The structure and function of the Golgi apparatus: a hundred years of questions

Journal of Experimental Botany, Aug 1998

Over the last century, the Golgi apparatus has attracted the attention of researchers world-wide. This highly variable and polymorphic organelle plays a central role in intracellular membrane traffic. Not only does it receive all the secretory material and membrane synthesized by the endoplasmic reticulum and modifies these products by glycosylation, but also packages them and sends them in vesicular carriers to their correct destinations. It is also capable of the synthesis of complex polysaccharides used for building cell walls, a feature unique for higher plants. Yet, the current models of Golgi function are based on those established for yeast and mammalian cells and may not be completely relevant to plants. This review is an attempt to summarize the current knowledge of the plant Golgi apparatus and, where possible, to discuss the applicability of the current models of Golgi function to the plant cell.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

The structure and function of the Golgi apparatus: a hundred years of questions

Journal of Experimental Botany The structure and function of the Golgi apparatus: a hundred years of questions Alexandra V. Andreeva 0 Mikhail A. Kutuzov 0 David E. Evans 0 Chris R. Hawes 0 0 Research School of Biological and Molecular Sciences, Oxford Brookes University , Gipsy Lane Campus, Headington, Oxford OX3 0BP , UK Over the last century, the Golgi apparatus has attracted the attention of researchers world-wide. This highly variable and polymorphic organelle plays a central role in intracellular membrane traffic. Not only does it receive all the secretory material and membrane synthesized by the endoplasmic reticulum and modifies these products by glycosylation, but also packages them and sends them in vesicular carriers to their correct destinations. It is also capable of the synthesis of complex polysaccharides used for building cell walls, a feature unique for higher plants. Yet, the current models of Golgi function are based on those established for yeast and mammalian cells and may not be completely relevant to plants. This review is an attempt to summarize the current knowledge of the plant Golgi apparatus and, where possible, to discuss the applicability of the current models of Golgi function to the plant cell. Golgi apparatus; intracellular membrane traffic; secretion; vesicles Introduction One hundred years of analysis Over the decades, the Golgi apparatus (GA) has been one of the most controversial of the cellular organelles ( Whaley, 1975) . Elaboration of a detailed model of GA functioning has proved diYcult because of the extremely high diversity of the organelle, including its morphology, position in the cell, intensity of its activity, and the nature of its products. The GA was apparently discovered by La Valette St George ( 1865 , 1867). However, his descriptions show that the techniques he employed probably did not allow a clear visualization of the organelle. The breakthrough was made when Camillo Golgi invented a method which allowed him to visualize an apparato reticolare interno in a sharp contrast with other cellular components, and demonstrated that this organelle was a component of a wide variety of cells from diVerent tissues (Golgi, 1898) . In the late 1920s, Bowen addressed the presence of the GA in plant cells and concluded that they do contain this organelle (Bowen 1926, 1928) . The plant GA, however, received little attention until the late 1950s when it was demonstrated in cells from a number of mono- and dicotyledons, as well as several cryptogams. However, only in the early 1960s was the GA widely accepted as an organelle of plant cells due to a number of works using the newly developed techniques of electron microscopy. Yet only during the past decade, that is about a century after Golgi’s discovery, has significant knowledge been acquired of its molecular organization. A detailed historical review on the discovery and investigation of the GA has recently appeared (Berger, 1997 ). State of the methodology The development of new cryofixation methods, such as ultra-rapid freeze-fixation combined with freezesubstitution or deep-etch replication techniques has greatly improved the quality of cellular structural preservation ( Hawes and Martin, 1986; Meindl et al., 1992) . Combined with the increasing use of immunocytochemistry to locate both structural components and the products of the GA (Staehelin and Moore, 1995; Satiat-Jeunemaitre and Hawes, 1992; Zhang and Staehelin, 1992 ) , these methods are providing more accurate information on the morphology and dynamics of this central organelle of the secretory pathway ( Figs 1–3). More recently, techniques that permit the in vivo study of Golgi activity using green fluorescent protein tagged marker proteins are starting to reveal new aspects of protein flow through the mammalian secretory pathway ( Presley et al., 1997; Scales et al., 1997) . It should be expected that such technology will soon be successfully applied to plant secretory systems. A paper reporting targeting of the green fluorescent protein to the plant Golgi has recently been accepted for publication (Boevink et al., 1998 ). Isolation of the GA presents some formidable technical diYculties ( Whaley, 1975) . However, a combination of protein characterization by mass spectrometry after separation on 2D gels with the analysis of sequence databases avoids some of the problems associated with GA purification and will permit the identification of marker Golgi proteins (as described by P Dupree; html ). Molecular cloning has revealed the structure of many Golgi proteins in yeast and mammals. Homologues of some of them have been identified in plants (mainly in Arabidopsis thaliana), suggesting that the basic principles and organization of molecular machinery for vesicle traYcking are likely to be similar in mammals, yeast and plants. The availability of a large number of plant cDNA/ genomic sequences in the public databases (Newman et al., 1994; Cooke et al., 1996 ) now facilitates further identification of the plant homologues of mammalian and yeast proteins by database searching. However, the number of proteins identified in plants participating in intracellular membrane traYc is not yet suYcient to determine the extent to which transport mechanisms are conserved. In addition, the plant Golgi is likely to possess specific proteins (for example, regulatory ones, such as participating in hormone perception and signal transduction), and they may escape identification by approaches based on homology searches and yeast complementation screens. A number of pharmacological agents have also proved to be useful in studying the plant GA, such as monensin (which has various moderately specific eVects on GA function; Zhang et al., 1996 ) , cyclopiazonic acid (an inhibitor of Ca2+-ATPases; Ho¨ ftberger et al., 1995) and brefeldin A (a fungal toxin with a poorly understood mechanism of action; Satiat-Jeunemaitre et al., 1996; Staehelin and Driouich, 1997 ) . Spatial organization Why does a cell need a Golgi apparatus? Prokaryotes have no GA and use the prokaryote-specific sec system and signal recognition particle-dependent translocation mechanism, situated on the plasma membrane, to secrete proteins (Schekman, 1994; Wolin, 1994 ) . Eukaryotes, on the other hand, have a complex intracellular traYc system in which the GA plays a central role. The presence of GA in eukaryotic cells permits a higher level of sorting, modification and targeting of secreted materials commensurate with complex subcellular compartmentalization and with the diversity of functions of cells and tissues in multicellular organisms. An hypothesis for the origin of GA has been presented by Becker and Melkonian (1996) . In most prokaryotes, biosynthesis of membrane proteins and lipids, as well as attachment of the single chromosome, are associated with the plasma membrane. In eukaryotes, these are functions of the ER/nuclear envelope, which is postulated to have arisen by invagination of a specialized part of the plasma membrane. Loss of continuity between the ER/nuclear envelope and the plasma membrane required a transfer system between the two compartments which resulted in the evolution of a GA. Interestingly, the lipid composition of the ER membrane resembles that of a prokaryotic plasma membrane (Becker and Melkonian, 1996 ) . The diversity and complexity of form and function of GA are then suggested to result from the optimization of this basic system. Stacks and cisternae GA architecture has been described in most detail for a limited number of particular systems such as algae ( Becker and Melkonian, 1996) and secreting root cap cells (Mollenhauer and Morre´, 1994); detailed comparison between polysaccharide- and protein-secreting cells can also be found in the literature (Juniper et al., 1982) . Golgi stacks are polarized structures, i.e. the morphology of cisternae and enzymatic activities change gradually from the cis to the trans face: the cisternal width decreases, while the intercisternal width, the density of intercisternal elements and polysaccharide content increase in a cis to trans direction ( Robinson and Kristen, 1982) . The extent of this polarization is cell type-specific (Staehelin et al., 1990) . The mechanisms which shape the GA architecture are not known. Although the basic morphological features of GA are qualitatively similar, various species and cells may be characterized by the diVerent number of Golgi stacks per cell, from one in Chlamydomonas to several hundreds in maize root cap cells or even thousands in giant fibre cells in cotton ( Walne, 1967; Mollenhauer and Morre´, 1994; Driouich and Staehelin, 1997 ) . The number of cisternae per stack can also vary significantly, from 5–7 in the root cap cells (Mollenhauer and Morre´, 1994) to approximately 30 in Euglena (Becker and Melkonian, 1996) . The number of cisternae in a stack and/or the number of stacks per cell can also change depending on the physiological conditions ( Iijima and Kono, 1992 ), on the stage of development, or on the changes in cellular function. Thus, in the cells of maize root cap, the onset of the intense secretory phase is preceded by a considerable increase in the number and the size of Golgi stacks (Mollenhauer, 1965a) . These cells are specialized and not programmed to undergo further mitosis; therefore, the changes in Golgi morphology in this case are likely to be controlled by the functional needs of the cell. Similar observations have been made for meristematic cells undergoing diVerentiation into root cap cells in Nicotiana and Arabidopsis (Staehelin et al., 1990), and also for the slimesecreting Drosophyllum cells, where the number of stacks per cell increases with the gland maturation (Schnepf and Bush, 1976 ) . An earlier work suggested that, in general, the number of cisternae per stack decreases with increasing secretory activity (Schnepf, 1969) . It has also been demonstrated that Golgi stack productivity can vary between growing cells and non-growing secreting cells. Thus, in terms of area of vesicle membrane produced, pollen tip Golgi produce approximately five times more membrane per unit area of cisternum than do the Golgi of a heavily secreting maize root cap cells which produces fewer larger product filled vesicles (Steer and O’Driscoll, 1991 ) . Some observations indicate that Golgi architecture may also be controlled by genetically determined developmental programmes. In colchicinetreated Chlamydomonas, the number of Golgi stacks (which is normally one per cell ) increases proportionally to the number of genomic copies and decreases with the recovery of the cells ( Walne, 1967 ). In mammalian cells, Golgi stacks are connected by tubules (Mollenhauer and Morre´, 1994; Cole et al., 1996 ) , and lateral diVusion of lipids and of chimaeric GFPcontaining proteins has been observed between Golgi stacks in vivo (Cole et al., 1996). At least in some cases, tubular networks associated with the Golgi and clearly distinct from the ER have been demonstrated in plant cells (Mollenhauer and Morre´, 1994; Harris and Oparka, 1983 ) . Harris and Oparka (1983 ) have described tubular interconnections between the GA and ER in mung bean cotyledons, which may link ER directly not only to the cis, but also to the trans face. Whether this tubular network may connect Golgi stacks with each other, is not firmly established. Since, in plants, diVerent stacks are dispersed through the cytoplasm either as single units or as small clusters, plant Golgi stacks are generally considered as functionally independent (Staehelin and Moore, 1995 ). Integrity of Golgi stacks DiVerent cisternae of the same Golgi stack are interconnected by filaments of unknown nature spaced regularly along adjacent cisternae (reviewed by Barr and Warren, 1996 ) . In plant cells, intercisternal elements were discovered in maize root cells by Mollenhauer (1965b) and in Nitella by Turner and Whaley ( 1965 ). According to Staehelin et al. ( 1990), they are present only between trans cisternae of cells which are or will be actively involved in slime synthesis, but not in the meristematic cells. These elements are also observed in some ( but not all ) suspension-cultured cells (Driouich et al., 1994 ) . In early works, the intercisternal elements were suggested to be necessary for maintenance of the flattened shape of the cisternae, but not for their stacking ( Kristen, 1978, and references therein) . However, at least in animal cells, proteolysis of intercisternal elements is paralleled by unstacking of Golgi cisternae (Cluett and Brown, 1992) . Intracisternal elements have also been reported ( Franke et al., 1972) . Several candidate structural components of intercisternal elements have been proposed (discussed by Barr and Warren, 1996 ) including (i) oligomers of the oligosaccharide processing enzymes (which can also play a role in the retention of these enzymes in the GA, see below); (ii) a family of GA proteins identified as autoantigens in some autoimmune diseases (giantin, golgin and several other related proteins which are thought to contain regions of coiled-coil similar to the rod domain of myosin), and (iii) cytoskeleton proteins (spectrin, ankyrin, comitin). Plant proteins related to golgin and giantin can be detected by dbEST searching (Andreeva et al., unpublished observations), however their functions and intracellular localization are not known. Spectrin has been detected in Chlamydomonas ( Lorenz et al., 1995 ) and pea (Bisikirska and Sikorski, 1997 ) . Mobility of the Golgi apparatus While in mammalian cells Golgi stacks are localized in a juxtanuclear position, their position in plant cells generally seems irregular. However, at least in some situations, they apparently move to a location where their activity is needed. One example of such mobility is the organization of Golgi stacks near the growing cell plate at the end of mitosis. In mammalian cells, microtubules are essential for the maintenance of global GA architecture in the cell, but not of its stacked structure (Barr and Warren, 1996) . Depolymerization of microtubules (either in prophase or as a result of addition of depolymerizing agents such as nocodazole) leads to the dispersal of Golgi stacks throughout the cytoplasm (GriYng, 1991) , resulting in a phenotype similar to the situation in plant cells. Repolymerization of microtubules (either in telophase or upon removal of a depolymerizing agent) is followed by the relocation of Golgi stacks to the juxtanuclear region. In plant cells, microtubules appear not to play such a role, and their depolymerization has no eVect on the distribution of Golgi stacks. In plants, the spatial organization of the GA is likely to depend on actin and possibly actin-binding proteins, such as spectrin and myosin-like proteins (see above). This is supported by observations of aggregation and clustering of Golgi stacks in the presence of actindisrupting agents such as cytochalasin (Mollenhauer and Morre´, 1976; Satiat-Jeunemaitre et al., 1996 ) . Individual Golgi stacks can probably be carried by cytoplasmic streaming, and it seems reasonable to suggest that the surrounding actin filaments participate in providing co-ordination between them and the ER. Golgi apparatus in mitosis Following the depolymerization of microtubules and GA dispersion during prophase, the mammalian GA vesiculates by a complex mechanism involving continuous budding of COPI coated vesicles (60–65% of the GA membranes), as well as by a COPI-independent mechanism ( Misteli and Waren, 1995; Rabouille and Warren, 1997 ) . Then, by the late telophase, the Golgi vesicles fuse to reform cisternae. A subset of cytosolic factors (NSF, SNAPs, p115, and p97) that leads to reassembly of GA in mammalian cells has been identified. In order for the cisternae to stack, dephosphorylation of some components appears to be essential, since stacking is blocked by microcystin ( Rabouille and Warren, 1997), an inhibitor of protein phosphatases 1 and 2A. Although structural homologues of at least some of these mammalian Golgi reassembly factors are expressed in plant cells (Andreeva et al., 1998 ) , there is no evidence for any GA disassembly/reassembly at any stage of the plant cell cycle. An exception is the conversion of the GA to vesicular clusters during seed desiccation (Mollenhauer and Morre´, 1978) ; the mechanism of this vesiculation is unknown. The persistence of the Golgi stacks during mitosis in plant cells is probably due to necessity for a functional GA in anaphase, when the cell plate starts to form (Staehelin and Hepler, 1996 ) , while in animal cells the GA is not functional during mitosis. The question then to be asked is how and when does plant GA replicate? The process of GA division is best studied in some algae where the number of Golgi stacks is small. The data available for Micrasterias and Closterium (Noguchi, 1983, 1988 ) indicate that the number of cisternae per stack is the same before and after cytokinesis, while the diameter of the stacks approximately halves. In Closterium, Golgi stacks begin to divide synchronously (and at the same time as the chloroplast) at a premitotic stage, and duplicate in number before cytokinesis ( Ueda, 1997). Images of putatively dividing Golgi stacks have been reported by Craig and Staehelin ( 1988 ). In onion root meristems, it has been reported that the number of Golgi stacks increases approximately twice during mitosis, mainly between prophase and anaphase, and that this process appears to be controlled by the same mechanisms which control the onset of mitosis but not of cytokinesis (Garcia-Herdugo et al., 1988) . Many essential questions about GA replication remain unanswered. What is the membrane material used to restore the normal size of a stack after its division? Does it divide longitudinally or transversely and what does determine the exact site of scission? What are the molecular mechanisms of the division itself and of its regulation? Is the machinery of GA division in the plant cell similar to that involved in the disassembly/reassembly of the animal GA? Perhaps it is also pertinent to suggest that the possibility of de novo formation of Golgi from ER membranes should also be considered as a mechanism for increasing stack number. Function Plant GA as a ‘complex polysaccharide factory’ The plant GA serves two major functions: protein glycosylation and synthesis of cell wall polysaccharides (hemicellulose and pectins, but not cellulose). Polysaccharide synthesis in the GA, a unique feature of plant cells, was first demonstrated in 1966 by Northcote and PickettHeaps. To date, although some Golgi enzymes involved in this pathway have been identified, solubilized and partially characterized ( Hanna et al., 1991; BruyantVannier et al., 1996; Baydoun and Brett, 1997 ) , non of them have been purified, and no antibodies against them are available. A membrane-anchored endo-1,4-b-glucanase has been recently cloned from tomato, and one of its forms localized specifically in the Golgi membranes (Brummell et al., 1997); its function in the GA is, however, unknown. The cloning of a plant glycosyltransferase gene has yet to be published. Nevertheless, the availability of antibodies against polysaccharide products allowed the development of models of polysaccharide synthesis in the plant GA, at least for two main classes of polysaccharides synthesized by dicotyledons, namely polygalacturonic acid/rhamnogalacturonan I and xyloglucan (Driouich and Staehelin, 1997) . N- and O-glycosylation of proteins occur in the GA of both animal and plant cells. While the early steps of N-glycosylation are very similar in mammalian and plant GA, the terminal residues in plant N-glycans diVer: they contain a-1,3 fucose instead of a-1,6 fucose in mammals, b-1,2 xylose is found in plant glycans while N-acetylneuraminic acid is not ( Faye et al., 1992 ) . Composition of sugars used in O-glycans is also diVerent in plants and mammals and, in addition to Ser and Thr, hydroxyproline can be O-glycosylated in plants. This suggests that the plant GA contains specific sets of corresponding enzymes (Driouich and Staehelin, 1997) . Location of GA enzymes As stated above, the current views on location of the enzymes in plant GA are based mainly on indirect evidence obtained using antibodies against their substrates and products ( Hawes et al., 1996 ) . In some cases, location may be cell-type specific. A ‘classic’ example is location of polygalacturonic acid/rhamnogalacturonan I in the cisor medial- Golgi cisternae of cortical root tip cells ( Moore et al., 1991 ) , but mostly in trans-Golgi cisternae and the trans-Golgi network in slime secreting root cap cells (Lynch and Staehelin, 1992 ) . The principal questions to be answered in order to understand Golgi enzyme location are (i) which signals determine their position within the stack, and (ii) what are the mechanisms preventing their mislocalization and their leakage with the products. There is no significant sequence homology between various glycosidases and glycosyltransferases which might serve for recognition by a specific receptor; this makes homology-based searches for their plant counterparts diYcult. However, the overall molecular organization of these enzymes is similar: they consist of an amino terminal cytoplasmic tail, a signal anchor transmembrane domain, a stem region and a large lumenal hydrophilic catalytic domain (Colley, 1997) . For mammalian cells two major hypotheses have been forwarded to explain the nature of the localization signals of these enzymes: a bilayer thickness model and an oligomerization/kin recognition model. The bilayer thickness model postulates that location of a particular protein depends on the length of its transmembrane domain, which determines its retention in membranes of optimal width. Two lines of evidence support this hypothesis ( Bretscher and Munro, 1993; Masibay et al., 1993) : firstly, glycosyltransferase transmembrane domains are often suYcient for Golgi retention, and increasing their length leads to location in the more trans cisternae and eventually in the plasma membrane; secondly, cis to trans thickening of Golgi membranes has been demonstrated (Grove et al., 1968). The latter is probably due to the increase in cholesterol content from the ER membranes through the Golgi cisternae to the plasma membrane (Bretscher and Munro, 1993 ) , as increasing cholesterol content is known to increase the width of the membrane (Nezil and Bloom, 1992 ) . The oligomerization/kin recognition model of Golgi retention ( Machamer, 1991; Nilsson et al., 1994) proposes that the Golgi proteins can form insoluble homo- or hetero-oligomers which are unable to partition into transport vesicles destined for later compartments. The experimental data (mostly indirect, obtained using immunoprecipitation, ER co-retention, insolubility assays) in favour of oligomerization of Golgi enzymes are discussed by Colley (1997). In addition, interaction of the Golgi enzymes with cytoskeletal proteins on the cytoplasmic face may play a role in their retention (Barr and Warren, 1996; Colley, 1997, and references therein) . The reality of Golgi organization seems not to be adequately described by either of these models alone. The contribution of diVerent mechanisms is likely to vary depending on a particular protein and a particular cell type, and the features which are suYcient for correct Golgi protein localization in one tissue may be insuYcient in another. This may be accounted for by variability of the Golgi membrane characteristics (such as lipid composition of membranes, cisternal pH and ion concentration, associated skeletal proteins) in diVerent cell types. However, the precise data on these parameters are currently very limited. It should be noted that the presence of a particular enzyme in a particular cisternum does not necessarily mean that it is functional in this location, as appropriate substrates or donors may be lacking. Their concentrations are under the control of another group of Golgi proteins—nucleotide substrate transporters. Transporters The reactions carried out by the enzymes of the GA lumen consume nucleotide sugars which have to be translocated from the cytoplasm by specific transporters. At least in some cases, concentrations of the substrates are rate-limiting for respective reactions and, therefore, the transporters are probably able to regulate protein and lipid modifications in the Golgi lumen ( Abeijon et al., 1997) . Transporters of the nucleotide substrates are integral membrane proteins and function as antiporters with the corresponding nucleoside monophosphates. Very little information is available about their compartmentalization. While numerous mammalian nucleotide substrate transporters are known, only recently have the first plant transporters been identified (Mun˜ oz et al., 1996) . Also the topography and function of Golgi uridine-5∞diphosphatase, participating in metabolism of nucleotide sugars, from pea stems have been reported (Orellana et al., 1997 ) . Nucleotide diphosphate sugars imported into the Golgi are used by glycosyltransferases to transfer sugars on to glycoproteins, producing nucleosidediphosphates, which are glycosyltransferase inhibitors. They are cleaved by nucleoside diphosphatases, and nucleoside monophosphates serve as substrates for antiporters to import nucleotide diphosphate sugars ( Hirschberg, 1997) . What are the mechanisms of transport through the stack? Two principal models have been developed to explain the organization and function of the Golgi stack. According to the ‘vesicle shuttle model’ (initially proposed by Farquhar and Palade (1981 ) as a ‘stationary cisternal model’), each individual cisternum fulfils a particular set of processing reactions and possesses its own set of the enzymes. The transport of products between cisternae and retrieval of ‘escaped’ enzymes are mediated by vesicles (COPI for the retrograde and, possibly, also anterograde transport) or, according to a variation of this model (a ‘tubular intercisternal model’) by fusogenic tubes, whose buds are stabilized by COP coats. The ‘vesicle shuttle model’ has received experimental support from the studies by Rothman and coworkers ( Balch et al., 1984; Rothman and Wieland, 1996 ) . The model of ‘cisternal progression’ or ‘cisternal maturation’ was initially proposed by Grasse´ ( 1957 ) as a ‘directed maturation model’ and further developed by Morre´ et al. (1979) . This model (recently reviewed by Bannykh and Balch, 1997) suggests that whole cisternae with their contents move as units from the cis to the trans face through the stack. The trans-cisternum vesiculates, and a new cisternum is assembled at the cis-face from the ER-derived vesicles and COPI vesicles which recycle the enzymes from the vesiculated trans-cisternum. One of the major arguments in support of this view comes from biogenesis of algal scales initially described by Brown ( 1969 ). Both models encounter certain diYculties in explaining all the existing data. The experimental evidence accumulated in favour of each of these models has been analysed in the recent reviews (Schnepf, 1993; Hawes and SatiatJeunemaitre, 1996; Bannykh and Balch, 1997; Schekman and Mellman, 1997; Farquhar and Hauri, 1997) . It is diYcult to date to provide direct and definitive proof in favour of any of these models, and it is possible that both mechanisms are not mutually excluding and may take place under certain conditions. Essential assumptions of the ‘cisternal maturation’ as opposed to the ‘vesicle shuttle’ model concerning distribution of the Golgi enzymes are the presence in each cisternum of all processing enzymes or of only a specific subset of them, respectively. Both assumptions contradict the experimental data which suggest that the enzymes are not evenly distributed nor localized strictly to the specific cisternae, but rather form concentration gradients within the stack ( Hawes and Satiat-Jeunemaitre, 1996 ) . Glick et al. ( 1997) have recently developed a quantitative model which accounts for such a distribution pattern and reconciles ‘cisternal maturation’ with the observed asymmetric enzyme distribution in the stack. Their model assumes that the retrograde transport of Golgi enzymes, which occurs from each cisternum, is characterized by limited carrying capacity of the COPI vesicles and by diVerent aYnity of various Golgi enzymes for the receptor in COPI vesicles. This would result in preferential packaging and recycling of those enzymes which exhibit the highest aYnities for the receptor; they would therefore be concentrated in the cis-cisternae. The trans-Golgi enzymes are postulated to be the weakest competitors. Computer simulation shows that repeated cycles of cisternal progression/maturation lead to distribution of the enzymes to cis-, medial- or trans-Golgi according to their packaging eYciencies. COPI vesicles All models of Golgi function agree that COPI vesicles ( but not COPII vesicles which are out of the scope of this review) are essential for retrograde transport. A detailed model of the signalling cascade that might regulate COPI vesicle formation, which emerges from ample experimental data on yeast and mammalian cells, and also Dictyostelium, has been proposed by Roth and Sternweis ( 1997). Phosphatidylinositol (x)-phosphate produced by phosphatidylinositol kinases activates ARNO (the nucleotide exchange protein for ARF ), which catalyses the exchange of GDP for GTP on ARF. GTPbound (i.e. activated ) form of ARF then activates phospholipase D, which converts phosphatidylcholine to phosphatidic acid. Elevated local concentration of phosphatidic acid promotes membrane binding of COPI coat components, which include a stoichiometric set of otherwise cytoplasmic proteins (a-, b-, b∞-, c-, d- and f-COP). Presumptive plant homologues of the COPI components have been detected in EST database (Andreeva et al., 1998) and certainly non-clathrin coated vesicles can be seen associated with the margins of cisternal stacks in many electron micrographs ( Hawes and SatiatJeunemaitre, 1996) . Intra-Golgi transport appears to be regulated by a small GTP-binding protein rab 6 (Martinez et al., 1994 ) and possibly by rab1 (NuoVer et al., 1994) , or by YPT31/32 in yeast (Lazar et al., 1997 ) . In plants, rab 6 and numerous isoforms of rab 1 and ARF have been identified (see, for example, Regad et al., 1993; Bednarek et al., 1994; Borg et al., 1997 ) . Lipid regulators of vesicular transport (phoshoinositides, diacylglycerol ) may integrate signals from many other pathways of signal transduction where they are involved (Drøbak, 1993; Martin, 1997 ) . In this context, of interest is the evidence for lipid activation of the exchange factors for Rac/Rho, small GTPases which can stimulate rearrangments of the cytoskeleton and have been reported to have eVects on vesicular transport (Sugai et al., 1992; Lamaze et al., 1996; Roth and Sternweis, 1997) . Golgi apparatus and lipids The GA is able to synthesize lipids. For example, ubiquinone and plastoquinone are synthesized in the Golgi membranes of spinach leaves and then transported to the mitochondria and chloropasts, respectively (Swiezewska et al., 1993; Osowska-Rogers et al., 1994) . The mechanism of transport (apparently directed exclusively to the mitochondria or the chloroplasts) remains unknown. Lipid recognition may involve a signal associated with the lipid itself, carrier protein specificity and/or specific lipid receptors in the target membranes. Involvement of GA in the intracellular transport of lipids in plant cells has not been studied in much detail (Moreau and Cassagne, 1994) . Transport of very long fatty acids has been suggested to occur via the GA, while long chain fatty acids may be transported by lipid transfer proteins in plant cells ( Bertho et al., 1991 ) . Golgi apparatus and chloroplast protein precursors. In some cases, not only chloroplast lipids but also chloroplast protein precursors may be transported from the GA to the chloroplast. In dinoflagellates, diatoms and Euglena, precursors of some chloroplast proteins are cotranslationally targeted to the ER and, at least in the best studied system Euglena gracilis, are then transported to the GA (Sulli and Schwartzbach, 1995, 1996, and references therein) . As in the higher plants, the mature small subunit of ribulose-1,5-bisphosphate carboxylase/ oxygenase is a soluble protein in E. gracilis. Yet, it is inserted into the ER membrane as a polyprotein precursor and transported as an integral membrane protein to the GA prior to chloroplast import and polyprotein processing. Usage of the ER-GA pathway by the precursors of chloroplast proteins has not been detected in multicellular plants and is possibly limited to the algae whose chloroplasts are surrounded by three or four membranes and are thought to have originated by endosymbiosis of eukaryotic heterotrophic hosts with eukaryotic photosynthetic cells. Concluding remarks Despite the pleiomorphic nature of the GA and the considerable controversy surrounding its investigation, there is nearly a consensus on the core of characteristics common to the organelle in all eukaryotic cells. However, as can be seen above, many key questions still cannot be conclusively answered and the diVerent models still propose diVerent solutions to the questions. Some fundamental questions, to our knowledge, have not yet been investigated, for example: How is quality control, which should be no less important than that in the ER (Pedrazzini et al., 1997) , performed in the Golgi stack? What is the future of any proteins processed incorrectly? Are they directed to vacuole/cytoplasm for degradation, or digested in GA? Can a particular Golgi stack ‘die’ and, if so, how does it ‘die’ and what is its life time? Can plant GA appear de novo, for example, from the ER membranes? It is still not known what molecular machinery determines, despite the common principles of organization, the striking diVerences observed between the GA not only in diVerent kingdoms, but also in the cells of the same organism at diVerent developmental stages, in diVerent tissues and cell types. What are the laws which shape the GA ‘life style’ (which can be now observed in vivo in mammalian cells) in a particular environment, for example, under stress conditions? Considering the rapid development of the field in the last two decades, it is unlikely that the current questions on Golgi function will take another hundred years to answer. However, considering the complexity of cellular organization, a new set of problems can be expected to emerge which, to date, may only be figments of the imagination! Abeijon C , Mandon EC , Hirschberg CB . 1997 . Transporters of nucleotide sugars, nucleotide sulfate and ATP in the Golgi apparatus . Trends in Biochemical Sciences 22 , 203 - 7 . Andreeva AV , Kutuzov MA , Evans DE , Hawes CR . 1998 . Proteins involved in membrane transport between the ER and the Golgi apparatus: 21 putative plant homologues revealed by dbEST searching . Cell Biology International (in press). Balch WE , Dunphy WG , Braell WA , Rothman JE . 1984 . Reconstitution of the transport of protein between successive compartments of the Golgi measured by coupled incorporation of N-acetylglucosamine . Cell 39 , 405 - 16 . Bannykh SI , Balch W. 1997 . Membrane dynamics at the endoplasmic reticulum-Golgi interface . Journal of Cell Biology 138 , 1 - 4 . Barr FA , Warren G. 1996 . Disassembly and reassembly of the Golgi apparatus . Cell and Developmental Biology 7 , 505 - 10 . Baydoun EAH , Brett CT . 1997 . Distribution of xylosyltransferases and glucuronyltransferase within the Golgi apparatus in etiolated pea (Pisum sativum L.) epicotyls . Journal of Experimental Botany 48 , 1209 - 14 . Becker B , Melkonian M. 1996 . The secretory pathway of protists: spatial and functional organization and evolution . Microbiology Reviews 60 , 697 - 721 . Bednarek SY , Reynolds TL , Schroeder M , Grabowski R , Hengst L , Gallwitz D , Raikhel NV . 1994 . A small GTP-binding protein from Arabidopsis thaliana functionally complements the yeast YPT1 null mutant . Plant Physiology 104 , 591 - 6 . Berger EG . 1997 . The Golgi apparatus: from discovery to contemporary studies . In: Berger EG , Roth J , eds. The Golgi apparatus. Basel, Switzerland: Birkha¨user Verlag. Bertho P , Moreau P , Morre´ DJ, Cassagne C. 1991 . Monensin blocks the transfer of very long chain fatty acid-containing lipids to the plasma membrane of leek seedlings. Evidence for lipid sorting based on fatty acyl chain length . Biochimica et Biophysica Acta 1070 , 127 - 34 . Bisikirska B , Sikorski AF . 1997 . Some properties of spectrinlike proteins from Pisum sativum . Zeitschrift fu¨r Naturforschung-Journal of Biosciences 52 , 180 - 6 . Boevink P , Oparka K , Santa Cruz S , Martin B , Betteridge A , Hawes C. 1998 . Stacks on tracks: the plant Golgi apparatus traYcs on an actin/ER network . The Plant Journal (in press). Borg S , Brandstrup B , Jensen TJ , Poulsen C. 1997 . Identification of new protein species among 33 diVerent small GTP-binding proteins encoded by cDNAs from Lotus japonicus, and expression of corresponding mRNAs in developing root nodules . The Plant Journal 11 , 237 - 50 . Bowen RH . 1926 . The Golgi apparatus-its structure and functional significance . Anatomical Record 32 , 151 - 93 . Bowen RH . 1928 . Studies on the structure of plant protoplasm. I. The osmiophilic platelets . Zeitschrift fu¨r Zellforschung 6 , 689 - 725 . Bretscher MS , Munro S. 1993 . Cholesterol and the Golgi apparatus . Science 261 , 1280 - 1 . Brown RM . 1969 . Observations on the relationship of the Golgi apparatus to wall formation in the marine chrysophycean alga, Pleurochrysis scherVelii Pringsheim . Journal of Cell Biology 41 , 109 - 23 . Brummell DA , Catala C , Lashbrook CC , Bennett AB . 1997 . A membrane-anchored E-type endo-1,4-b-glucanase is localized on Golgi and plasma membranes of higher plants . Proceedings of the National Academy of Sciences, USA 94 , 4794 - 9 . Bruyant-Vannier MP , Gaudinet-Schaumann A , Bourlard T , Morvan C. 1996 . Solubilization and partial characterization of pectin methyltransferase from flax cells . Plant Physiology and Biochemistry 34 , 489 - 99 . Cluett EB , Brown WJ . 1992 . Adhesion of Golgi cisternae by proteinaceous interactions: intercisternal bridges as putative adhesive structures . Journal of Cell Science 103 , 773 - 84 . Cole NB , Smith CL , Sciaky N , Terasaki M , Edidin M , Lippincott-Schwartz J. 1996 . DiVusional mobility of Golgi proteins in membranes of living cells . Nature 273 , 797 - 801 . Colley KJ . 1997 . Golgi localization of glycosyltransferases: more questions than answers . Glycobiology 7 , 1 - 13 . Cooke R , Raynal M , Laudie´ M, Grellet F , Delseny M , Morris PC , Guerrier D , Giraudat J , Quigley F , Clabault G , Li YF , Mache R , Krivitzky M , Gy IJJ , Kreis M , Lecharny A , Parmentier Y , Marbach J , Fleck J , Cle´ment B , Philipps G , Herve` C, Bardet C , Tremousaygue D , Lescure B , Lacomme C , Roby D , Jourjon MF , Chabrier P , Charpenteau JL , Desprez T , Amselem J , Chiapello H , Ho¨ fte H. 1996 . Further progress towards a catalogue of all Arabidopsis genes: analysis of a set of 5000 non-redundant ESTs . The Plant Journal 9 , 101 - 24 . Craig S , Staehelin LA . 1988 . High pressure freezing of intact plant tissues. Evaluation and characterization of novel features of the endoplasmic reticulum and associated membrane systems . European Journal of Cell Biology 46 , 80 - 93 . Driouich A , Levy S , Staehelin L , Faye L. 1994 . Structural and functional organization of the Golgi apparatus in plant cells . Plant Physiology and Biochemistry 32 , 731 - 45 . Driouich A , Staehelin LA . 1997 . The plant Golgi apparatus: structural organization and functional properties . In: Berger EG , Roth J , eds. The Golgi apparatus. Switzerland: Birkha¨user Verlag. Drøbak BK . 1993 . Plant phosphoinositides and intracellular signalling . Plant Physiology 102 , 705 - 9 . Farquhar MG , Hauri H-P. 1997 . Protein sorting and vesicular traYc in the Golgi apparatus . In: Berger EG , Roth J , eds. The Golgi apparatus. Switzerland: Birkha¨user Verlag. Farquhar MG , Palade GE . 1981 . The Golgi apparatus (complex)-( 1954 -1981) -from artefact to center stage . Journal of Cell Biology 91 , 77S - 103S . Faye L , Fitchette-Laine´ AC , Gomord V , Chekkafi A , Delaunay AM , Driouich A. 1992 Detection, biosynthesis and some functions of glycans N-linked to plant secreted proteins . In: Battey NH , Dickinson HG , Hetherington AM , eds. Posttranslational modifications in plants. SEB Seminar series , Vol. 53 . Cambridge University Press, 213 - 42 . Franke WW , Kartenbeck J , Krien S , VanderWoude WJ , Scheer U , Morre´ DJ. 1972 . Inter- and intracisternal elements of the Golgi apparatus. A system of membrane-to-membrane cross-links . Zeitschrift fu¨ r Mikroskopisch-anatomische forschung 132 , 365 - 80 . Garcia-Herdugo G , Gonza´lez- Reyes JA , Gracia-Navarro F , Navas P. 1988 . Growth kinetics of the Golgi apparatus during the cell cycle in onion root meristems . Planta 175 , 305 - 12 . Glick BS , Elston T , Oster G. 1997 . A cisternal maturation mechanism can explain the asymmetry of the Golgi stack . FEBS Letters 414 , 177 - 81 . Golgi C. 1898 . Sur la structure des cellules nerveuses . Archives Italiennes de Biologie 30 , 60 - 71 . (Originally published in Bollettino della Societa med .-chir. di Pavia , 1898 .) Grasse ´ PP. 1957 . Ultrastructure, polarite´ et reproduction de l'appareil de Golgi. Compte rendu hebdomadaire des se ´ances de l' Academie des sciences 245 , 1278 - 81 . GriYng LR . 1991 . Comparisons of Golgi structure and dynamics in plant and animal cells . Journal of Electron Microscopy Technique 17 , 179 - 99 . Grove SN , Bracker CE , Morre´ DJ . 1968 . Cytomembrane diVerentiation in the endoplasmic reticulum- Golgi apparatus-vesicle complex . Science 161 , 171 - 3 . Hanna R , Brummell DA , Camirand A , Hensel A , Russel EF , Maclachlan GA . 1991 . Solubilization and properties of GDPfucosyltransferases from pea epicotyl membranes . Archives for Biochemistry and Biophysics 290 , 7 - 13 . Harris N , Oparka KJ . 1983 . Connections between dictyosomes, ER and GERL in cotyledons of mung bean (Vigna radiata L.) . Protoplasma 114 , 93 - 102 . Hawes C , Martin B. 1986 . Deep etching of plant cellscytoskeleton and coated pits . Cell Biology International 10 , 985 - 92 . Hawes C , Satiat-Jeunemaitre B. 1996 . Stacks of questionsHow does the plant Golgi work? Trends in Plant Sciences 1 , 395 - 401 . Hawes C , Faye L , Satiat-Jeunemaitre B. 1996 . The Golgi apparatus and pathways of vesicle traYcking . In: Smallwood M , Knox P , Bowles D , Greenwich CT , eds. Membranes: specialized functions in plants . JAI , 337 - 65 . Hirschberg CB . 1997 . Transport of nucleotide sugars, nucleotide sulfate and ATP into the lumen of the Golgi apparatus . In: Berger EG , Roth J , eds. The Golgi apparatus. Switzerland: Birkha¨user Verlag. H o¨ftberger M , Turl T , Meindl U. 1995 . Disturbance of the secetory pathway in Micrasterias denticula by tunicamycin and cyclopiazonic acid . Protoplasma 189 , 173 - 9 . Iijima M , Kono Y. 1992 . Development of Golgi apparatus in the root cap cells of maize (Zea mays L.) is aVected by compacted soil . Annals of Botany 70 , 207 - 12 . Juniper B , Hawes CR , Horne JC. 1982 . The relationship between the dictyosomes and the forms of the endoplasmic reticulum in plant cells with diVerent export programs . Botanical Gazette 143 , 135 - 45 . Kristen U. 1978 . Ultrastructure and a possible function of the intercisternal elements in dictyosomes . Planta 138 , 29 - 33 . Lamaze C , Chuang TH , Terlecky LJ , Bokoch GM , Schmid SL . 1996 . Regulation of receptor-mediated endocytosis by Rho and Rac . Nature 382 , 177 - 9 . La Valette St George AJH . 1865 . U¨ ber die Genese der Samenko¨ rper. Part 1 . Archiv fu¨ r mikroskopische Anatomie 1 , 403 - 14 . La Valette St George AJH . 1867 . U¨ ber die Genese der Samenko¨ rper. Part 2 . Archiv fu¨ r mikroskopische Anatomie 1 , 263 - 73 . Lazar T , Go¨ tte M, Gallwitz D. 1997 . Vesicular transport: how many Ypt/Rab-GTPases make a eukaryotic cell? Trends in Biochemical Sciences 22 , 468 - 72 . Lorenz M , Bisikirska B , Hanuslorenz B , Strzalka K , Sikorski AF . 1995 . Proteins reacting with anti-spectrin antibodies are present in Chlamydomonas cells . Cell Biology International 19 , 625 - 32 . Lynch M , Staehelin L. 1992 . Domain-specific and cell type-specific localization of two types of cell wall matrix polysaccharides in the clover root tip . Journal of Cell Biology 118 , 467 - 9 . Machamer CE . 1991 . Golgi retention signals: do membranes hold the key? Trends in Cell Biology 1 , 141 - 4 . Martin TFJ . 1997 . Phosphoinositides as spatial regulators of membrane traYc . Current Opinion Neurobiology 7 , 331 - 8 . Martinez O , Schmidt A , Salamero J , Hoflack B , Roa M , Goud B. 1994 . The small GTP-binding protein rab6 functions in intra-Golgi transport . Journal of Cell Biology 127 , 1575 - 88 . Masibay AS , Balaji PV , Boeggeman EE , Qasba PK . 1993 . Mutational analysis of the Golgi retention signal of bovine b-1,4-galactosyltransferase . Journal of Biological Chemistry 268 , 9908 - 16 . Meindl U , Lancelle S , Hepler PK . 1992 . Vesicle production and fusion during lobe formation in Micrasterias visualized by high-pressure freeze fixation . Protoplasma 170 , 104 - 11 . Misteli T , Warren G. 1995 . A role for tubular networks and a COPI-independent pathway in the mitotic fragmentation of Golgi stacks in a cell-free system . Journal of Cell Biology 120 , 1027 - 39 . Mollenhauer HH . 1965a . Transition forms of Golgi apparatus secretion vesicles . Journal of Ultrastructure Research 12 , 439 - 46 . Mollenhauer HH . 1965b . An intercisternal structure in the Golgi apparatus . Journal of Cell Biology 24 , 504 - 11 . Mollenhauer HH , Morre´ DJ . 1976 . Transition elements between endoplasmic reticulum and Golgi apparatus in plant cells . Journal of Cell Science 19 , 231 - 7 . Mollenhauer HH , Morre´ DJ . 1978 . Structural diVerences contrast higher plant and animal Golgi apparatus . Journal of Cell Science 32 , 357 - 62 . Mollenhauer HH , Morre´ DJ . 1994 . Structure of Golgi apparatus . Protoplasma 180 , 14 - 28 . Moore PJ , Swords KMM , Lynch MA , Staehelin LA . 1991 . Spatial reorganization of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants . Journal of Cell Biology 112 , 589 - 602 . Moreau P , Cassagne C. 1994 . Phospholipid traYcking and membrane biogenesis . Biochimica et Biophysica Acta 1197 , 257 - 90 . Morre´ DJ , Kartenbeck J , Franke WW . 1979 . Membrane flow and interconversions among endomembranes . Biochimica et Biophysica Acta 559 , 71 - 152 . Mu n˜oz P , Norambuena L , Orellana A. 1996 . Evidence for a UDP-glucose transporter in Golgi apparatus-derived vesicles from pea and its possible role in polysaccharide biosynthesis . Plant Physiology 112 , 1585 - 94 . Newman T , de Bruijn, Green P , Keegstra K , Kende H , McIntoch L , Ohlrogge J , Raikhel N , Somerville A , Thomashow M , Retzel E , Somerville C. 1994 . Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones . Plant Physiology 106 , 1241 - 55 . Nezil FA , Bloom M. 1992 . Combined influence of cholesterol and synthetic amphiphilic peptides upon bilayer thickness in model membranes . Biophysical Journal 61 , 1176 - 83 . Nilsson T , Hoe MH , Slusarewicz P , Rabouille C , Watson R , Hunte F , Watzele G , Berger EG , Warren G. 1994 . Kin recognition between medial-Golgi enzymes in HeLa cells . EMBO Journal 13 , 562 - 74 . Noguchi T. 1983 . Number of dictyosomes in a single cell of the green alga Micrasterias americana . Botanical Magazine (Tokyo) 96 , 277 - 80 . Noguchi T. 1988 . Numerical and structural changes in dictyosomes during zygote germination of Closterium ehrenbergii . Protoplasma 95 , 135 - 42 . Northcote D , Pickett-Heaps JD . 1966 . A function of the Golgi apparatus in polysaccharide synthesis and transport in the root cap cells of wheat . Biochemical Journal 98 , 159 - 67 . NuoVer C , Davidson HW , Matteson J , Meinkoth J , Balch WE . 1994 . A GDP-bound form of rab1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments . Journal of Cell Biology 125 , 225 - 37 . Orellana A , Neckelmann G , Norambuena L. 1997 . Topography and function of Golgi uridine-5∞-diphosphatase from pea stems . Plant Physiology 114 , 99 - 107 . Osowska-Rogers S , Swiezewska E , Andersson B , Dallner G. 1994 . The endoplasmic reticulum-Golgi system is a major site of plastoquinone synthesis in spinach leaves . Biochemical and Biophysical Research Communications 205 , 714 - 21 . Pedrazzini E , Giovinazzo G , Bielli A , de Virgilio M , Frigerio L , Pesca M , Faoro F , Bollini R , Ceriotti A , Vitale A. 1997 . Protein quality control along the route to the plant vacuole . The Plant Cell 9 , 1869 - 80 . Presley JF , Nelson BC , Schroer TA , Hirschberg K , Zaal KJM , Lippincott-Schwartz J. 1997 . ER-to-Golgi transport visualized in living cells . Nature 389 , 81 - 5 . Rabouille C , Warren G. 1997 . Changes in the architecture of the Golgi apparatus during mitosis . In: Berger EG , Roth J , eds. The Golgi apparatus. Switzerland: Birkha¨user Verlag. Regad F , Bardet S , Tremousaygue D , Moisan A , Lescure B , Axelos M. 1993 . cDNA cloning and expression of an Arabidopsis GTP-binding protein of the Arf family . FEBS Letters 316 , 133 - 6 . Robinson DG , Kristen U. 1982 . Membrane flow via the Golgi apparatus in higher plant cells . International Review of Cytology 77 , 89 - 127 . Roth MG , Sternweis PC . 1997 . The role of lipid signaling in constitutive membrane traYc . Current Opinion in Cell Biology 9 , 519 - 26 . Rothman JE , Wieland FT . 1996 . Protein sorting by transport vesicles . Science 272 , 227 - 34 . Satiat-Jeunemaitre B , Hawes C. 1992 . Redistribution of a Golgi glycoprotein in plant cells treated with brefeldin A . Journal of Cell Science 103 , 1153 - 66 . Satiat-Jeunemaitre B , Steele C , Hawes C. 1996 . Golgi-membrane dynamics are cytoskeleton dependent. A study on Golgi stack movement induced by brefeldin A . Protoplasma 191 , 21 - 33 . Scales SJ , Pepperkok R , Kreis TE . 1997 . Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI vesicles . Cell 90 , 1137 - 48 . Schekman R. 1994 . Translocation gets a push . Cell 78 , 911 - 13 . Schekman R , Mellman I. 1997 . Does COPI go both ways ? Cell 90 , 197 - 200 . Schnepf E. 1969 . Sekretion und Exkretion bei Pflanzen . Protoplasmatologia 8 , 181 . Schnepf E. 1993 . Golgi apparatus and slime secretion in plants: the early implications and recent models of membrane traYc . Protoplasma 172 , 3 - 11 . Schnepf E , Bush J. 1976 . Morphology and kinetics of slime secretion in glands of Mimulus tinlingii . Zeitschrift fu¨r Pflanzenphysiology 79 , 62 - 71 . Staehelin LA , Driouich A. 1997 . Brefeldin A eVects in plants: are diVerent Golgi responses caused by diVerent sites of action? Plant Physiology 104 , 401 - 3 . Staehelin LA , Giddings Jr TH , Kiss JZ , Sack FD . 1990 . Macromolecular diVerentiation of Golgi stacks in root tip of Arabidopsis and Nicotiana seedlings as visualized in high pressure frozen and freeze-substituted samples . Protoplasma 157 , 75 - 91 . Staehelin LA , Hepler PK . 1996 . Cytokinesis in higher plants . Cell 84 , 821 - 4 . Staehelin L , Moore I. 1995 . The plant Golgi apparatus: structure, functional organization and traYcking mechanisms . Annual Review of Plant Physiology and Plant Molecular Biology 46 , 261 - 88 . Steer MW , O'Driscoll D. 1991 . Vesicle dynamics and membrane turnover in plant cells . In: Hawes CR , Coleman JOD , Evans DE , eds. Endocytosis, exocytosis and vesicle traYc in plants . Cambridge University Press, 129 - 42 . Sugai M , Chen CH , Wu HC . 1992 . Bacterial ADP-ribosyltransferase with a substrate specificity of the Rho protein disassembles the Golgi apparatus in Vero cells and mimics the action of brefeldin A . Proceedings of the National Academy of Sciences, USA 89 , 8903 - 7 . Sulli C , Schwartzbach SD . 1995 . The polyprotein precursor to the Euglena light-harvesting chlorophyll a/b-binding protein is transported to the Golgi apparatus prior to chloroplast import and polyprotein processing . Journal of Biological Chemistry 270 , 13084 - 90 . Sulli C , Schwartzbach SD . 1996 . A soluble protein is imported into Euglena chloroplasts as a membrane-bound precursor . The Plant Cell 8 , 43 - 53 . Swiezewska E , Dallner G , Andersson B , Ernster L. 1993 . Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves . Journal of Biological Chemistry 268 , 1494 - 9 . Turner FR , Whaley WG . 1965 . Intercisternal elements of the Golgi apparatus . Science 147 , 1303 - 4 . Ueda K. 1997 . The synchronous division of dictyosomes at the premitotic stage . Annals of Botany 80 , 29 - 33 . Whaley WG . 1975 . The Golgi apparatus . Cell Biology Monographs , Vol. 2 . Wien , New York: Springer-Verlag. Walne PL . 1967 . The eVects of colchicine on cellular organization in Chlamydomonas . II. Ultrastructure. American Journal of Botany 54 , 564 - 77 . Wolin SL . 1994 . From the elephant to E. coli: SRP-dependent protein targeting . Cell 77 , 787 - 90 . Zhang GF , Driouich A , Staehelin LA . 1996 . Monensin-induced redistribution of enzymes and products from Golgi stacks to swollen vesicles in plant cells . European Journal of Cell Biology 71 , 332 - 40 . Zhang GF , Staehelin LA . 1992 . Functional compartmentation of the Golgi apparatus of plant cells. Immunocytochemical analysis of high-pressure frozen- and freeze-substituted sycamore maple suspension culture cells . Plant Physiology 99 , 1070 - 83 .

This is a preview of a remote PDF:

Alexandra V. Andreeva, Mikhail A. Kutuzov, David E. Evans, Chris R. Hawes. The structure and function of the Golgi apparatus: a hundred years of questions, Journal of Experimental Botany, 1998, 1281-1291, DOI: 10.1093/jxb/49.325.1281