways crosstalk in plants. Current Opinion in Plant Biology 28: 39–47.

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Shen, Jinbo, Wang, Xiangfeng, and Jiang, Liwen(Oct 2020) Exocytosis, Endocytosis and Membrane Recycling in Plant Cells. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029216]