Download Transport Between the Endoplasmic Reticulum and Golgi Apparatus

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Blackwell Munksgaard
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Blackwell Munksgaard 2005
doi: 10.1111/j.1600-0854.2005.00278.x
Review
Crossing the Divide – Transport Between the
Endoplasmic Reticulum and Golgi Apparatus in Plants
Sally L. Hanton*, Lauren E. Bortolotti, Luciana
Renna, Giovanni Stefano and Federica Brandizzi
Department of Biology, 112 Science Place, University of
Saskatchewan, Saskatoon, Saskatchewan S7N 5E2,
Canada
*Corresponding author: Sally L. Hanton, sally.hanton@
usask.ca
The transport of proteins between the endoplasmic
reticulum (ER) and the Golgi apparatus in plants is an
exciting and constantly expanding topic, which has
attracted much attention in recent years. The study of
protein transport within the secretory pathway is a relatively new field, dating back to the 1970s for mammalian
cells and considerably later for plants. This may explain
why COPI- and COPII-mediated transport between the ER
and the Golgi in plants is only now becoming clear, while
the existence of these pathways in other organisms is
relatively well documented. We summarize current knowledge of these protein transport routes, as well as highlighting key differences between those of plant systems
and those of mammals and yeast. These differences have
necessitated the study of plant-specific aspects of protein
transport in the early secretory pathway, and this review
discusses recent developments in this area. Advances in
live-cell-imaging technology have allowed the observation
of protein movement in vivo, giving a new insight into
many of the processes involved in vesicle formation and
protein trafficking. The use of these new technologies has
been combined with more traditional methods, such as
protein biochemistry and electron microscopy, to increase
our understanding of the transport routes in the cell.
Key words: COPI, COPII, endoplasmic reticulum, ER export
site, Golgi, protein transport
Received 9 December 2004, revised and accepted for
publication 24 January 2005
The secretory pathway is complex system of organelles
specialized for the synthesis, transport, modification and
secretion of proteins and other macromolecules (1). As
such, this system plays a vital role in the life of a cell. It
is generally assumed that protein transport through the
secretory pathway is controlled by vesicular transport
intermediates that carry cargo molecules from one organelle to the next. Vesicular transport can occur in the
forward (anterograde) direction, from the endoplasmic reticulum (ER) towards the plasma membrane, or in reverse
(retrograde). The entire secretory pathway exists in equilibrium between anterograde and retrograde transport, and
any disruption of a part of this balance can result in
dramatic changes in the biology of a cell.
Vesicle budding and fusion mechanisms at the ER–Golgi
interface are highly conserved between species (2–4). The
formation of vesicles is induced by the action of cytoplasmic coat protein complexes (COPs) that polymerize on the
membrane surface, capturing both cargo molecules and
those that function in vesicle direction, such as soluble
N-ethylmaleimide-sensitive factor attachment protein
receptors (SNAREs) in the process. The membrane
becomes deformed during the polymerization of the coat,
resulting in the formation of a nascent vesicle. Small
proteins with GTPase activity regulate the assembly and
disassembly of the vesicle coat by cycling between GTPbound (activated) forms and GDP-bound (inactivated)
forms. The activated form initiates the recruitment of
coat proteins to the membrane, whereas hydrolysis of
GTP to GDP alters the conformation of the GTPase and
triggers uncoating of the vesicle. The GTPase activity is
tightly regulated by guanine-nucleotide exchange factors
(GEFs) and GTPase-activating proteins (GAPs), which prevent unproductive cycles of membrane coating and
uncoating.
The Secretory Pathways of Plants and Animals
are not Identical
The organization of the organelles that make up the secretory pathway of plants differs greatly from that of mammals
and yeast. Despite the identification of plant homologues of
proteins that are known to be involved in vesicular transport
in other systems, the mechanisms in plants have not yet
been fully characterized. Given the differences in the features of the secretory pathway of plants compared with
those of other organisms, it seems likely that plants have
evolved unique characteristics for achieving efficient protein
transport between organelles. We discuss current knowledge of these characteristics, although further study will be
necessary to elucidate many of the processes involved in
protein transport in plant cells.
The ER in plants is pushed to the cortex of the cell by the
large central vacuole, whereas the mammalian ER has no
such constraints and can exist throughout the cell, radiating
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out from the nuclear envelope. The domains of the ER
from which proteins are exported to the Golgi apparatus,
termed ER export sites (ERES), are relatively immobile in
mammals (5), while in plants, they are highly motile (6).
Similarly, the mammalian Golgi apparatus remains relatively stationary in the perinuclear region of the cell and is
much larger than the plant Golgi. It has been reported that in
various plant cellular systems the Golgi apparatus is present
as multiple stacks that are distributed throughout the
cytosol and are capable of rapid movement
(7–9)
(Figure 1). The mammalian secretory pathway contains an
additional organelle known as the ER-Golgi intermediate
compartment (ERGIC), which does not exist in plants,
although the cis-Golgi may play a similar role. In contrast,
the plant cell contains one or more vacuolar compartments
(10), which can perform different functions such as protein
degradation, turgor maintenance and protein storage,
depending on the tissue and species. Animal cells contain
lysosomes, which perform a similar degradative function
to that of the lytic vacuole in plants, but are much smaller
and are distributed throughout the cell. The presence of
different types of vacuoles in plants necessitates the existence of additional transport pathways that allow cargo
molecules to travel to these organelles. Finally, the most
distal location in the plant cell is the cell wall, which requires
the secretion of a variety of molecules for its generation and
maintenance. This transport is one of the driving forces
behind the secretory pathway.
Despite these differences in the secretory pathways, proteins in both plants and animals are generally transported
in the anterograde direction from the ER to the Golgi
apparatus, at which point they are sorted for further transport either forward, in the direction of the cell surface and
organelles in the later secretory pathway, or back towards
the ER.
The Complexity of Protein Transport in Plants
Figure 2 shows a schematic representation of the secretory pathway in plants, summarizing the main transport
pathways that have been established and proposed.
Export from the ER to the Golgi occurs via a COPIImediated mechanism (arrow 1) (6,11,12), but evidence
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9.4
18.9
28.3
37.8
47.2
Figure 1: The endoplasmic reticulum and Golgi apparatus in plants are motile. Confocal laser scanning microscope images showing
an epidermal cell from tobacco leaves, coexpressing a GFP-tagged Golgi marker protein and a YFP-tagged endoplasmic reticulum (ER)
marker protein. Images were taken at different time-points (seconds; shown at top left of each image) to demonstrate the movement of
both ER and Golgi. The white arrowhead indicates a single Golgi body throughout the time series, while the empty arrowhead indicates
movement within the ER. Size bar ¼ 2 mm.
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Protein Traffic at the Plant ER–Golgi Interface
5
4
TGN
PVC
PSV
Golgi
6
3
1
2
Lytic
vacuole
ER
PVC
for a second anterograde pathway that is not controlled by
COPII has also been postulated (arrow 2) (13). To balance
these forward transport pathways, at least one retrograde
pathway must exist to carry cargo molecules back from
the Golgi to the ER. Retrieval of proteins from Golgi to ER
is required for a variety of reasons. Some proteins are
intended to be resident within the ER, sometimes with a
role in the folding and modification of newly synthesized
proteins. These proteins can escape from the ER through
accidental incorporation into the lumen of export carriers,
and then need to be retrieved from the Golgi (12,14). It
seems likely that other proteins that are involved in the
export machinery itself may also be salvaged so that they
can be re-used in a subsequent round of vesicle formation
and transport. The retrieval mechanism is based on the
presence of one or more signals in the sequence of the
protein (15), which can be recognized by a receptor or
receptor-like protein. The binding of ligand to receptor is
thought to induce the formation of a retrograde vesicle to
transport ER-resident proteins back to their destination, as
has been shown in mammals (16,17). These vesicles are
known as COPI vesicles (arrow 3) (18,19), although COPIindependent retrograde transport pathways have been
proposed in mammalian cells (20–22). One or more of
these alternative routes may also exist in plants to balance
the effects of the COPII-independent anterograde route
suggested by Törmäkangas et al. (13).
Later transport in the secretory pathway is mediated by
other vesicle types such as clathrin-coated vesicles (arrow
4) (23), which have been proposed to mediate transport
from the Golgi apparatus to the lytic vacuole, and dense
vesicles (arrow 5) (24,25), which convey cargo proteins to
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Figure 2: Overview of the
secretory pathway in plants.
Schematic representation of
organelles and their connecting
protein transport routes in the
plant-secretory pathway. Routes
are numbered as follows: 1 –
COPII-mediated endoplasmic
reticulum (ER)–Golgi traffic; 2 –
COPII-independent ER–Golgi
traffic; 3 – COPI-mediated Golgi–
ER traffic; 4 – traffic in clathrincoated vesicles (CCVs) from the
trans-Golgi network (TGN) to the
prevacuolar compartment (PVC);
5 – traffic via dense vesicles
(DVs) to the protein storage
vacuole (PSV); 6 – direct ER–
PSV traffic.
the storage vacuole. In addition to these routes that carry
cargo from the Golgi to the vacuoles, a variety of vesicle
types that appear to transport storage proteins directly
from the ER to the protein storage vacuole (PSV) have
been identified in seeds (arrow 6) (26–28). It has been
shown in developing wheat grains that aggregates of storage proteins form within the ER bud off to form vesicular
structures surrounded by rough ER (27), which are incorporated into the vacuole through a mechanism similar to
autophagy. Comparable structures have been identified in
germinating seeds, designated KDEL-tailed cysteine proteinase-accumulating vesicles (KVs) (26), and in maturing
seeds, termed precursor-accumulating (PAC) vesicles (28).
The contents of these vesicles are mainly unglycosylated
storage proteins, which do not require Golgi-mediated
modifications. However, other storage proteins that carry
complex glycan chains have been found on the periphery
of the PAC vesicles (28). This may indicate that Golgiderived vesicles carrying these glycoproteins have fused
with the PAC vesicles en route to the PSV. Alternatively,
these proteins may be transported to the Golgi for glycan
processing to take place, followed by recycling to the ER
for packaging into PAC vesicles and transport to the PSV.
Further investigation into the precise mechanisms by
which proteins are transported to the PSV is required to
clarify these ambiguities.
The multitude of transport pathways present in plant cells
means that the trafficking of proteins in vesicular intermediates is a vast subject that cannot be properly discussed in a single review. This review therefore focuses
specifically on the complex area of transport between the
ER and the Golgi in plant cells. We discuss the formation
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mechanisms and functions of COPI vesicles and review
current knowledge of putative COPII carriers, as well as the
various models for the transfer of proteins between ER
and Golgi in plant cells.
Anterograde Transport from the ER is
Mediated by COPII
Although COPII-mediated export of proteins from the ER is
not the only anterograde ER–Golgi route that has been
proposed in plants, it has received the most attention and
is therefore the best-characterized pathway between
these organelles at this time. Transport mediated by
COPI and COPII is very similar in many respects. The
main difference between the two is that while COPII
carriers originate in the ER and export newly synthesized
proteins to the Golgi complex, COPI vesicles bud from the
cis-Golgi and travel to the ER. In mammalian cells, COPII
vesicles transport proteins as far as the ERGIC. After this,
it has been suggested that the proteins are repackaged
into vesicles that mediate transport to the Golgi apparatus
and may be involved in forward transport through the Golgi
(29,30). A recent study has shown that protein transport
occurs from the ERGIC both forward to the Golgi and back
towards to the ER (30), supporting the argument that the
ERGIC is a discrete stable compartment. However, this does
not preclude the possibility that it eventually develops into
the cis-Golgi in an extension of the cisternal maturation
model (31–34). It appears that the ERGIC in mammals is
similar in function to the cis-Golgi in plants, in that it is a point
from which proteins can be returned to the ER or transported
forward to distal locations. It has also been reported that
COPI vesicles may bud directly from the ER in yeast and
mammals (35,36), although no data supporting this
possibility in plants have yet been presented.
The formation of both COPII and COPI vesicles requires
the activation of a specific small GTPase, which causes the
recruitment of structural components of the vesicle coat to
the membrane, resulting in the formation of a vesicle that
can then bud from the membrane and travel to its destination. COPII vesicles have not yet been isolated from
plants, but homologues of several of the components of
the COPII coat have been identified (11,37,38) and have
been used to study the pathway (6,12). The small, cytosolic GTPase Sar1p mediates COPII vesicle formation in
yeast and mammals. Three isoforms of Sar1p have been
identified in Arabidopsis (39), at least one of which
(AtSar1a) is capable of complementing Saccharomyces
cerevisiae mutants (38). This suggests similarities
between the mechanisms of vesicle budding in the two
systems. The activation of Sar1p is mediated by an
ER-localized integral membrane protein called Sec12p, a
functional homologue of which has been identified in
Arabidopsis (37,38). Sec12p is a GEF, recruiting Sar1p to
the ER membrane in order to become activated through
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the exchange of GDP for GTP, which initiates vesicle formation. Sec12p is not incorporated into COPII carriers (6,
40), meaning that activated Sar1p can maintain its membrane association independently of Sec12p. It has been
shown in crystallization studies that mammalian Sar1p
possesses an amphipathic N-terminal domain that is
exposed on binding to GTP and allows direct interaction
of Sar1p with the membrane (41). The homology between
mammalian and plant Sar1p suggests that this may also be
the case in plants, although this has yet to be confirmed
experimentally.
It has been demonstrated through in vitro studies of nonplant systems that the coat proteins of COPII vesicles
form two heterodimeric complexes that are sequentially
recruited to the membrane by activated Sar1p (40,42).
Sec23/24p binds to Sar1p, after which the Sec13/31p
complex completes the coat. The assembly of the coat
proteins on the membrane causes membrane curvature
and eventually vesicle budding. After this, the protein coat
must be released in order for the vesicle to fuse with the
target membrane (in this case the Golgi apparatus). This
step is induced by the hydrolysis of GTP by Sar1p, causing
a conformational change that allows Sar1p to dissociate
from the membrane (41). The hydrolysis of GTP is stimulated by the presence of a GAP, Sec23p (43). The fact that
the GAP is a functional part of the COPII coat means that it
is in close proximity to Sar1p, which may cause rapid GTP
hydrolysis and increase the instability of the vesicular
structure. The release of Sar1p from the membrane
causes the dissociation of the coat proteins, leaving a
membranous vesicle that can fuse with the Golgi apparatus and release its contents. Proteins are then sorted for
further anterograde transport or retrograde transport back
towards the ER. The instability of the COPII vesicle may
account for some of the difficulties faced when attempting
to isolate them from plants. However, daSilva et al. (6)
demonstrated that recruitment of Sar1p to ERES can be
enhanced by overexpressing certain membrane cargo proteins. It may therefore be possible to isolate COPII vesicles using an analogous experimental system to increase
the number of vesicles produced.
Disruption of COPII-mediated transport has a dramatic
effect on protein transport within the cell (6,9,12,44–47).
This demonstrates the importance of the secretory pathway to the normal functioning of the cell. The mutation of a
single residue in Sar1p can prevent it from becoming activated, effectively restricting it to the GDP-bound form and
preventing the budding of vesicles from the ER in mammals, yeast and plants (45,46,48). Similarly, mutation of
another amino acid reduces the GTPase activity of Sar1p,
causing it to be confined to the GTP-bound form. This
mutant GTPase allows vesicles to bud from the ER, but
prevents them from uncoating and fusing with the Golgi
apparatus in yeast (46,49). Although it has been shown that
the GTP-restricted mutant of Sar1p inhibits the export of
proteins from the ER in plants (9,12,45,50), the accumulation
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Protein Traffic at the Plant ER–Golgi Interface
of coated vesicles has yet to be confirmed in this system.
However, it has been shown that in conditions of low expression, a yellow fluorescent protein fusion to Sar1p (GTP) accumulates at ERES in tobacco leaf epidermal cells (6). This may
be taken to mean that the mutant labels a population of
transport intermediates that are not capable of fusion with
the target membrane.
High expression of these mutant GTPases often results in
cell death. COPII-mediated transport can also be inhibited
by the overexpression of Sec12p in both plants and yeast
(6,12,44), which causes the continual recruitment of Sar1p
to the ER membrane and prevents vesicle budding. This
titration effect can be reversed by overexpressing Sar1p,
in order that some activated Sar1p molecules are present
and can form functional vesicles (12,44).
COPI – the Retrograde Counterpart of COPII
The existence of COPI vesicles has been demonstrated in
mammalian (51), yeast (52) and plant cells (11,18,19).
COPI vesicles bud from the cis-cisternae of the Golgi (18)
and mediate traffic from the cis-Golgi back to the ER
(53,54). This is an essential pathway that continually
recycles proteins and lipids from the Golgi to the ER in
order to maintain an equilibrium with COPII transport,
sustaining the balance between the anterograde and the
retrograde transport pathways.
The minimal machinery for the budding of COPI-coated
vesicles consists of coatomer, a stable cytosolic complex
comprising seven subunits a-, b-, b0 -, g-, d-, e- and z-COP
(51), as well as the small GTPase ARF1p (55,56). Homologues of a-, b-, b0 - and g-COP have been isolated from rice
(19), while g-, d- and e-COP have been identified in cauliflower, maize and Arabidopsis (11,18). In addition, ARF1p
homologues from Arabidopsis have also been identified
(39,57). These findings suggested that COPI vesicles
exist in plants, a hypothesis which was confirmed by the
in vitro induction of COPI-coated vesicles from cauliflower
cytosol (18).
COPI coat assembly is initiated by the exchange of GDP
for GTP by ARF1p in a similar manner to that of Sar1p. The
GDP-bound form of ARF1p interacts with p23, a Golgi
membrane protein, through the myristoylated N-terminus
of the GTPase (58). GDP is then exchanged for GTP
through interaction with the GEF (56,59), causing a conformational shift that allows direct interaction of ARF1p
with the membrane. It has been shown that myristoylation
is not required for this direct interaction (60), but rather that
the 17 N-terminal amino acids of mammalian ARF1p form
an amphipathic structure similar to that of Sar1p that can
be inserted between phospholipids in the Golgi membrane
(61,62). The activated, membrane-associated ARF1p
recruits preassembled coatomer from the cytosol (63).
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This induces curvature of the membrane, resulting in the
formation of a nascent vesicle that can then bud from the
membrane.
ARF1p has multiple functions within the cell in addition to
its regulatory role in COPI-mediated transport. These functions appear to be defined by different GEFs that can all
activate ARF1p (64). For example, it has been shown that
ARF1p is involved in the regulation of the BP80-mediated
route to the vacuole in plants (50), probably due to the
interaction of ARF1p with constituents of the clathrin
coat (65–67). The identification of GNOM, an Arabidopsis
ARF-GEF that is localized to the endosomes (68), in conjunction with the data presented by Pimpl et al. (50), supports the hypothesis that the nature of the GEF
determines the action of ARF1p. It is not clear which
GEF is responsible for initiating COPI vesicle formation,
but the most likely candidates are thought to be Gea1p,
Gea2p (69) and ARNO (70). Of these, only the Gea GEFs
have been identified in Arabidopsis (71), suggesting that in
plants at least, Gea may be responsible for the activation of
ARF1p, leading to COPI vesicle formation. Further investigation is required to confirm this, as the existence of an
alternative, plant-specific GEF cannot be ruled out.
Uncoating of COPI vesicles requires GTP hydrolysis to
allow ARF1p to dissociate from the vesicle membrane. A
GAP is involved in this process, and both plants and
animals possess several ARF-GAPs, all of which contain
a conserved catalytic domain (39,72). It is not clear which
of these is responsible for COPI uncoating. Fifteen ARFGAPs have been identified in Arabidopsis, some containing
plant-specific regions. All 15 have homology to one
another, but also exhibit considerable diversity within this
homology (39). This suggests that the different ARF-GAPs
may perform a variety of functions within the cell, which
might be expected given that 12 ARF GTPases as well as
numerous ARF-related GTPases have been identified in
Arabidopsis (39), although their respective functions are
not yet clear. It is also possible that different GAPs can
act on the same ARF and regulate its function in a similar
manner to that of the GEFs.
Disruption of Retrograde Transport Inhibits
Forward Protein Trafficking
The importance of the COPI pathway in maintaining both
retrograde and anterograde transport has been demonstrated in several studies. Brefeldin A (BFA) is a drug that
inhibits several ARF1-GEFs including Gea1p and Gea2p
(59,73), preventing the activation of ARF1p and the subsequent formation of COPI vesicles. The inhibitory effect
of BFA on COPI vesicle formation in plants was demonstrated directly by Pimpl et al. (18) using extracts from
cauliflower. Various other studies have observed the
effects of BFA on the plant-secretory pathway, both in
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terms of its functionality (6,50,74,75) and in terms of its
morphology (76–79). The morphological effects of BFA on
the plant secretory pathway appear to vary depending on
the system studied, the concentration of the drug used
and the exposure time. In tobacco BY-2 cells, prolonged
treatment with 10 mg/mL of BFA results in the sequential
incorporation of Golgi membranes into the ER and the
formation of a so-called BFA compartment composed of
both organelles (76). In contrast, treatment of maize roots
with 100 mg/mL of BFA has a much less pronounced effect
(77), although the same concentration of BFA in tobacco
leaf cells causes the complete disappearance of Golgi
bodies (80). Much lower concentrations of BFA have a
dramatic effect on the function of the secretory pathway,
0.3 mg/mL being sufficient to reduce the secretion of a
marker protein by almost half in tobacco leaf protoplasts
(50). This indicates that COPI transport is required in order
for anterograde protein trafficking to occur. However, BFA
may affect other pathways within the cell (79), causing
complete disruption of the protein transport machinery
and general collapse of protein trafficking.
A more specific disruption of COPI-mediated transport can
be achieved by using mutant forms of ARF1p that are
restricted to either the GTP or GDP-bound form. The inhibition of vesicle budding (GDP-restricted form) or fusion
(GTP-restricted form) both upset the fine balance between
anterograde and retrograde transport, resulting in an inhibition of both pathways (50,78,81,82). These studies have
clearly demonstrated the requirement for retrograde transport in order to maintain anterograde transport. When one
of the pathways is inhibited, it is likely that a build-up of
membrane and vesicle proteins occurs within the target
organelle, leaving a depletion of these important vesicle
components in the donor organelle that eventually prevents transport from occurring.
What is the Signal?
Studies in mammalian cells have shown that certain membrane cargo molecules are selected for incorporation into
COPII transport intermediates and that these are concentrated
in specific domains of the ER, termed ERES (83–87). Signals in
the cytosolic domains of transmembrane proteins are thought
to mediate the recruitment of the COPII coat to the membrane,
thereby inducing vesicle formation. It is not clear whether the
same mechanism operates in plant cells, although the high
degree of homology between the COPII components in plants
and other systems (38) suggests that the signals involved may
be similar. Co-expression of GFP-tagged membrane cargo
proteins and Sar1-YFP has been used to demonstrate the
induction of ERES formation in plants (6), and a recent study
has shown that a plant p24 protein can interact with both COPI
and COPII coat proteins in vitro (88). A similar signalling system
also operates for the assimilation of transmembrane proteins
into COPI vesicles for transport back from the Golgi to the ER in
both mammalian and plant cells (15, 53, 54). However, several
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different types of export signals have been identified in yeast
and mammals (89), and further study is required to demonstrate whether all of these signals are functional in plants or
whether certain transport mechanisms are specific to different
systems.
It has been shown that soluble proteins are exported from
the ER in plants by a COPII-dependent bulk flow mechanism
(12,14). This means that proteins that are intended to remain
in the ER may be exported as far as the Golgi apparatus along
with those travelling to distal locations. The escape of proteins from the ER in this manner is combated by the presence of an H/KDEL motif at the C-terminus of the protein,
which is recognized by a Golgi-localized membrane receptor
(ERD2p) (90). This receptor induces the activation of ARF1p
in mammals by recruiting the GEF (17,91), and thereby
causes the formation of COPI vesicles as described above.
It is not clear whether soluble proteins simply diffuse into
COPII carriers that are created in response to an accumulation of membrane proteins that contain specific signals for
export. It is possible that a receptor for specific soluble
proteins that need to be exported from the ER exists in
plants, and that this could allow a fast-track system of
transport from ER to Golgi. Endoplasmic reticulum-export
receptors (termed Erv14p and Erv29p) for certain soluble
and transmembrane proteins in yeast have been identified
(92–95), although it is not known whether homologues of
these receptors exist in plants.
A di-acidic or di-basic motif in the cytosolic tail of transmembrane cargo proteins is thought to be important in
recruiting the COPII coat in mammals (85,86,96), but
other signals that may be involved have also been identified (89). The type I transmembrane protein ERGIC-53,
which localizes to the ERGIC in mammals, contains a
di-aromatic motif that is reported to be important for its
export from the ER (97). This is similar to the signal identified in plants by Contreras et al. (88), although the function
of this signal has not yet been analysed in vivo in plants. It
has been shown that the length of the transmembrane
domain plays an important role in regulating the final destination of single-spanning membrane proteins in plants
(98), but export signals may play a role in increasing the
rate of export of proteins from the ER. It may also be that
export signals can override the length of the transmembrane domain in determining the destination of the protein.
Much more investigation is evidently needed in plant cells
before any conclusions regarding protein signals required
for ER export can be formed.
Mechanisms of Protein Transfer Between ER
and Golgi in Plants
It is generally assumed that the function of ERES is to select
and concentrate cargo molecules into vesicles for export to
the Golgi (6,84,99–101), although non-vesicular carriers
have been observed for some cargoes in mammalian cells
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Protein Traffic at the Plant ER–Golgi Interface
(102,103). Golgi stacks in plants are found throughout the
cytosol and travel along actin filaments in leaves (74). The
ER tubules in plants are also dynamic and are constantly
forming and breaking connections (104), giving rise to an
extremely motile system (Figure 1). Protein transport may
be challenged by the relatively high mobility of the ER and
Golgi, which could have led to the evolution of specific
mechanisms in plants in order to permit efficient trafficking.
The mobility of the early plant secretory pathway has suggested three possible mechanisms for protein transport
between the ER and the Golgi (summarized in Figure 3).
The first of these postulates that Golgi bodies move along
the ER to reach vesicles budding from ERES, at which
point the cargo molecules can be transferred from the ER
to the Golgi (7). This model was named the ‘vacuumcleaner model’ and was proposed based on the movement
of Golgi bodies along ER membranes. The second model is
referred to as the stop-and-go model (8), and suggests that
there is an as yet unidentified signal present on fixed ERES
that causes Golgi bodies to become transiently detached
from the actin microfilaments, while they acquire cargo
proteins from the ER, after which they would reattach to
the actin and continue to move. However, neither of these
studies included data demonstrating the occurrence of
cargo transport during the postulated interactions of Golgi
with ERES, meaning that no correlation between cargo
transport and Golgi movement has been experimentally
determined.
A more recent investigation (6) utilized advanced in vivo
imaging techniques to demonstrate that ERES are capable
of movement over the ER, and that they are closely linked
to Golgi bodies (Figure 4). This would allow continual transfer of cargo between ER and Golgi, allowing transport to
go on uninterrupted by Golgi movement. The experimental
evidence provided by daSilva et al. (6) demonstrates that the
models postulating fixed ERES and motile Golgi do not necessarily reflect the peripatetic nature of the early secretory pathway in plants. The biological function of the actin-mediated
movement of this system remains to be established, but does
not seem to be related to the transport of cargo molecules
between the ER and the Golgi bodies (6,74). The exact nature
of the connection between the ERES and the Golgi bodies is
also not completely understood. It has been demonstrated
that the activities of the Sar1p-COPII and ARF1p-coatomer
systems jointly serve to form and maintain forward protein
transport to the Golgi bodies, whose components continuously circulate through the ER (6,74). Similarly, ERES are
dynamic structures that exist by virtue of COPI and COPII
A
B
C
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Figure 3: Comparison of the
models for protein transport
between endoplasmic reticulum export sites (ERES) and
Golgi bodies. Schematic representation of the three models
for the transfer of proteins from
the ER to the Golgi apparatus. A)
The vacuum cleaner model. Golgi
bodies move along the ER
surface, picking up cargo. The
entire ER is capable of exporting
proteins. B) The stop-and-go
model. Golgi bodies move along
the ER and stop at fixed ERES,
where protein transport takes
place. After transfer of cargo
from ER to Golgi, the Golgi body
moves to the next site and
collects more cargo. C) The
mobile ERES model. Golgi
bodies and ERES move together,
allowing continual protein
transport between the two
organelles.
273
Hanton et al.
A
B
C
Figure 4: Colocalization of endoplasmic reticulum export sites (ERES) and Golgi bodies. Confocal laser scanning microscope
images showing a tobacco epidermal leaf cell coexpressing ERD2-GFP (A, Golgi marker) and Sar1p-YFP (B, ERES marker). Note the
colocalization of Golgi and ERES (C, merged image; white arrowhead). Size bar ¼ 2 mm.
cycling (6). It is difficult to envisage how Golgi bodies and
ERES can move together, yet not be physically linked. The
movement of the Golgi may be associated with the actin
cytoskeleton via a mechanism that has not yet been investigated, while ERES may be differentiated on the ER, as the
Golgi bodies travel over the ER membranes due to continuous
cycling of COPI and COPII components. It is unclear why the
movement of Golgi stacks through the cell should be necessary, if cargo transport can occur while they are stationary. It
may be that Golgi movement is required for the efficient
transport of proteins to distal locations. Further investigation
is required to determine the precise nature of ER–Golgi transport.
Future Perspectives
Although our knowledge of the protein transport between
the ER and the Golgi in plants has increased manyfold in
recent years, there are several aspects of this process that
remain elusive. In addition to specific subjects discussed
earlier in this review, such as the unidentified GEF involved
in COPI vesicle formation and the reason for Golgi movement on the ER network, there are wider questions to be
addressed.
The direction of vesicles to their destinations is mediated
by SNAREs, which together with various cytosolic factors
form complexes that allow fusion of vesicles with specific
target organelles. Genes encoding 54 different SNAREs
have been identified in Arabidopsis and are localized on
organelles throughout the secretory pathway (105,106).
Six of these SNAREs are found in the ER membrane and
a further nine in the Golgi membranes (106), but it is not
clear whether these proteins exhibit functional redundancy
or if they each have a specific function, perhaps in different
pathways. Small GTPases called Rabs are also involved in
vesicle trafficking. Plants contain 57 Rab GTPases, some
of which have a high homology to mammalian Rabs,
others apparently being unique to plants (107). Although
a few of the Rabs in plants have been studied in some
detail (108–113), little is known about the localization and
274
function of most of these proteins. These are just two
examples of areas that remain poorly understood within
the larger topic of protein transport in plant cells, leaving
plenty of scope for further research in the field.
Current research into the subject of ER to Golgi transport
in plants increases our knowledge of the topic on an
almost daily basis. However, the complexity of the interactions between different proteins and between proteins
and membranes requires yet more investigation. The
advances in confocal microscopy that allow us to observe
the relative rates of transport of different proteins in living
cells provide an ideal tool to complement more traditional
biochemical approaches. Together, these techniques can
provide us with accurate, quantitative information to aid in
our understanding of the pathways in the plant cell.
Acknowledgments
This work was supported by grants awarded to FB from the University of
Saskatchewan, CFI and the Canada Research Chair fund. SLH is also
indebted to the Department of Biology, U of S, for a Post-Doctoral Fellowship. GS is supported by a Graduate College Studies Award and CRC, and
LR by a University of Saskatchewan New Faculty Award. Dr JP Taylor
(Chapel Hill, USA) is thanked for critically reading the manuscript. SLH
thanks Dr J Denecke (Leeds, UK) and L Kriek (Oudenaarde, Belgium) for
continued support and inspiration over the last few years.
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