Download Traffic between the plant endoplasmic reticulum and Golgi

Traffic between the plant endoplasmic reticulum and Golgi
apparatus: to the Golgi and beyond
Loren A Matheson1, Sally L Hanton1 and Federica Brandizzi1,2
Significant advances have been made in recent years that have
increased our understanding of the trafficking to and from
membranes that are functionally linked to the Golgi apparatus
in plants. New routes from the Golgi to organelles outside the
secretory pathway are now being identified, revealing the
importance of the Golgi apparatus as a major sorting station in
the plant cell. This review discusses our current perception of
Golgi structure and organization as well as the molecular
mechanisms that direct traffic in and out of the Golgi.
Addresses
1
Department of Biology, 112 Science Place, University of
Saskatchewan, Saskatoon, Saskatchewan S7N 5E2, Canada
2
Department of Energy, Plant Research Laboratory, Michigan State
University, East Lansing, Michigan 48824, USA
Corresponding author: Brandizzi, Federica ([email protected])
Current Opinion in Plant Biology 2006, 9:601–609
This review comes from a themed issue on
Cell biology
Edited by Laurie G Smith and Ulrike Mayer
Available online 28th September 2006
1369-5266/$ – see front matter
# 2006 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2006.09.016
(for ‘secretion associated, ras-related protein1’) and two
structural heterodimers, Sec23/24 and Sec13/31. The
nature of the transport intermediates that carry cargo
from the ER to the Golgi is unknown; however, there
is speculation surrounding the existence of closed compartments, such as vesicles or tubules, and the possibility
that export occurs via a direct connection (reviewed by
[1]). Various protein motifs that mediate the export of
transmembrane proteins from the ER have been identified ([5,6,7]; Figure 1), but it remains to be shown
whether these signals recruit or are recruited by the
cytosolic COPII components. No signals have been discovered for soluble cargo intended for forward transport
in the secretory pathway; it appears that a bulk flow
mechanism transports these proteins [8].
Proteins move from the Golgi to the ER via retrograde
transport. In contrast to the anterograde route, the retrograde route depends on signals that mediate the transport
of transmembrane and soluble proteins (Figure 1; [9,10]).
The retrograde route is thought to be mediated by COPI,
which consists of the small GTPase ADP-RIBOSYLATION FACTOR1 (ARF1) plus a heptameric complex of
structural coat components, homologs of most of which
have been identified in plants (reviewed by [11]). Inhibition of COPI function results in impaired ER export and
disruption of the ERES [4], indicating the possibility of a
role for ARF1 in anterograde transport in addition to its
role in retrograde transport.
Introduction
A central function has been attributed to the Golgi
apparatus in the plant secretory pathway, directing
traffic to and from such diverse organelles as the endoplasmic reticulum (ER), lytic and storage vacuoles, and
the plasma membrane. More recently, the Golgi apparatus has been implicated in the transport of proteins to
‘non-conventional’ secretory organelles, such as peroxisomes and chloroplasts. In this review, we discuss recent
findings in plants that contribute to our understanding of
the efficient trafficking between the ER and Golgi, and
beyond.
Protein transport between ER and Golgi
The first step in the transport of proteins through the
secretory pathway is generally the transfer from the ER to
the Golgi apparatus (reviewed by [1]). This occurs by
means of a coat protein complex II (COPII)-mediated
mechanism at specialized areas known as ER export sites
(ERES), from which anterograde transport to the Golgi
apparatus is thought to occur [2–4]. COPII is composed
of three cytosolic components: the small GTPase Sar1
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Is the Golgi apparatus a sub-compartment of
the ER?
As in mammalian and yeast systems, the plant Golgi
apparatus receives exported proteins from the ER via
ERES. However, questions regarding the association of
ERES and the Golgi apparatus in plants have been raised.
It appears that ERES and Golgi bodies have a continuous
association in tobacco leaf epidermal cells [2,4]; whereas
in tobacco BY-2 (Bright Yellow-2) suspension cells, multiple ERES can associate transiently with a single Golgi
stack [3]. It is not clear whether these variations are due
solely to the differences in the expression systems or
rather to the use of different ERES markers. A fluorescent
fusion of the Arabidopsis Sec24 COPII component has
been localized to the peri-Golgi area in tobacco leaf
epidermal cells [2]. This fusion has a similar distribution
in Arabidopsis leaf epidermal cells (LA Matheson, F
Brandizzi, unpublished; Figure 2), supporting the evidence that ERES track in close proximity with Golgi
bodies in leaves (Figure 2b; [2]). Although a physical link
between the ER and Golgi apparatus cannot be defined
Current Opinion in Plant Biology 2006, 9:601–609
602 Cell biology
Figure 1
Protein motifs that are important for anterograde and retrograde cargo recognition in plant cells. In anterograde transport, (a) di-acidic motifs are
important for forward transport of multi-spanning, type I and type II membrane proteins out of the ER, as shown by ER export studies with
Golgi and ER-resident membrane proteins [5]. The involvement of (b) a dibasic motif has been demonstrated in the ER export of a type II
membrane-spanning prolyl hydroxylase [7]. (c) A dihydrophobic signal in the cytosolic domain of a type I membrane-spanning p24 protein has
been shown to interact with a COPII coat component, Sec23 in vitro, although this is only possible when a dilysine motif adjacent to the
dihydrophobic motif is mutated [6]. It is thought that both signals cooperate to recruit the COPI coat, whereas only the dihydrophobic motif is
able to interact with Sec23. (d) Anterograde ER–Golgi transport of soluble proteins is thought to occur solely through a passive bulk-flow
mechanism [8] because no specific motif has been identified. (e) There is a possibility that as-yet-undiscovered signals within soluble proteins
direct their anterograde transport. In retrograde transport, (f) transmembrane proteins are selected for transport from the Golgi to the ER by a
dilysine motif at the carboxyl terminus of the cytosolic tail that interacts with components of the COPI coat [9,51]. (g) An additional motif for Golgi
to ER transport was identified in FATTY ACID DESATURASE 2 (FAD2), which possesses a carboxy-terminal sequence that is enriched in
aromatic residues and that is necessary for the ER retention of FAD2 [10]. (h) Retrograde Golgi–ER transport of soluble proteins is achieved by
carboxy-terminal H/KDEL signals that are recognized by the receptor ER RETENTION DEFECTIVE 2 (ERD2) [52]. (i) Other signals might exist that direct
the transport of soluble protein back to the ER from the Golgi.
conclusively by light microscopy, these data suggest that
the ER, ERES and Golgi apparatus in leaf epidermal cells
could exist and migrate in a continuous fashion. This is
supported by recent evidence showing that Golgi bodies
move with, not over, the surface of the ER [12]. In fact,
the Golgi apparatus in plants not only might be physically
linked to the ER but also might be a specialized subcompartment of the ER formed through continuous
membrane flow [4,13].
Additional evidence that the Golgi apparatus is a functional
extension of the ER comes from data indicating that Golgi
membrane integrity depends on active exchange of cargo
between the Golgi and ER. Treatment of cells with the
fungal metabolite brefeldin A (BFA), a known inhibitor of
ARF1 activation, leads to redistribution of Golgi membrane proteins to the ER [2,14]. Similarly, when ER-toGolgi transport is inhibited by a dominant negative mutant
Current Opinion in Plant Biology 2006, 9:601–609
of ARF1 that is impaired in GTP/GDP exchange, Golgi
membrane proteins are absorbed into the ER and the
punctate distribution of Sec23 and Sec24, as well as that
of Sar1, at the ERES is lost [2,4].
The first described function of ARF proteins in protein
transport was to facilitate the formation of COPI-coated
vesicles on the cis-Golgi. Although studies in plant cells are
behind those in other systems, plant homologs of b- and gCOP have been shown to co-localize with ARF1 at the
plant Golgi apparatus, indicating the possibility of a direct
interaction [15]. Studies in tobacco epidermal cells confirmed that ARF1 and e-COP are dynamically associated
with the Golgi apparatus. These studies also suggested that
the different cycling rates of ARF1 and coatomer on and off
the Golgi membranes might be essential to generate a
functional COPI domain (Figure 3; [4]). Furthermore, they
showed that active COPI-mediated transport is necessary
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Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 603
Figure 2
ER export sites in Arabidopsis leaf epidermal cells. (a–d) Confocal images of Arabidopsis leaf epidermal cells expressing either (a) the ER export
site marker YFP–Sec24 alone, or (b) YFP–Sec24 with (c) a Golgi marker, ERD2-green fluorescent protein (GFP). (d) Merged image of (b) and (c).
YFP–Sec24 localizes at punctate structures (arrowheads) when it is expressed alone or in combination with a Golgi marker [4]. Scale bar
represents 10 mm. (e–g) Time-lapse of a cell co-expressing YFP–Sec24 and ERD2–GFP presented in vertical display as a single channel for (e)
ERD2–GFP, (f) YFP-Sec24 and (g) as merged images. The arrowhead indicates an ERES that is moving with a Golgi stack. Time is shown in
seconds at the top right of each image. Scale bar represents 5 mm.
for the maintenance of ERES integrity. This implies that
the distribution of Golgi membrane protein is maintained
by the balanced action of COPI and COPII transport routes
between the ER and Golgi, lending support to the hypothesis that the Golgi apparatus is a sub-compartment of the
ER that is dependent on secretion [13]. The ARF1–coatomer complex is most likely indirectly required for anterograde trafficking out of the ER because of its role in
recycling components that are essential for differentiation
of the ER export domains [4]. However, this remains to be
proven experimentally in plants.
The Golgi apparatus is continuously
remodelled
Organelles are typically distinguished from one another by
their enzymatic content, which is specified by cellular
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function. However, the boundaries between the ER and
Golgi are unclear. These organelles undergo continuous
exchange of material, and so the existence of each emerges
as a product of dynamically controlled membrane trafficking and sorting processes. To maintain Golgi apparatus
integrity, cells must manage complex membrane trafficking to and from the ER and maintain secretory membrane
flow through the stack. Recent studies have provided
evidence of constant remodeling of both the membranous
and soluble components of the Golgi apparatus (Figure 3).
Using fluorescence recovery after photobleaching (FRAP)
techniques, it has been shown that e-COP, a subunit of
coatomer, associates transiently with the Golgi membranes
(Figure 3; [4]). In addition, Golgi membrane
proteins continuously cycle between ER and Golgi, as
demonstrated by photobleaching experiments using
Current Opinion in Plant Biology 2006, 9:601–609
604 Cell biology
Figure 3
Localization and dynamics of different classes of Golgi components. Fluorescence recovery after photobleaching (FRAP) experiments show that
peripheral and integral membrane components of the Golgi apparatus, such as eCOP, full length GRIP (FLGRIP) and ERD2, continuously cycle on
and off Golgi membranes. (a) Schematic representation of Golgi-localized peripheral (eCOP and FLGRIP) or integral membrane (ERD2)
proteins. It should be noted that the predicted number of membrane-spanning domains and membrane orientation of ERD2 in plants remain to
be confirmed experimentally. (b) The pre-bleach image shows tobacco epidermal cells expressing the YFP chimeras before the bleaching event.
Golgi stacks (arrow) were photobleached, and the recovery of fluorescence to the area was monitored. Images at representative time points
post-bleach (t1/2 and full recovery) are shown. Time of acquisition post-bleach is shown at the bottom left of each frame. The cytosolic pools of eCOP–
YFP and YFP–FLGRIP give a high level of background fluorescence, which is absent in cells expressing ERD2–YFP. Scale bars represent 2 mm.
ER-RETENTION DEFECTIVE 2 (ERD2)–yellow
fluorescent protein (YFP) (Figure 3) and Golgi enzymes
that are distributed in different cisternae [16]. As evidence
of the rapid cycling of various soluble and membrane
components of the Golgi apparatus increases, the question
remains as to how the Golgi apparatus manages to preserve
Current Opinion in Plant Biology 2006, 9:601–609
a highly organized structure and whether this structure can
be considered an entity unto itself.
Golgins, a diverse family of Golgi-resident proteins, have
been implicated in the formation of a matrix that might be
responsible for the structure of the Golgi apparatus [17].
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Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 605
Golgins have large coiled-coil domains and an ability to
bind effector molecules, including activated GTP-binding proteins of the Ras-protein families [17]. Perhaps the
best-characterized function of golgins in mammalian and
yeast systems is their role in membrane-tethering events
[17]. Models of Golgi structure and function derived from
yeast and mammalian cells cannot be directly extrapolated to plant cells because of the innate differences
between these cellular systems. However, these studies
have provided a starting point in the search for possible
factors that might contribute to the unique structure and
motile nature of the Golgi apparatus in plants.
The Arabidopsis genome encodes several homologs of
mammalian and yeast peripheral and integral membrane
golgins [18]. The first membrane-spanning plant golgin
to be cloned and characterized was AtCASP (for CCAAT
displacement protein alternatively spliced product), but
its functions at the Golgi apparatus have yet to be
explored [19]. Many peripheral golgins share a 40amino-acid carboxy-terminal GRIP domain (named for
the first four mammalian proteins in which it was found:
golgin-97, RanBP2a, Imh1p, and p230/golgin-245), which
is sufficient for trans-Golgi targeting. Recently, fluorescent fusions of the GRIP domain of a peripheral Arabidopsis golgin (AtGRIP) and of the full-length AtGRIP
were shown to localize at the Golgi apparatus, and to cycle
continuously on and off the Golgi (Figure 3; [20–22]).
The mechanism by which AtGRIP is recruited to the
Golgi apparatus has also been elucidated, revealing a
cellular role for the small GTPase ARL1 (ARF-like
GTPase 1) [20,22]. Subsequent studies have provided
experimental evidence that ARL1 localizes to the plant
Golgi apparatus and that two key residues (F51 and Y81)
are responsible for its role in recruiting the AtGRIP
domain [22]. The function of GRIP at the plant Golgi
apparatus, and further interactions between GTPases and
golgins in plants, remains to be discovered. It is possible
that these so-called matrix proteins have a role in stabilizing the stack by maintaining efficient vesicular traffic to,
through and from the Golgi apparatus.
Post-Golgi transport
Transport beyond the Golgi apparatus can reach a variety of
different locations in plant cells. These destinations
include the lytic and protein storage vacuoles (PSV), to
which cargo molecules are transported by established
routes (reviewed by [23,24]). New data continually increase
our knowledge of these routes, particularly with regard to
receptor trafficking [25,26,27,28]. It has been shown that
ARF1 is involved in the transport of proteins to the lytic
vacuole, in addition to its role in COPI-mediated transport
[29]. A fluorescent fusion of ARF1 localizes to the Golgi
apparatus as well as to additional punctate structures that
detach from the Golgi apparatus [4,30]. The function of
these structures has not yet been elucidated, but they might
represent the trans-Golgi network (TGN) [4,31], endocytic
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compartments [30], or precursors of the prevacuolar compartment. Microscopy supports the existence of a TGNlike structure at the plant Golgi [31,32]. Earlier studies have
also pointed to the existence of subdomains of the TGN
[33]. The golgin AtGRIP is thought to localize at the transGolgi, although its localization at the TGN has not been
excluded [20]. It has yet to be shown whether disrupting the
correct targeting of AtGRIP to the Golgi by mutating
essential residues (i.e. Y717 or K719; [22]) can affect the
integrity of the plant TGN or its subdomains, as has been
demonstrated in mammalian cells [34,35].
Recent studies have shown that the Golgi apparatus plays
a role in transporting some proteins to the chloroplast
[36,37], although import routes directly from the cytosol
are better characterized and might be more numerous
(reviewed by [38]). Similar Golgi-mediated pathways
have yet to be established for mitochondrial proteins.
The early secretory pathway has also been implicated in
protein transport to peroxisomes, although it is not clear
whether the Golgi apparatus is involved. Again, cytosolic
import pathways into peroxisomes have been identified
for several proteins [39,40], but the ER also appears to
play a prominent role in the transport of proteins into
peroxisomes. It appears that several peroxisomal proteins
accumulate in subdomains of the ER [41–43], although it
is not clear whether these proteins are en route to the
peroxisome or whether they contain specific signals that
mediate dual targeting to the peroxisome and ER. This
phenomenon has been observed for a protein disulphide
isomerase in the green alga Chlamydomonas reinhardtii,
which is targeted to the chloroplast and ER [44]. Similar
mechanisms could exist in higher plants, possibly allowing dual targeting to different combinations of organelles.
A transport route from the peroxisome to the ER has also
been identified [45], indicating the potential for protein
cycling between the two organelles. No evidence has yet
been presented to implicate the Golgi apparatus in ERto-peroxisome transport, suggesting that proteins might
be transported from ER to peroxisomes independently of
the Golgi apparatus. Similar Golgi-independent routes
have been suggested for the transport of storage proteins
to the PSV [46,47] and might exist between the ER and
other organelles, although this has yet to be shown.
Conclusions and future perspectives
Recent studies have resulted in a marked increase in our
understanding of the structure and functions of the Golgi
apparatus in plants. However, there are many questions to
be answered (Figure 4). An increased understanding of
the functions and interactions of golgins and ARF proteins might provide new insight into the structure and
function of the Golgi apparatus, cargo transport, the
relationship between the Golgi stack and the ER, and
the unique patterns of movement displayed by individual
Golgi stacks. For example, the cycling of the GTPase
ARF1 between the GDP-bound form in the cytosol and
Current Opinion in Plant Biology 2006, 9:601–609
606 Cell biology
Figure 4
Summary of the established and unidentified transport routes within the early secretory pathway in plants. Because of the unique nature of the
early secretory pathway in plants, many questions remain under investigation. They are divided into four main categories, represented in the diagram
by the four colored letters. (a) ER to Golgi communication: the relationship between ERES and Golgi bodies is the subject of an ongoing debate
because distinct theories on the dynamics of transport have been presented on the basis of studies in different model systems [2,3]. Recent data
have suggested that Golgi bodies move with the ER — at the same rate and in the same direction [12] — and the secretory unit model has
proposed a continuum between the ER, ERES and the Golgi apparatus [2]. If the ER and Golgi are physically linked, can the Golgi be considered
a unique entity? The possibility exists that the Golgi apparatus might be a specialized sub-compartment of the ER that is dependent on secretion.
(b) Cargo export: ER to Golgi transport is mediated by COPII, although the nature of the transport intermediates is unclear. How do COPII
components interact with membrane protein motifs to initiate transport? Are there specific signals for the anterograde transport of soluble proteins
or is it mediated solely by bulk-flow? Retrograde transport is thought to be controlled by COPI, as it is in mammalian and yeast systems, although
this has yet to be shown directly in plants. There are several unidentified potential transport routes, including Golgi–mitochondria,
Golgi–peroxisome, ER–lytic vacuole and ER–peroxisome routes. (c) Structure and organization: how do the ER and Golgi apparatus interact yet
maintain specific organelle identities? Two plant golgins have been identified and characterized [19–22]. Do other golgins exist in plants and
what functional role do they play within the Golgi apparatus? Does ARF1 have an additional functional role at the level of structural organization of
Current Opinion in Plant Biology 2006, 9:601–609
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Traffic to and from the Golgi apparatus Matheson, Hanton and Brandizzi 607
the GTP-bound form on the Golgi membranes has been
observed in living cells [4]. It is not clear how ARF1 is
specifically recruited to Golgi membranes. It is possible
that Golgi-associated guanine nucleotide exchange factors (GEFs) recruit ARF1 to the Golgi membrane; however, evidence from mammalian cells suggests that other
membrane proteins such as SNAREs (soluble N-ethylmaleimide-sensitive factor attachment protein receptors)
could serve indirectly as ARF1 receptors [48]. It could
also be that membrane-bound golgins, such as CASP,
recruit ARF1 to the Golgi apparatus.
On a larger scale, questions can be raised regarding the
number of Golgi bodies in plant cells. The Golgi apparatus in plants exists as individual stacks that double in
number during cell division [49], but the mechanisms for
this have not yet been identified. Does this increase in the
number of Golgi bodies occur as a result of the division of
existing Golgi stacks or are they synthesized de novo from
ER membranes? A sterol regulatory element binding
protein (SREBP)-based mechanism has been described
in mammals that links endomembranes and gene transcription: translocation of a regulatory protein to the
nucleus via the Golgi results in the activation of a target
gene [50]. It is possible that a similar system might
operate in plants, allowing the coordination of a nuclear
response with the activity of the early secretory pathway.
Finally, we pose the question as to whether the Golgi is a
necessary organelle in the plant cell. The existence of
multiple Golgi-independent protein transport pathways
that originate in the ER and traffic cargo molecules to a
variety of destinations indicates that the Golgi, although
important to the secretory pathway, might not be as vital
to the whole cell, at least in the short-term. This hypothesis is supported by the fact that BFA-mediated disruption of the Golgi apparatus does not result in immediate
cell death, and that removal of the drug can allow regeneration of functional Golgi bodies [14].
The question remains: is the Golgi an essential part of the
cell that mediates many varied processes or is it a dispensable subdomain of the ER, without which the cell
can survive for extended periods of time? Our perception
of the Golgi apparatus has been modified considerably
because of recent findings that have proposed additional
functions for this intriguing organelle. This trend is likely
to continue as the field endeavors to resolve the myriad of
unanswered questions.
Acknowledgements
We apologize to colleagues whose work could only be covered by reference
to reviews and discussion in other papers because of space limitations. This
work was supported by the Canada Research Chair Program and the Natural
Science and Engineering Research Council of Canada and the Department
of Energy, Michigan State University.
References and recommended reading
Papers of particular interest, published within the annual period of
review, have been highlighted as:
of special interest
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(Figur 4 Legend Continued ) the Golgi apparatus? It has been suggested that ARF1 might be involved in recruiting components that are involved in the
Golgi matrix in mammalian cells [48]. Does ARF1 behave in a similar fashion in plant cells? How is ARF1 recruited to the Golgi apparatus? What is
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Current Opinion in Plant Biology 2006, 9:601–609
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The authors studied protein flow within the membrane of the ER as it is
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over an actin scaffold. Tracking of Golgi movement demonstrated that
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