Download The structure and function of the Golgi apparatus

Journal of Experimental Botany, Vol. 49, No. 325, pp. 1281–1291, August 1998
The structure and function of the Golgi apparatus:
a hundred years of questions
Alexandra V. Andreeva, Mikhail A. Kutuzov, David E. Evans and Chris R. Hawes1
Research School of Biological and Molecular Sciences, Oxford Brookes University, Gipsy Lane Campus,
Headington, Oxford OX3 0BP, UK
Received 19 January 1998; Accepted 19 March 1998
Abstract
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.
Key words: Golgi apparatus, intracellular membrane traffic,
secretion, vesicles.
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 different 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
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 difficult 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
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).
1 To whom correspondence should be addressed. Fax: +44 1865 483955. E-mail: [email protected]
© Oxford University Press 1998
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Andreeva et al.
Fig. 1. Confocal serial optical section reconstruction of the Golgi
apparatus in a suspension-cultured tobacco (BY2) cell. The Golgi
stacks were immunostained with monoclonal antibody (JIM 84)
recognizing a Golgi-associated glycoprotein. Bar=10 mm. Material
supplied by B Satiat-Jeunemaitre.
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
difficulties ( 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;
http://www.bio.cam.ac.uk/dept/biochem/UTOs/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
trafficking 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 traffic is not yet sufficient 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 effects on GA
function; Zhang et al., 1996), cyclopiazonic acid (an
inhibitor of Ca2+-ATPases; Höftberger 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
Fig. 2. Golgi stack in a maize root cap cell. Note the network of
vesicles and tubules at the trans-face ( T ) and the close association with
a tubule of endoplasmic reticulum ( ER) with the cis-face. The material
was post-fixed in a zinc iodide/osmium tetroxide mixture to impregnate
selectively the endomembrane system. Bar=100 nm.
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
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 traffic 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
The Golgi apparatus 1283
Fig. 3. Golgi structure in suspension-cultured carrot cells after ultra-rapid freeze fixation by slamming against a helium-cooled copper block.
(A) Freeze-substitution in osmium acetone showing the trans-network of tubules and vesicles plus intercisternal elements. (B) Deep-etched and
rotary shadowed replicated preparation. Note small vesicles (arrows) associated with the periphery of the cisternae across the stack. Bars=200 nm.
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 Morré, 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 different 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
Morré, 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 Morré, 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 differentiation 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
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Andreeva et al.
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 Morré, 1994; Cole et al., 1996),
and lateral diffusion 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 Morré, 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, different 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
Different 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 (Griffing, 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 effect
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
Morré, 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
The Golgi apparatus 1285
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 Morré, 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 differ: 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 different 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.
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Andreeva et al.
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
difficult. 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 sufficient 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 different mechanisms is likely to vary
depending on a particular protein and a particular cell
type, and the features which are sufficient for correct
Golgi protein localization in one tissue may be insufficient
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 different 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 (Muñoz 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 Grassé (1957) as a
‘directed maturation model’ and further developed by
Morré et al. (1979). This model (recently reviewed by
The Golgi apparatus 1287
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 difficulties 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
difficult 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 different
affinity 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
affinities 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
efficiencies.
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 (Nuoffer 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 effects 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
1288
Andreeva et al.
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 different models still propose different 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 differences observed between the GA not only
in different kingdoms, but also in the cells of the same
organism at different developmental stages, in different
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!
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