Seminars in Cell & Developmental Biology 18 (2007) 471–478 Review Coated vesicles in plant cells Matthew J. Paul, Lorenzo Frigerio ∗ Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom Available online 10 July 2007 Abstract Coated vesicles represent vital transport intermediates in all eukaryotic cells. While the basic mechanisms of membrane exchange are conserved through the kingdoms, the unique topology of the plant endomembrane system is mirrored by several differences in the genesis, function and regulation of coated vesicles. Efforts to unravel the complex network of proteins underlying the behaviour of these vesicles have recently benefited from the application in planta of several molecular tools used in mammalian systems, as well as from advances in imaging technology and the ongoing analysis of the Arabidopsis genome. In this review, we provide an overview of the roles of coated vesicles in plant cells and highlight salient new developments in the field. © 2007 Elsevier Ltd. All rights reserved. Keywords: Plant secretory pathway; Protein trafficking; Endocytosis; Endoplasmic reticulum; Golgi; Vacuole; Coated vesicles; Clathrin; COPI; COPII; Retromer Contents 1. Vesicular trafficking in plant cells ......................................................................................... 471 2. Small GTP-binding proteins and associated factors ......................................................................... 473 3. Plant vesicle coat families ................................................................................................ 473 3.1. Clathrin .......................................................................................................... 473 3.2. COPI and COPII .................................................................................................. 474 3.3. Retromer......................................................................................................... 475 4. Conclusions and perspectives ............................................................................................. 475 Acknowledgements ..................................................................................................... 476 References ............................................................................................................. 476 1. Vesicular trafficking in plant cells The endoplasmic reticulum, a dynamic mesh-like structure traversing the cortical cytoplasm of plant cells, represents the The plant endomembrane system encompasses a series of entry compartment for nascent polypeptides destined for secre- compartments which provide specialised surfaces and segre- tion [1–3]. From the ER, cargo molecules following the secretory gated areas for the production and storage of biomolecules. An pathway reach a stack of the fragmented, mobile Golgi appara- overview of the plant secretory pathway and the coated vesicles tus [4] without passing through an intermediate compartment described in this review is shown in Fig. 1. such as the mammalian vesiculo-tubular compartment (VTC [5]). Compelling evidence now exists to support an extremely close functional and physical relationship between plant ER and Abbreviations: CCV, clathrin-coated vesicles; CHC, clathrin heavy chain; Golgi compartments ([6,7], reviewed in Ref. [8]). Nevertheless, CLC, clathrin light chain; ER, endoplasmic reticulum; ERES, endoplasmic retic- the formation of coatomer (COPI and COPII) transport inter- ulum export sites; GAP, GTPase activating protein; GEF, guanosine nucleotide mediates remains essential for the transfer of cargo and for the exchange factor; LV, lytic vacuole; MVB, multivesicular body; PVC, prevacuo- maintenance of membrane flux [6,9]. lar compartment; PSV, protein storage vacuole; VSR, vacuolar sorting receptor; Anterograde transport routes from the Golgi stacks and ret- VTC, vesiculo-tubular compartment ∗ Corresponding author. Fax: +44 24 765 23701. rograde (endocytic) routes from the cell surface converge at a E-mail address: [email protected] (L. Frigerio). poorly defined group of compartments, interchangeably termed 1084-9521/$ – see front matter © 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.semcdb.2007.07.005 472 M.J. Paul, L. Frigerio / Seminars in Cell & Developmental Biology 18 (2007) 471–478 Fig. 1. A model for the distribution of coated vesicles and receptor proteins throughout the plant endomembrane system. Coloured circles represent soluble cargo molecules within the secretory/endocytic pathway and black arrows denote presumptive membrane fusion events. Cargoes entering the pathway at the level of the ER proceed towards the Golgi apparatus via COPII-coated vesicles, possibly following interaction with receptor proteins of the p24 family [84–86] or after passive diffusion into an ERES [8]. It is also possible that anterograde transport by cisternal maturation may occur for certain cargoes. ER resident proteins (orange circles) are recycled from downstream compartments by the plant ERD2 receptor homologue, while a distinct subpopulation of COPI coats (COPIb; [12]) mediates intra-Golgi retention and recycling events. Cargoes progress from the Golgi towards vacuoles either in uncoated, ‘dense’ vesicles [20,21] or clathrin-coated vesicles [12,22] depending on the nature of the cargo and/or the presence of a cognate cargo receptor. Clathrin-coated vesicles are also involved in endocytosis, e.g. that of the auxin transporter PIN2 [11], and these coats may be distinguished by the presence of distinct sets of adaptor proteins [55,59]. Finally, retromer coats have been implicated in the retrieval of cargo receptors from the PVC [23,26]. Abbreviations: ER, endoplasmic reticulum, ERES, ER export site, CCV, clathrin-coated vesicle, DV, dense vesicle, PVC, prevacuolar compartment, MVB, multivesicular body, VSR, vacuolar sorting receptor. prevacuolar compartments (PVC) or endosomes [10]. Very tion of a full range of key plant orthologues for proteins with recently, clathrin-coated vesicles (CCV) have been convincingly established roles in clathrin-mediated transport in mammals shown to be implicated in endocytosis in the plant secretory and yeasts. pathway [11]. This is consistent with their observed distribution Plant cells also contain functional orthologues of the retromer within the cell [12–14]. In mammalian and yeast cells, CCV are coat complex which was first identified and characterised in also involved in post-Golgi trafficking routes to a terminal intra- yeast [23,24]. In yeast cells, retromer is required for the recy- cellular compartment [15,16]. In plant cells, the precise role of cling of cargo receptors from the pre-vacuolar compartment to clathrin in anterograde transport is still a matter of some debate the trans-Golgi [25]. Consistent with an equivalent role in plant as there exist at least two separate routes to functionally distinct cells, a component of the plant retromer complex is required for vacuolar compartments [17–19]. In addition, some plants can the correct sorting of vacuolar cargo in developing Arabidopsis handle post-Golgi sorting of storage proteins through electron- seed [26]. opaque, ‘dense’ vesicles (DV) with no detectable protein coat The similarity between vesiculation events in plants and those [20,21]. However, a role for clathrin in vacuolar transport in of mammalian and yeast cells has provided invaluable clues plant cells is illustrated by the recent in situ detection of clathrin into the function of the plant endomembrane system. However, coats in restricted regions around the trans-Golgi cisternae of the unique topology, compartments and cargoes present in the the Golgi apparatus [12,22]. The concept of multiple roles plant secretory pathway necessitate the close examination of for clathrin coats in plant cells is supported by the identifica- each aspect of vesicular transport in these cells. Here, we review M.J. Paul, L. Frigerio / Seminars in Cell & Developmental Biology 18 (2007) 471–478 473 the latest findings concerning the roles of various vesicle coats 3. Plant vesicle coat families in the selective recruitment of cargo at each step of this path- way and highlight plant-specific adaptations to the vesiculation 3.1. Clathrin machinery. The clathrin coat was the first proteinaceous vesicle coat to be 2. Small GTP-binding proteins and associated observed [38] and structurally characterised [39]. It remains the factors most fully understood coat complex in both plants and animals today. Three structural clathrin heavy chain molecules (CHC, In common with mammals and yeasts, plant vesiculation Mr ∼180 kDa) come together through the interactions between events are governed by members of the Ras superfamily of domains near the C-termini of the heavy chains to form a triske- small GTP binding proteins [27]. The Arf subfamily of small lion, the basic structural unit of the clathrin coat. Purified CHC GTPases, which includes the Sar, ARF and ARF-like ARL triskelia demonstrate self-assembly at a physiological pH [40] to GTPases, are involved in the formation and budding of vesi- form cages which have been the focus of detailed structural stud- cles throughout the plant endomembrane system [28,29]. ARF ies [41,42]. CHC is encoded by two genes in both mammals and GTPases are associated with clathrin coats as well as COPI Arabidopsis and displays a remarkable degree of conservation coated vesicles, whereas COPII coat nucleation is triggered by between the two organisms (∼75% similarity, [13]). Each heavy