Exocytosis and Endocytosis

Abstract

Exocytosis is a general term used to denote vesicle fusion at the plasma membrane, and it is the final step in the secretory pathway that typically begins in the endoplasmic reticulum (ER), passes through the Golgi apparatus, and ends at the outside of the cell. Endocytosis refers to the recovery of vesicles from the plasma membrane. Exocytotic vesicle fusion involves the coalescence of vesicle and plasma membranes and allows the so-called fusion pore to form. The fusion pore is a channel that passes through the vesicle and plasma membranes and allows delivery of the vesicle contents to the extracellular compartment. Docking is the process by which the exocytotic vesicle is fixed beneath the plasma membrane before fusion. It is generally believed to involve molecular recognition between vesicle and plasma membrane and is therefore one aspect of vesicle targeting. Another kind of targeting can be provided by the cytoskeletal proteins that move vesicles around the cell. Sorting is a term that can be applied to vesicles, in which case it simply describes the consequences of targeting. Sorting has a more useful and distinct meaning when applied to vesicle contents: these contents vary according to the destination of the vesicle and the state of differentiation of the cell. Sorting of contents can occur in the ER or Golgi or post-Golgi compartments, as can processing, in which polysaccharides or proteins are modified enzymatically into their mature form, ready for delivery. The problem in discussing exocytosis and endocytosis is deciding where to start and where to finish: it is difficult to consider vesicle fusion without docking, docking without targeting, and targeting without sorting. Similarly, to stop at the point of vesicle retrieval (perhaps only microseconds after its fusion) is arbitrary, if only because the subsequent journey can involve recycling (see, e.g., Murthy and Stevens, 1998), so that the same vesicle may visit the plasma membrane many times. Furthermore, for a full explanation of exocytosis and endocytosis, we must consider the myriad uses to which these processes are put in the full diversity of plant cell types; vesicle trafficking pathways are likely to vary according to the needs of the cell and its stage of development. Figure 1illustrates the range of secretory vesicle/plasma membrane dynamics that require mechanistic explanations. In this review, we follow the secretory vesicle on its journey from the Golgi apparatus to the plasma membrane and discuss the factors that control its docking, fusion, and recycling there. We emphasize the relatively new results from plant cells but place these against a background of data from animal cells and yeast, in which more is known. One interesting feature of exocytosis in plants is its Ca2+ sensitivity, and we discuss the significance of this in relation to the known importance of Ca2+ as an intracellular regulator. Finally, we consider key areas for future study that will lead to a more complete understanding of the role that the regulation of exocytosis and endocytosis plays in plant development. A recent review indicated that there are at least three parallel pathways from the Golgi apparatus to the cell surface in mammals and that these pathways operate to varying extents in different cell types (Keller and Simons, 1997). There is no reason to suppose that in plants the situation is any less complex. Indeed, the older, morphological literature abounds with possible pathways and vesicle types (see Battey and Blackbourn, 1993). It cannot be determined by inspection whether vesicles are exocytotic, endocytotic, or bound for destinations other than the plasma membrane. In many cases, however, particularly in green algae (Domozych, 1991), it seems clear that there is more than one type of vesicle delivered to the plasma membrane. Electrophysiological data similarly indicate at least two vesicle populations in barley aleurone protoplasts (Homann and Tester, 1997). We must nevertheless await future classification of the factors that sort vesicle contents and regulate the delivery of different vesicle types to the plasma membrane. A major technical obstacle is the lack of good assays of the kind that have been used so widely and effectively in mammalian and yeast cells for analysis of post-Golgi transport (reviewed in Battey et al., 1996). The Exocytotic Pathway in Plants. (A) The pollen tube. At left, aniline-blue staining of pollen tubes growing from the stigmatic surface down the style of Capsicum. Photograph courtesy of Dr. Naci Onus (Department of Agricultural Botany, University of Reading). At right, directional exocytosis maintains polar growth in the lily pollen tube. Golgi vesicles accumulate at the tip, where they undergo exocytosis to supply membrane and wall material for growth. ×3240. Reprinted from Lancelle et al. (1997), by permission of the authors and Springer-Verlag, Vienna. (B) The honeysuckle nectary. At left, honeysuckle flowers.