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Traffic between the plant endoplasmic reticulum and Golgi apparatus: to the Golgi and beyond Loren A Matheson1, Sally L Hanton1 and Federica Brandizzi1,2 Significant advances have been made in recent years that have increased our understanding of the trafficking to and from membranes that are functionally linked to the Golgi apparatus in plants. New routes from the Golgi to organelles outside the secretory pathway are now being identified, revealing the importance of the Golgi apparatus as a major sorting station in the plant cell. This review discusses our current perception of Golgi structure and organization as well as the molecular mechanisms that direct traffic in and out of the Golgi. Addresses 1 Department of Biology, 112 Science Place, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5E2, Canada 2 Department of Energy, Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, USA Corresponding author: Brandizzi, Federica ([email protected]) Current Opinion in Plant Biology 2006, 9:601–609 This review comes from a themed issue on Cell biology Edited by Laurie G Smith and Ulrike Mayer Available online 28th September 2006 1369-5266/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2006.09.016 (for ‘secretion associated, ras-related protein1’) and two structural heterodimers, Sec23/24 and Sec13/31. The nature of the transport intermediates that carry cargo from the ER to the Golgi is unknown; however, there is speculation surrounding the existence of closed compartments, such as vesicles or tubules, and the possibility that export occurs via a direct connection (reviewed by [1]). Various protein motifs that mediate the export of transmembrane proteins from the ER have been identified ([5,6,7]; Figure 1), but it remains to be shown whether these signals recruit or are recruited by the cytosolic COPII components. No signals have been discovered for soluble cargo intended for forward transport in the secretory pathway; it appears that a bulk flow mechanism transports these proteins [8]. Proteins move from the Golgi to the ER via retrograde transport. In contrast to the anterograde route, the retrograde route depends on signals that mediate the transport of transmembrane and soluble proteins (Figure 1; [9,10]). The retrograde route is thought to be mediated by COPI, which consists of the small GTPase ADP-RIBOSYLATION FACTOR1 (ARF1) plus a heptameric complex of structural coat components, homologs of most of which have been identified in plants (reviewed by [11]). Inhibition of COPI function results in impaired ER export and disruption of the ERES [4], indicating the possibility of a role for ARF1 in anterograde transport in addition to its role in retrograde transport. Introduction A central function has been attributed to the Golgi apparatus in the plant secretory pathway, directing traffic to and from such diverse organelles as the endoplasmic reticulum (ER), lytic and storage vacuoles, and the plasma membrane. More recently, the Golgi apparatus has been implicated in the transport of proteins to ‘non-conventional’ secretory organelles, such as peroxisomes and chloroplasts. In this review, we discuss recent findings in plants that contribute to our understanding of the efficient trafficking between the ER and Golgi, and beyond. Protein transport between ER and Golgi The first step in the transport of proteins through the secretory pathway is generally the transfer from the ER to the Golgi apparatus (reviewed by [1]). This occurs by means of a coat protein complex II (COPII)-mediated mechanism at specialized areas known as ER export sites (ERES), from which anterograde transport to the Golgi apparatus is thought to occur [2–4]. COPII is composed of three cytosolic components: the small GTPase Sar1 www.sciencedirect.com Is the Golgi apparatus a sub-compartment of the ER? As in mammalian and yeast systems, the plant Golgi apparatus receives exported proteins from the ER via ERES. However, questions regarding the association of ERES and the Golgi apparatus in plants have been raised. It appears that ERES and Golgi bodies have a continuous association in tobacco leaf epidermal cells [2,4]; whereas in tobacco BY-2 (Bright Yellow-2) suspension cells, multiple ERES can associate transiently with a single Golgi stack [3]. It is not clear whether these variations are due solely to the differences in the expression systems or rather to the use of different ERES markers. A fluorescent fusion of the Arabidopsis Sec24 COPII component has been localized to the peri-Golgi area in tobacco leaf epidermal cells [2]. This fusion has a similar distribution in Arabidopsis leaf epidermal cells (LA Matheson, F Brandizzi, unpublished; Figure 2), supporting the evidence that ERES track in close proximity with Golgi bodies in leaves (Figure 2b; [2]). Although a physical link between the ER and Golgi apparatus cannot be defined Current Opinion in Plant Biology 2006, 9:601–609 602 Cell biology Figure 1 Protein motifs that are important for anterograde and retrograde cargo recognition in plant cells. In anterograde transport, (a) di-acidic motifs are important for forward transport of multi-spanning, type I and type II membrane proteins out of the ER, as shown by ER export studies with Golgi and ER-resident membrane proteins [5]. The involvement of (b) a dibasic motif has been demonstrated in the ER export of a type II membrane-spanning prolyl hydroxylase [7]. (c) A dihydrophobic signal in the cytosolic domain of a type I membrane-spanning p24 protein has been shown to interact with a COPII coat component, Sec23 in vitro, although this is only possible when a dilysine motif adjacent to the dihydrophobic motif is mutated [6]. It is thought that both signals cooperate to recruit the COPI coat, whereas only the dihydrophobic motif is able to interact with Sec23. (d) Anterograde ER–Golgi transport of soluble proteins is thought to occur solely through a passive bulk-flow mechanism [8] because no specific motif has been identified. (e) There is a possibility that as-yet-undiscovered signals within soluble proteins direct their anterograde transport. In retrograde transport, (f) transmembrane proteins are selected for transport from the Golgi to the ER by a dilysine motif at the carboxyl terminus of the cytosolic tail that interacts with components of the COPI coat [9,51]. (g) An additional motif for Golgi to ER transport was identified in FATTY ACID DESATURASE 2 (FAD2), which possesses a carboxy-terminal sequence that is enriched in aromatic residues and that is necessary for the ER retention of FAD2 [10]. (h) Retrograde Golgi–ER transport of soluble proteins is achieved by carboxy-terminal H/KDEL signals that are recognized by the receptor ER RETENTION DEFECTIVE 2 (ERD2) [52]. (i) Other signals might exist that direct the transport of soluble protein back to the ER from the Golgi. conclusively by light microscopy, these data suggest that the ER, ERES and Golgi apparatus in leaf epidermal cells could exist and migrate in a continuous fashion. This is supported by recent evidence showing that Golgi bodies move with, not over, the surface of the ER [12]. In fact, the Golgi apparatus in plants not only might be physically linked to the ER but also might be a specialized subcompartment of the ER formed through continuous membrane flow [4,13]. Additional evidence that the Golgi apparatus is a functional extension of the ER comes from data indicating that Golgi membrane integrity depends on active exchange of cargo between the Golgi and ER. Treatment of cells with the fungal metabolite brefeldin A (BFA), a known inhibitor of ARF1 activation, leads to redistribution of Golgi membrane proteins to the ER [2,14]. Similarly, when ER-toGolgi transport is inhibited by a dominant negative mutant Current Opinion in Plant Biology 2006, 9:601–609 of ARF1 that is impaired in GTP/GDP exchange, Golgi membrane proteins are absorbed into the ER and the punctate distribution of Sec23 and Sec24, as well as that of Sar1, at the ERES is lost [2,4]. The first described function of ARF proteins in protein transport was to facilitate the formation of COPI-coated vesicles on the cis-Golgi. Although studies in plant cells are behind those in other systems, plant homologs of b- and gCOP have been shown to co-localize with ARF1 at the plant Golgi apparatus, indicating the possibility of a direct interaction [15]. Studies in tobacco epidermal cells confirmed that ARF1 and e-COP are dynamically associated with the Golgi apparatus. These studies also suggested that the different cycling rates of ARF1 and coatomer on and off the Golgi membranes might be essential to generate a functional COPI domain (Figure 3; [4]). Furthermore, they showed that active COPI-mediated transport is necessary www.sciencedirect.com Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 603 Figure 2 ER export sites in Arabidopsis leaf epidermal cells. (a–d) Confocal images of Arabidopsis leaf epidermal cells expressing either (a) the ER export site marker YFP–Sec24 alone, or (b) YFP–Sec24 with (c) a Golgi marker, ERD2-green fluorescent protein (GFP). (d) Merged image of (b) and (c). YFP–Sec24 localizes at punctate structures (arrowheads) when it is expressed alone or in combination with a Golgi marker [4]. Scale bar represents 10 mm. (e–g) Time-lapse of a cell co-expressing YFP–Sec24 and ERD2–GFP presented in vertical display as a single channel for (e) ERD2–GFP, (f) YFP-Sec24 and (g) as merged images. The arrowhead indicates an ERES that is moving with a Golgi stack. Time is shown in seconds at the top right of each image. Scale bar represents 5 mm. for the maintenance of ERES integrity. This implies that the distribution of Golgi membrane protein is maintained by the balanced action of COPI and COPII transport routes between the ER and Golgi, lending support to the hypothesis that the Golgi apparatus is a sub-compartment of the ER that is dependent on secretion [13]. The ARF1–coatomer complex is most likely indirectly required for anterograde trafficking out of the ER because of its role in recycling components that are essential for differentiation of the ER export domains [4]. However, this remains to be proven experimentally in plants. The Golgi apparatus is continuously remodelled Organelles are typically distinguished from one another by their enzymatic content, which is specified by cellular www.sciencedirect.com function. However, the boundaries between the ER and Golgi are unclear. These organelles undergo continuous exchange of material, and so the existence of each emerges as a product of dynamically controlled membrane trafficking and sorting processes. To maintain Golgi apparatus integrity, cells must manage complex membrane trafficking to and from the ER and maintain secretory membrane flow through the stack. Recent studies have provided evidence of constant remodeling of both the membranous and soluble components of the Golgi apparatus (Figure 3). Using fluorescence recovery after photobleaching (FRAP) techniques, it has been shown that e-COP, a subunit of coatomer, associates transiently with the Golgi membranes (Figure 3; [4]). In addition, Golgi membrane proteins continuously cycle between ER and Golgi, as demonstrated by photobleaching experiments using Current Opinion in Plant Biology 2006, 9:601–609 604 Cell biology Figure 3 Localization and dynamics of different classes of Golgi components. Fluorescence recovery after photobleaching (FRAP) experiments show that peripheral and integral membrane components of the Golgi apparatus, such as eCOP, full length GRIP (FLGRIP) and ERD2, continuously cycle on and off Golgi membranes. (a) Schematic representation of Golgi-localized peripheral (eCOP and FLGRIP) or integral membrane (ERD2) proteins. It should be noted that the predicted number of membrane-spanning domains and membrane orientation of ERD2 in plants remain to be confirmed experimentally. (b) The pre-bleach image shows tobacco epidermal cells expressing the YFP chimeras before the bleaching event. Golgi stacks (arrow) were photobleached, and the recovery of fluorescence to the area was monitored. Images at representative time points post-bleach (t1/2 and full recovery) are shown. Time of acquisition post-bleach is shown at the bottom left of each frame. The cytosolic pools of eCOP– YFP and YFP–FLGRIP give a high level of background fluorescence, which is absent in cells expressing ERD2–YFP. Scale bars represent 2 mm. ER-RETENTION DEFECTIVE 2 (ERD2)–yellow fluorescent protein (YFP) (Figure 3) and Golgi enzymes that are distributed in different cisternae [16]. As evidence of the rapid cycling of various soluble and membrane components of the Golgi apparatus increases, the question remains as to how the Golgi apparatus manages to preserve Current Opinion in Plant Biology 2006, 9:601–609 a highly organized structure and whether this structure can be considered an entity unto itself. Golgins, a diverse family of Golgi-resident proteins, have been implicated in the formation of a matrix that might be responsible for the structure of the Golgi apparatus [17]. www.sciencedirect.com Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 605 Golgins have large coiled-coil domains and an ability to bind effector molecules, including activated GTP-binding proteins of the Ras-protein families [17]. Perhaps the best-characterized function of golgins in mammalian and yeast systems is their role in membrane-tethering events [17]. Models of Golgi structure and function derived from yeast and mammalian cells cannot be directly extrapolated to plant cells because of the innate differences between these cellular systems. However, these studies have provided a starting point in the search for possible factors that might contribute to the unique structure and motile nature of the Golgi apparatus in plants. The Arabidopsis genome encodes several homologs of mammalian and yeast peripheral and integral membrane golgins [18]. The first membrane-spanning plant golgin to be cloned and characterized was AtCASP (for CCAAT displacement protein alternatively spliced product), but its functions at the Golgi apparatus have yet to be explored [19]. Many peripheral golgins share a 40amino-acid carboxy-terminal GRIP domain (named for the first four mammalian proteins in which it was found: golgin-97, RanBP2a, Imh1p, and p230/golgin-245), which is sufficient for trans-Golgi targeting. Recently, fluorescent fusions of the GRIP domain of a peripheral Arabidopsis golgin (AtGRIP) and of the full-length AtGRIP were shown to localize at the Golgi apparatus, and to cycle continuously on and off the Golgi (Figure 3; [20–22]). The mechanism by which AtGRIP is recruited to the Golgi apparatus has also been elucidated, revealing a cellular role for the small GTPase ARL1 (ARF-like GTPase 1) [20,22]. Subsequent studies have provided experimental evidence that ARL1 localizes to the plant Golgi apparatus and that two key residues (F51 and Y81) are responsible for its role in recruiting the AtGRIP domain [22]. The function of GRIP at the plant Golgi apparatus, and further interactions between GTPases and golgins in plants, remains to be discovered. It is possible that these so-called matrix proteins have a role in stabilizing the stack by maintaining efficient vesicular traffic to, through and from the Golgi apparatus. Post-Golgi transport Transport beyond the Golgi apparatus can reach a variety of different locations in plant cells. These destinations include the lytic and protein storage vacuoles (PSV), to which cargo molecules are transported by established routes (reviewed by [23,24]). New data continually increase our knowledge of these routes, particularly with regard to receptor trafficking [25,26,27,28]. It has been shown that ARF1 is involved in the transport of proteins to the lytic vacuole, in addition to its role in COPI-mediated transport [29]. A fluorescent fusion of ARF1 localizes to the Golgi apparatus as well as to additional punctate structures that detach from the Golgi apparatus [4,30]. The function of these structures has not yet been elucidated, but they might represent the trans-Golgi network (TGN) [4,31], endocytic www.sciencedirect.com compartments [30], or precursors of the prevacuolar compartment. Microscopy supports the existence of a TGNlike structure at the plant Golgi [31,32]. Earlier studies have also pointed to the existence of subdomains of the TGN [33]. The golgin AtGRIP is thought to localize at the transGolgi, although its localization at the TGN has not been excluded [20]. It has yet to be shown whether disrupting the correct targeting of AtGRIP to the Golgi by mutating essential residues (i.e. Y717 or K719; [22]) can affect the integrity of the plant TGN or its subdomains, as has been demonstrated in mammalian cells [34,35]. Recent studies have shown that the Golgi apparatus plays a role in transporting some proteins to the chloroplast [36,37], although import routes directly from the cytosol are better characterized and might be more numerous (reviewed by [38]). Similar Golgi-mediated pathways have yet to be established for mitochondrial proteins. The early secretory pathway has also been implicated in protein transport to peroxisomes, although it is not clear whether the Golgi apparatus is involved. Again, cytosolic import pathways into peroxisomes have been identified for several proteins [39,40], but the ER also appears to play a prominent role in the transport of proteins into peroxisomes. It appears that several peroxisomal proteins accumulate in subdomains of the ER [41–43], although it is not clear whether these proteins are en route to the peroxisome or whether they contain specific signals that mediate dual targeting to the peroxisome and ER. This phenomenon has been observed for a protein disulphide isomerase in the green alga Chlamydomonas reinhardtii, which is targeted to the chloroplast and ER [44]. Similar mechanisms could exist in higher plants, possibly allowing dual targeting to different combinations of organelles. A transport route from the peroxisome to the ER has also been identified [45], indicating the potential for protein cycling between the two organelles. No evidence has yet been presented to implicate the Golgi apparatus in ERto-peroxisome transport, suggesting that proteins might be transported from ER to peroxisomes independently of the Golgi apparatus. Similar Golgi-independent routes have been suggested for the transport of storage proteins to the PSV [46,47] and might exist between the ER and other organelles, although this has yet to be shown. Conclusions and future perspectives Recent studies have resulted in a marked increase in our understanding of the structure and functions of the Golgi apparatus in plants. However, there are many questions to be answered (Figure 4). An increased understanding of the functions and interactions of golgins and ARF proteins might provide new insight into the structure and function of the Golgi apparatus, cargo transport, the relationship between the Golgi stack and the ER, and the unique patterns of movement displayed by individual Golgi stacks. For example, the cycling of the GTPase ARF1 between the GDP-bound form in the cytosol and Current Opinion in Plant Biology 2006, 9:601–609 606 Cell biology Figure 4 Summary of the established and unidentified transport routes within the early secretory pathway in plants. Because of the unique nature of the early secretory pathway in plants, many questions remain under investigation. They are divided into four main categories, represented in the diagram by the four colored letters. (a) ER to Golgi communication: the relationship between ERES and Golgi bodies is the subject of an ongoing debate because distinct theories on the dynamics of transport have been presented on the basis of studies in different model systems [2,3]. Recent data have suggested that Golgi bodies move with the ER — at the same rate and in the same direction [12] — and the secretory unit model has proposed a continuum between the ER, ERES and the Golgi apparatus [2]. If the ER and Golgi are physically linked, can the Golgi be considered a unique entity? The possibility exists that the Golgi apparatus might be a specialized sub-compartment of the ER that is dependent on secretion. (b) Cargo export: ER to Golgi transport is mediated by COPII, although the nature of the transport intermediates is unclear. How do COPII components interact with membrane protein motifs to initiate transport? Are there specific signals for the anterograde transport of soluble proteins or is it mediated solely by bulk-flow? Retrograde transport is thought to be controlled by COPI, as it is in mammalian and yeast systems, although this has yet to be shown directly in plants. There are several unidentified potential transport routes, including Golgi–mitochondria, Golgi–peroxisome, ER–lytic vacuole and ER–peroxisome routes. (c) Structure and organization: how do the ER and Golgi apparatus interact yet maintain specific organelle identities? Two plant golgins have been identified and characterized [19–22]. Do other golgins exist in plants and what functional role do they play within the Golgi apparatus? Does ARF1 have an additional functional role at the level of structural organization of Current Opinion in Plant Biology 2006, 9:601–609 www.sciencedirect.com Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 607 the GTP-bound form on the Golgi membranes has been observed in living cells [4]. It is not clear how ARF1 is specifically recruited to Golgi membranes. It is possible that Golgi-associated guanine nucleotide exchange factors (GEFs) recruit ARF1 to the Golgi membrane; however, evidence from mammalian cells suggests that other membrane proteins such as SNAREs (soluble N-ethylmaleimide-sensitive factor attachment protein receptors) could serve indirectly as ARF1 receptors [48]. It could also be that membrane-bound golgins, such as CASP, recruit ARF1 to the Golgi apparatus. On a larger scale, questions can be raised regarding the number of Golgi bodies in plant cells. The Golgi apparatus in plants exists as individual stacks that double in number during cell division [49], but the mechanisms for this have not yet been identified. Does this increase in the number of Golgi bodies occur as a result of the division of existing Golgi stacks or are they synthesized de novo from ER membranes? A sterol regulatory element binding protein (SREBP)-based mechanism has been described in mammals that links endomembranes and gene transcription: translocation of a regulatory protein to the nucleus via the Golgi results in the activation of a target gene [50]. It is possible that a similar system might operate in plants, allowing the coordination of a nuclear response with the activity of the early secretory pathway. Finally, we pose the question as to whether the Golgi is a necessary organelle in the plant cell. The existence of multiple Golgi-independent protein transport pathways that originate in the ER and traffic cargo molecules to a variety of destinations indicates that the Golgi, although important to the secretory pathway, might not be as vital to the whole cell, at least in the short-term. This hypothesis is supported by the fact that BFA-mediated disruption of the Golgi apparatus does not result in immediate cell death, and that removal of the drug can allow regeneration of functional Golgi bodies [14]. The question remains: is the Golgi an essential part of the cell that mediates many varied processes or is it a dispensable subdomain of the ER, without which the cell can survive for extended periods of time? Our perception of the Golgi apparatus has been modified considerably because of recent findings that have proposed additional functions for this intriguing organelle. This trend is likely to continue as the field endeavors to resolve the myriad of unanswered questions. Acknowledgements We apologize to colleagues whose work could only be covered by reference to reviews and discussion in other papers because of space limitations. This work was supported by the Canada Research Chair Program and the Natural Science and Engineering Research Council of Canada and the Department of Energy, Michigan State University. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest 1. Hanton SL, Matheson LA, Brandizzi F: Seeking a way out: export of proteins from the plant endoplasmic reticulum. Trends Plant Sci 2006, 11:335-343. 2. daSilva LL, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F: Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 2004, 16:1753-1771. 3. Yang YD, Elamawi R, Bubeck J, Pepperkok R, Ritzenthaler C, Robinson DG: Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotiana tabacum BY-2 cells provides evidence for transient association of Golgi stacks with endoplasmic reticulum exit sites. Plant Cell 2005, 17:1513-1531. 4. Stefano G, Renna L, Chatre L, Hanton SL, Moreau P, Hawes C, Brandizzi F: In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J 2006, 46:95-110. 5. Hanton SL, Renna L, Bortolotti LE, Chatre L, Stefano G, Brandizzi F: Diacidic motifs influence the export of transmembrane proteins from the endoplasmic reticulum in plant cells. Plant Cell 2005, 17:3081-3093. Diacidic motifs are shown to perform a significant function in the export of multispanning, type II and type I membrane proteins to the Golgi apparatus. The findings described in this paper indicate that diacidic ER export motifs are dominant over transmembrane domain length in determining the export of proteins from the ER. 6. Contreras I, Yang Y, Robinson DG, Aniento F: Sorting signals in the cytosolic tail of plant p24 proteins involved in the interaction with the COPII coat. Plant Cell Physiol 2004, 45:1779-1786. 7. Yuasa K, Toyooka K, Fukuda H, Matsuoka K: Membraneanchored prolyl hydroxylase with an export signal from the endoplasmic reticulum. Plant J 2005, 41:81-94. The authors cloned a novel prolyl 4-hydroxylase, a type II integral membrane protein, from tobacco BY-2 cells. Their results indicated that basic amino acids in the amino-terminal cytoplasmic region of the protein play a role in its export from the ER. Its membrane-anchored nature is plant-specific, as integral membrane prolyl hydroxylases have not been found in other systems. 8. Phillipson BA, Pimpl P, daSilva LL, Crofts AJ, Taylor JP, Movafeghi A, Robinson DG, Denecke J: Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell 2001, 13:2005-2020. 9. Contreras I, Ortiz-Zapater E, Aniento F: Sorting signals in the cytosolic tail of membrane proteins involved in the interaction with plant ARF1 and coatomer. Plant J 2004, 38:685-698. 10. McCartney AW, Dyer JM, Dhanoa PK, Kim PK, Andrews DW, McNew JA, Mullen RT: Membrane-bound fatty acid desaturases are inserted co-translationally into the ER and contain different ER retrieval motifs at their carboxy termini. Plant J 2004, 37:156-173. 11. Hanton SL, Bortolotti LE, Renna L, Stefano G, Brandizzi F: Crossing the divide — transport between the endoplasmic reticulum and Golgi apparatus in plants. Traffic 2005, 6:267-277. 12. Runions J, Brach T, Kuhner S, Hawes C: Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 2006, 57:43-50. (Figur 4 Legend Continued ) the Golgi apparatus? It has been suggested that ARF1 might be involved in recruiting components that are involved in the Golgi matrix in mammalian cells [48]. Does ARF1 behave in a similar fashion in plant cells? How is ARF1 recruited to the Golgi apparatus? What is the role of the ARF1 structures that detach from the Golgi apparatus [4]? (d) Feedback mechanism: is there a relationship between secretory activity and ER/Golgi morphology? If such a relationship exists, is there a feedback mechanism that allows the coordination of a response?. www.sciencedirect.com Current Opinion in Plant Biology 2006, 9:601–609 608 Cell biology The authors studied protein flow within the membrane of the ER as it is continuously remodelled. Their results suggest that the ER moves actively over an actin scaffold. Tracking of Golgi movement demonstrated that individual stacks move at the same rate and in the same direction as ERresident proteins, supporting the concept of a continuum between the ER, ERES and the Golgi apparatus. This paper demonstrates that both the transmembrane domain and the cytosolic tail of the plant vacuolar sorting receptor play a role in proper vacuolar targeting, indicating that multiple sequence motifs are necessary for its proper function. The mechanism of ER export of BP80, as well as the Golgi to prevacuolar compartment transport and recycling of this protein, is described. 13. Hawes C, Satiat-Jeunemaitre B: The plant Golgi apparatus — going with the flow. Biochim Biophys Acta 2005, 1744:465-480. 28. Jolliffe NA, Brown JC, Neumann U, Vicre M, Bachi A, Hawes C, Ceriotti A, Roberts LM, Frigerio L: Transport of ricin and 2S albumin precursors to the storage vacuoles of Ricinus communis endosperm involves the Golgi and VSR-like receptors. Plant J 2004, 39:821-833. 14. Ritzenthaler C, Nebenführ A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG: Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 2002, 14:237-261. 15. Couchy I, Bolte S, Crosnier MT, Brown S, Satiat-Jeunemaitre B: Identification and localization of a b-COP-like protein involved in the morphodynamics of the plant Golgi apparatus. J Exp Bot 2003, 54:2053-2063. 16. Brandizzi F, Snapp EL, Roberts AG, Lippincott-Schwartz J, Hawes C: Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 2002, 14:1293-1309. 17. Short B, Haas A, Barr FA: Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim Biophys Acta 2005, 1744:383-395. 18. Latijnhouwers M, Hawes C, Carvalho C: Holding it all together? Candidate proteins for the plant Golgi matrix. Curr Opin Plant Biol 2005, 8:632-639. This review discusses the current understanding of the golgin family of proteins in the context of a Golgi matrix. A comparison between plants and other systems attempts to identify putative plant homologues of candidate matrix proteins. This provides a starting point for further analyses of the structure and organization of the plant Golgi apparatus. 19. Renna L, Hanton SL, Stefano G, Bortolotti L, Misra V, Brandizzi F: Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol Biol 2005, 58:109-122. 20. Latijnhouwers M, Hawes C, Carvalho C, Oparka K, Gillingham AK, Boevink P: An Arabidopsis GRIP domain protein locates to the trans-Golgi and binds the small GTPase ARL1. Plant J2005, 44:459-470. 21. Gilson PR, Vergara CE, Kjer-Nielsen L, Teasdale RD, Bacic A, Gleeson PA: Identification of a Golgi-localised GRIP domain protein from Arabidopsis thaliana. Planta 2004, 219:1050-1056. 22. Stefano G, Renna L, Hanton S, Chatre L, Haas TA, Brandizzi F: ARL1 plays a role in the binding of the GRIP domain of a peripheral matrix protein to the Golgi apparatus in plant cells. Plant Mol Biol 2006, 61:431-449. 23. Jürgens G: Membrane trafficking in plants. Annu Rev Cell Dev Biol 2004, 20:481-504. 29. Pimpl P, Hanton SL, Taylor JP, Pinto-DaSilva LL, Denecke J: The GTPase ARF1p controls the sequence-specific vacuolar sorting route to the lytic vacuole. Plant Cell 2003, 15:1242-1256. 30. Xu J, Scheres B: Dissection of Arabidopsis ADPRIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 2005, 17:525-536. 31. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH: Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 2004, 29:49-65. 32. Saint-Jore-Dupas C, Gomord V, Paris N: Protein localization in the plant Golgi apparatus and the trans-Golgi network. Cell Mol Life Sci 2004, 61:159-171. 33. Bassham DC, Sanderfoot AA, Kovaleva V, Zheng H, Raikhel NV: AtVPS45 complex formation at the trans-Golgi network. Mol Biol Cell 2000, 11:2251-2265. 34. Yoshino A, Bieler BM, Harper DC, Cowan DA, Sutterwala S, Gay DM, Cole NB, McCaffery JM, Marks MS: A role for GRIP domain proteins and/or their ligands in structure and function of the trans Golgi network. J Cell Sci 2003, 116:4441-4454. 35. Derby MC, van Vliet C, Brown D, Luke MR, Lu L, Hong W, Stow JL, Gleeson PA: Mammalian GRIP domain proteins differ in their membrane binding properties and are recruited to distinct domains of the TGN. J Cell Sci 2004, 117:5865-5874. 36. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N et al.: Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 2005, 7:1124-1131. 37. Chen MH, Huang LF, Li HM, Chen YR, Yu SM: Signal peptidedependent targeting of a rice a-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol 2004, 135:1367-1377. 38. Gutensohn M, Fan E, Frielingsdorf S, Hanner P, Hou B, Hust B, Klosgen RB: Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J Plant Physiol 2006, 163:333-347. 39. Baker A, Sparkes IA: Peroxisome protein import: some answers, more questions. Curr Opin Plant Biol 2005, 8:640-647. 24. Robinson DG, Oliviusson P, Hinz G: Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic 2005, 6:615-625. 40. Sparkes IA, Hawes C, Baker A: AtPEX2 and AtPEX10 are targeted to peroxisomes independently of known endoplasmic reticulum trafficking routes. Plant Physiol 2005, 139:690-700. 25. daSilva LL, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J: Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 2005, 17:132-148. 41. Flynn CR, Heinze M, Schumann U, Gietl C, Trelease RN: Compartmentalization of the plant peroxin, AtPex10p, within subdomain(s) of ER. Plant Sci 2005, 168:635-652. 26. Oliviusson P, Heinzerling O, Hillmer S, Hinz G, Tse YC, Jiang L, Robinson DG: Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 2006, 18:1239-1252. The authors identified a membrane-binding retromer-like protein complex in plants, which is localized to the prevacuolar compartment. The data presented in this paper suggest that cargo transport to the lytic compartment, and receptor cycling between the trans-Golgi network and the endosomal/prevacuolar compartments, is strongly conserved among eukaryotes. 27. daSilva LLP, Foresti O, Denecke J: Targeting of the plant vacuolar sorting receptor BP80 is dependent on multiple sorting signals in the cytosolic tail. Plant Cell 2006, 18:1477-1497. Current Opinion in Plant Biology 2006, 9:601–609 42. Karnik SK, Trelease RN: Arabidopsis peroxin 16 coexists at steady state in peroxisomes and endoplasmic reticulum. Plant Physiol 2005, 138:1967-1981. 43. Lisenbee CS, Heinze M, Trelease RN: Peroxisomal ascorbate peroxidase resides within a subdomain of rough endoplasmic reticulum in wild-type Arabidopsis cells. Plant Physiol 2003, 132:870-882. 44. Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I, Danon A: Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc Natl Acad Sci USA 2005, 102:6225-6230. 45. McCartney AW, Greenwood JS, Fabian MR, White KA, Mullen RT: Localization of the tomato bushy stunt virus replication www.sciencedirect.com Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 609 protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 2005, 17:3513-3531. 46. Takahashi H, Saito Y, Kitagawa T, Morita S, Masumura T, Tanaka K: A novel vesicle derived directly from endoplasmic reticulum is involved in the transport of vacuolar storage proteins in rice endosperm. Plant Cell Physiol 2005, 46:245-249. 47. Oufattole M, Park JH, Poxleitner M, Jiang L, Rogers JC: Selective membrane protein internalization accompanies movement from the endoplasmic reticulum to the protein storage vacuole pathway in Arabidopsis. Plant Cell 2005, 17:3066-3080. 48. Donaldson JG, Honda A, Weigert R: Multiple activities for Arf1 at the Golgi complex. Biochim Biophys Acta 2005, 1744:364-373. 49. Segui-Simarro JM, Staehelin LA: Cell cycle-dependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: a quantitative and spatial analysis. Planta 2006, 223:223-236. 50. Espenshade PJ: SREBPs: sterol-regulated transcription factors. J Cell Sci 2006, 119:973-976. 51. Benghezal M, Wasteneys GO, Jones DA: The C-terminal dilysine motif confers endoplasmic reticulum localization to type I membrane proteins in plants. Plant Cell 2000, 12:1179-1201. 52. Denecke J, De Rycke R, Botterman J: Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J 1992, 11:23452355. Five things you might not know about Elsevier 1. Elsevier is a founder member of the WHO’s HINARI and AGORA initiatives, which enable the world’s poorest countries to gain free access to scientific literature. 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