Plant Exocytosis, Endocytosis and Membrane Recycling in Turgid Cells

Lorenzo Frigerio, University of Warwick, Coventry, UK

Published online: June 2010

DOI: 10.1002/9780470015902.a0001676.pub2

Full Article on Wiley Online Library

In plant cells, growth is dependent on cell wall building and plasma membrane growth. Secretion of proteins is vital for cell function and cell–cell communication. The fusion of secretory vesicles at the plasma membrane (exocytosis) is a key mechanism because it delivers proteins and lipids to the plasma membrane and proteins and polysaccharides to the cell wall. The anterograde flow of membranes is balanced by endocytosis, which retrieves excess membrane and recycles plasma membrane receptors and transporters. Exocytosis and endocytosis have recently been shown to underpin the establishment of cell polarity which is key to the control of plant developmental processes. The balance of exocytosis and endocytosis is, therefore, crucial to both plant signalling and development, is highly regulated and is an exciting subject of current research.

Key Concepts:

Exocytosis is the fusion of secretory vesicles with the plasma membrane.
Endocytosis retrieves lipids and proteins from the plasma membrane.
The balance of exocytosis and endocytosis regulates cell growth, polarity and expansion, ultimately underpinning all plant developmental processes.

Keywords: plants; vesicle trafficking; secretory pathway; exocytosis; endocytosis; plasma membrane; cell wall; Golgi; endosomes; clathrin-coated vesicles

	Figure 1. Schematic diagram of the plant secretory pathway. Secretory vesicles (circles) transport polysaccharide precursors, membrane and proteins to the plasma membrane (PM). Coordination of the rate and distribution of exocytosis (red arrows) and endocytosis (blue arrows) is crucial to allow the cell to balance the demands of growth and differentiation. The exocytic and endocytic routes intersect at the trans-Golgi network/early endosome (TGN/EE). The concentration of plasma membrane proteins such as signalling receptors can be regulated by endocytosis and degradation of the proteins in the multivesicular body/prevacuolar compartment (MVB/PVC) and eventually in the vacuole. ER, endoplasmic reticulum; CW, cell wall.
	Figure 2. The tip of the pollen tube. Here very active exocytosis allows the tube to grow rapidly down the style of the flower and deliver the male gametes for fertilisation. Reproduced from Lancelle et al. (1997) by permission of the authors and Springer (Wien).
	Figure 3. Venus fly trap, Dionaea muscipula. This insectivorous plant obtains much of its nitrogen and other elements as protein from insects that are trapped on the sticky leaves. Secretion of hydrolytic enzymes by glands on the leaf surface is essential for the digestion of the prey. This secretion is achieved by exocytosis of vesicles containing the enzymes. Photograph courtesy of Dr Alastair Culham (Department of Botany, The University of Reading).
	Figure 4. Cell plate (arrowed) growing outwards to divide the two daughter nuclei. Tobacco BY2 cells were stained with aniline blue. Photograph courtesy of Dr Pim van Kesteren (Department of Horticulture, The University of Reading).
	Figure 5. Exocytotic configurations in the plasma membrane of a sycamore cell. This face view of the membrane reveals horseshoe shapes where the secretory vesicles, after fusion with the plasma membrane, have been flattened against the membrane. See Staehelin and Chapman (1987) and Battey et al. (1996) for further details.
	Figure 6. Transient or permanent fusion – alternatives according to need? (a) Fluctuations in plasma membrane capacitance signal recorded in a cell-attached patch of a maize coleoptile protoplast. (b) Interpretation. Left: rapid fluctuations represent transient fusion, cargo is discharged but the vesicle matrix and membrane recycled. Right: step change in capacitance reflecting full fusion and membrane incorporation. Cyt, cytoplasm; Out, outside of plasma membrane. Reproduced from Thiel and Battey (1998) by permission of the authors and Kluwer Academic Publishers (Dordrecht, The Netherlands).

References
	Alassimone J, Naseer S and Geldner NA (2010) Developmental framework for endodermal differentiation and polarity. Proceedings of the National Academy of Sciences of the USA 107: 5214–5219.
	Backues SK, Konopka CA, McMichael CM and Bednarek SY (2007) Bridging the divide between cytokinesis and cell expansion. Current Opinion in Plant Biology 10: 607–615.
	Battey N, Carroll A, van Kesteren P, Taylor A and Brownlee C (1996) The measurement of exocytosis in plant cells. Journal of Experimental Botany 47: 717–728.
	Bove J, Vaillancourt B, Kroeger J et al. (2008) Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiology 147: 1646–1658.
	Cram WJ (1980) Pinocytosis in plants. New Phytologist 84: 1–17.
	Dettmer J, Hong-Hermesdorf A, Stierhof Y D and Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715–730.
	Dhonukshe P, Aniento F, Hwang I et al. (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Current Biology 17: 520–527.
	Gradmann D and Robinson DG (1989) Does turgor prevent endocytosis in plant cells? Plant, Cell and Environment 12: 151–154.
	Hwang I and Robinson DG (2009) Transport vesicles formation in plant cells. Current Opinion in Plant Biology 12: 660–669.
	Kleine-Vehn J and Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annual Review of Cell and Developmental Biology 24: 447–473.
	Lancelle SA, Cresti M and Hepler PK (1997) Growth inhibition and recovery in freeze-substituted Lilium longiflorum pollen tubes: structural effects of caffeine. Protoplasma 196: 21–33.
	Lauber MH, Waizenegger I, Steinmann T et al. (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. Journal of Cell Biology 139: 1485–1493.
	Perez-Gomez J and Moore I (2007) Plant endocytosis: it is clathrin after all. Current Biology 20: R217–219.
	Segui-Simarro JM, Austin JR 2nd, White EA and Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16: 836–856.
	Staehelin LA and Chapman RL (1987) Secretion and membrane recycling in plant cells: novel intermediary structures visualized in ultra-rapidly frozen sycamore and carrot suspension-culture cells. Planta 171: 43–57.
	Steer MW and Steer JM (1989) Pollen tube tip growth. New Phytologist 111: 323–358.
	book Taiz L and Zeiger E (2006) Plant Physiology, Fourth Edition. Sunderland, MA: Sinauer Associates.
	Taylor LP and Hepler PK (1997) Pollen germination and tube growth. Annual Review of Plant Physiology and Plant Molecular Biology 48: 461–491.
	Thiel G and Battey NH (1998) Exocytosis in plants. Plant Molecular Biology 38: 111–125.
	Thiel G, Kreft M and Zorec R (1998) Unitary exocytotic and endocytotic events in Zea mays coleoptile protoplasts. Plant Journal 13: 101–104.
	Toyooka K, Goto Y, Asatsuma S et al. (2009) A mobile secretory vesicle cluster involved in mass transport from the Golgi to the plant cell exterior. Plant Cell 21: 1212–1229.
Further Reading
	Grefen C and Blatt MR (2008) SNAREs – molecular governors in signalling and development. Current Opinion in Cell Biology 11: 600–609.
	Moscatelli A and Idilli A (2009) Pollen tube growth: a delicate equilibrium between secretory and endocytic pathways. International Journal of Plant Biology 51: 727–739.
	Richter S, Voss U and Jurgens G (2009) Post-Golgi traffic in plants. Traffic 10: 819–828.
	Van Damme D, Inze D and Russinova E (2008) Vesicle trafficking during somatic cytokinesis. Plant Physiology 147: 1544–1552.

Article Title:	Plant Exocytosis, Endocytosis and Membrane Recycling in Turgid Cells
* Name:
* E-mail:
* Note:

Plant Exocytosis, Endocytosis and Membrane Recycling in Turgid Cells

Key Concepts:

Related Sub-Topics: