523
REVIEW / SYNTHÈSE
Protein transport in the plant secretory pathway1
Sally L. Hanton and Federica Brandizzi
Abstract: The study of the plant secretory pathway is a relatively new field, developing rapidly over the last 30 years.
Many exciting discoveries have already been made in this area, but as old questions are answered new ones become apparent. Our understanding of the functions and mechanisms of the plant secretory pathway is constantly expanding, in part
because of the development of new technologies, mainly in bioimaging. The increasing accessibility of these new tools in
combination with more established methods provides an ideal way to increase knowledge of the secretory pathway in
plants. In this review we discuss recent developments in understanding protein transport between organelles in the plant secretory pathway.
Key words: secretory pathway, protein transport, endoplasmic reticulum, Golgi, vacuole.
Résumé : L’étude du cheminement sécrétoire chez les plantes est un champ d’étude relativement nouveau qui s’est développé rapidement au cours des trente dernières années. Ce domaine a déjà connu plusieurs découvertes intéressantes, mais
les réponses à de vieilles questions en soulèvent de nouvelles. Notre compréhension des fonctions et des mécanismes du
sentier sécrétoire des plantes progresse constamment, dû en partie au développement de nouvelles technologies, surtout la
bioimagerie. L’accessibilité accrue à ces nouveaux outils, combinée aux méthodes plus fiables, constitue une voie idéale
pour augmenter nos connaissances du sentier sécrétoire des plantes. Les auteurs discutent les développements récents dans
la compréhension du transport des protéines entre les organelles, via le sentier sécrétoire des plantes.
Mots clés : sentier sécrétoire, transport des protéines, réticulum endoplasmique, Golgi, vacuole.
[Traduit par la Rédaction]
Introduction
The secretory pathway in plants is made up of a series of
organelles specialized for the synthesis, processing, storage,
and degradation of macromolecules (Fig. 1). All eukaryotic
systems share the basic framework of endoplasmic reticulum
(ER), Golgi apparatus, vacuole or lysosome, and plasma
membrane, but plant cells possess some significant peculiarities. For example, the plant Golgi apparatus consists of
multiple Golgi stacks that are motile in the cytoplasm, travelling on an actin network (Boevink et al. 1998), while the
mammalian Golgi is a large, relatively stationary complex.
Plant cells can also contain multiple vacuole types (Paris et
al. 1996; Di Sansebastiano et al. 1998, 2001; Jauh et al.
1998, 1999), specialized for different and sometimes opposite functions. For example, vacuoles specialized for the
storage of proteins have been observed in the same cells as
those that function in protein degradation (Paris et al. 1996;
Di Sansebastiano et al. 1998, 2001). In addition to these
findings, Jauh et al. (1998, 1999) have used tonoplast intrinsic proteins (TIPs) to demonstrate the existence of up to
three types of vacuoles in the same cell, and suggest that
the combination of different TIP isoforms could represent
yet more vacuole types. This complexity is only one of
many that make the plant secretory pathway a fascinating
and challenging field to study.
Protein transport mechanisms: what is the
shuttle?
Transport of cargo molecules through the intricacies of
the secretory pathway is generally believed to occur through
vesicular transport, although other mechanisms may exist for
specific transport steps (Brandizzi et al. 2002a; Hawes and
Satiat-Jeunemaitre 2005). Vesicular transport takes place
through budding of a vesicle from one membrane and subsequent fusion of the vesicle with another. This causes redistribution within the cell not only of the contents of the
vesicle, but also of membranes. Correspondingly, to maintain a balance between organelles, transport must occur
both in the forward (anterograde) and backward (retrograde)
directions. In this way, the secretory pathway maintains its
equilibrium. For example, proteins are exported from the
ER to the Golgi apparatus via COPII-coated carriers, while
Received 18 August 2005. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 26 May 2006.
S.L. Hanton and F. Brandizzi.2 Department of Biology, 112 Science Place, University of Saskatchewan, Saskatoon, SK S7N 5E2,
Canada.
1This
review is one of a selection of papers published in the Special Issue on Plant Cell Biology.
author (e-mail: [email protected]).
2Corresponding
Can. J. Bot. 84: 523–530 (2006)
doi: 10.1139/B05-172
#
2006 NRC Canada
524
Can. J. Bot. Vol. 84, 2006
Fig. 1. Overview of the plant secretory pathway. Schematic representation of the organelles and the transport routes that connect them
within the secretory pathway of plants. Transport routes are numbered as follows: 1, ER protein storage vacuole (PSV) transport, mediated
by a variety of ER-derived vesicles; 2, Golgi–PSV transport, mediated by dense vesicles; 3, COPII-mediated ER–Golgi transport; 4, COPIIindependent ER–Golgi transport; 5, COPI-mediated Golgi–ER transport; 6, transport from trans-Golgi network (TGN) to prevacuolar compartment (PVC)/multivesicular body (MVB)/late endosome via clathrin-coated vesicles (CCVs); 7, recycling route from PVC/MVB/late endosome to TGN; 8, transport from PVC/MVB/late endosome to lytic vacuole; 9, transport from TGN to plasma membrane; 10, endocytic
pathway from plasma membrane to early endosome; 11, transport of endocytosed material from early endosome to PVC/MVB/late endosome; 12, transport of endocytosed material from early endosome to TGN.
other proteins that are required by the ER for various functions are thought to be carried back from the Golgi to the
ER by COPI-coated carriers (reviewed by Hanton et al.
2005a). In addition to these vesicle types, clathrin-coated
vesicles (CCVs) have been implicated in various transport
routes later in the secretory pathway, such as transport from
the trans-Golgi to the prevacuolar compartment (Kirsch et
al. 1994). However, it has also been postulated that direct
connections between organelles may exist. Brandizzi et al.
(2002a) have shown that transient tubular structures can
form between ER and Golgi, and it is possible that similar
structures may be involved in protein transport between
other organelles within the secretory pathway.
Protein synthesis and folding
The first organelle in the secretory pathway is the endoplasmic reticulum (ER). It consists of an intricate system of
membranes, specialized for the synthesis and folding of proteins. In plants, as in all eukaryotic cells, proteins enter the
secretory pathway through translocation across the ER membrane (reviewed by Nicchitta 2002); this can happen either
during (co-translational) or after (post-translational) translation. Specific signals are required for this translocation to
occur; soluble and some membrane-bound proteins possess
an N-terminal hydrophobic region called the signal peptide,
which mediates entry into the ER. On arrival in the ER lumen, the newly synthesized protein interacts with various ER
resident proteins termed chaperones, which assist in correct
folding and prevent inappropriate interactions with other proteins that could result in the formation of insoluble protein ag-
gregates. At this stage the new protein may be glycosylated,
which can lead to further modifications later in the transport
pathway. A complex quality control process is in place in the
ER to prevent misfolded or improperly assembled proteins
from exiting the ER and disrupting the secretory pathway (reviewed by Crofts and Denecke 1998; Ritter and Helenius
2000). Proteins that are irreversibly misfolded may be targeted to the cytoplasm for degradation via the ERAD pathway (Ward et al. 1995; reviewed by McCracken and Brodsky
2003). Characterization of this pathway in plants is in its infancy, but evidence for its existence has been presented by
various groups (Pedrazzini et al. 1997; Brandizzi et al. 2003;
Muller et al. 2005). Those proteins that are correctly folded
and assembled can be exported from the ER to the next stage
in the journey through the secretory pathway.
Export from the endoplasmic reticulum
Various export options are available at the point of exit
from the ER, dependent on the protein in question and the
tissue in which it is expressed. In the case of some storage
proteins, transport from the ER directly to the protein storage vacuole (PSV) has been reported. This is thought to occur via large vesicles containing aggregates of storage
proteins, termed protein bodies PBs, (Levanony et al. 1992),
precursor-accumulating (PAC) vesicles (Hara-Nishimura et
al. 1998), or KDEL-tailed cysteine protease-accumulating
vesicles KVs, (Toyooka et al. 2000), which have been observed at various stages of seed development in different
species. For simplicity, these will be referred to as PAC
vesicles from here on. Other routes to the PSV exist, but
#
2006 NRC Canada
Hanton and Brandizzi
originate at the Golgi apparatus (Hohl et al. 1996). It may be
the case that some proteins require Golgi-mediated modifications prior to trafficking to their final destination, hence
the need for two independent pathways to the same organelle. Indeed, some proteins found in the periphery of the
PAC vesicles bear modifications that indicate passage
through the Golgi (Hara-Nishimura et al. 1998). This suggests that Golgi-derived vesicles may fuse with PAC
vesicles en route to the PSV. It is possible that a similar
transport route exists to mediate transport in the opposite direction, in order that proteins intended for other destinations
but trapped in the aggregates in the PAC vesicles can be retrieved.
Transport of proteins from the ER to the Golgi apparatus
in plants is thought to occur by a COPII-mediated mechanism (reviewed by Hanton et al. 2005a). Considerable evidence for this has been presented, although direct
visualization of COPII-coated vesicular intermediates has
not yet been achieved in plants. COPII vesicles in yeast are
formed by the assembly of a protein coat that stimulates curvature of the ER membrane and eventually causes budding
of the vesicle (Barlowe et al. 1994). Homologues of the
components of the COPII coat have been identified in plants
(d’Enfert et al. 1992; Bar-Peled and Raikhel 1997; Contreras
et al. 2004b), leading to studies in which overexpression or
mutation of regulatory proteins involved in vesicle formation were used to demonstrate the presence and function of
a COPII-mediated transport route in plants (Takeuchi et al.
1998, 2000; Andreeva et al. 2000; Phillipson et al. 2001; daSilva et al. 2004; Yang et al. 2005). In addition to the
mounting evidence for COPII-mediated ER–Golgi transport,
a route from the ER that is independent of COPII has also
been proposed (Törmäkangas et al. 2001), although it is not
yet clear whether this is a widespread phenomenon. Because
Törmäkangas et al. (2001) studied the transport of phytepsin, a vacuolar protein, it may be the case that their proposed COPII-independent pathway is mediated by one of
the vesicle types involved in direct ER–vacuole transport
(Levanony et al. 1992; Hara-Nishimura et al. 1998; Toyooka
et al. 2000). It cannot be ruled out that another route that is
separate from both the COPII and ER to vacuole routes exists, although this has yet to be shown.
COPII transport intermediates are thought to bud from the
ER at specific areas, known as ER export sites (ERES).
These were first visualized in tobacco leaf epidermal cells
by (daSilva et al. 2004), using a fluorescent fusion of the
small GTPase Sar1 (secretion-associated and Ras-related 1).
Sar1 is thought to initiate COPII coat formation by recruiting
structural components to the membrane. Upon co-expression
with membrane-bound cargo molecules, Sar1 distributed to
punctate structures identified as ERES, which appeared as
discrete, motile structures in the ER membrane in close association with Golgi bodies. Fluorescence recovery after
photobleaching (FRAP) analyses showed that the exchange
of protein cargo continued during movement of ERES on
the ER. This has led to the proposal that ER–Golgi transport
is a continuous process that is facilitated by the constant
close proximity of ERES and Golgi bodies. It has also been
suggested that in tobacco BY-2 cells ERES labelled by
Sec13, a COPII coat component, are capable of association
with the Golgi but can also move independently (Yang et
525
al. 2005). It would be interesting to know whether the discrepancies between these studies are due to the expression
systems used, or to the different marker proteins.
Back and forth from the endoplasmic
reticulum
The plant ER has an interesting way of retaining proteins
required for its function; it allows them to leave and then retrieves them from the Golgi apparatus. Export of soluble
proteins from the ER to the Golgi apparatus occurs via a
bulk-flow mechanism (Phillipson et al. 2001). To counteract
their export, ER resident proteins possess retrieval signals.
In the case of soluble proteins, an H/KDEL motif is present
at the extreme C-terminus (Denecke et al. 1992), while
membrane-bound proteins possess either a di-lysine signal
(Benghezal et al. 2000) or an aromatic amino acid-enriched
signal (McCartney et al. 2004) at their C-terminus. The H/
KDEL sequence interacts with the receptor ERD2 in the
cis-Golgi (Lee et al. 1993; Crofts et al. 1999), which in
yeast has been shown to recruit proteins required for formation of retrograde vesicles (Aoe et al. 1997). In plants,
ERD2 appears to be localized across the entire Golgi apparatus (Boevink et al. 1998), and fluorescent fusions to the
receptor are widely used as ER or Golgi marker proteins
(Boevink et al. 1998; Brandizzi et al. 2002b, see also
Fig. 2B). The retrograde vesicles that carry cargo from the
Golgi to the ER are termed COPI and have been identified
and visualized in plants (Movafeghi et al. 1999; Contreras
et al. 2000; Pimpl et al. 2000), although it has not yet
been demonstrated that their function is identical to that
shown for COPI vesicles in other systems. The di-lysine
retrieval motif of membrane proteins interacts directly
with COPI components (Contreras et al. 2004a), leading to
the incorporation of these proteins into vesicles for transport back to the ER.
Although the export of soluble proteins from the ER occurs via bulk flow, it is not clear what mechanism regulates
the export of transmembrane proteins. The length of the
transmembrane domain of type I proteins is known to influence their final destinations within the secretory pathway
(Brandizzi et al. 2002b), but specific signals mediating export also exist. Di-hydrophobic and di-basic signals that
may influence ER export of transmembrane proteins have
been identified (Contreras et al. 2004b; Yuasa et al. 2005),
but have not yet been thoroughly characterized. A more recent publication has shown the existence and function of diacidic ER export motifs in multispanning and type II plant
transmembrane proteins (Hanton et al. 2005b). Interestingly,
the data present in this study also demonstrated that diacidic ER export motifs are dominant over transmembrane
domain length in determining the destinations of type I
transmembrane proteins within the secretory pathway of
plants.
Vacuolar sorting from the Golgi
For those proteins that continue anterograde transport past
the cis-Golgi, many more potential routes exist. Proteins
destined for vacuolar compartments undergo sorting in the
Golgi; it has been shown that segregation of proteins travelling to the lytic vacuole from those intended for the protein
#
2006 NRC Canada
526
Can. J. Bot. Vol. 84, 2006
Fig. 2. The vacuolar sorting receptor BP80 traffics between the Golgi apparatus and the prevacuolar compartment (PVC)/multivesicular
body (MVB)/late endosome. Confocal laser scanning microscope image showing co-expression of spGFP-BP80 (A, a green fluorescent protein (GFP) fusion to the transmembrane domain used by Brandizzi et al. 2002b) with ERD2-YFP (B, Brandizzi et al. 2002a) in a tobacco
leaf epidermal cell. spGFP-BP80 exhibits faint Golgi staining (solid arrowhead), but localizes predominantly at the PVC (open arrowhead).
Note the co-localization of ERD2-YFP with spGFP-BP80 at the Golgi apparatus but not at the PVC or ER (C, merged image). Scale bar =
5 mm.
storage vacuole can begin as early as the cis-Golgi compartment (Hillmer et al. 2001), although it is not clear whether
further sorting steps occur in later Golgi compartments.
Sorting to the lytic vacuole is mediated by a vacuolar sorting receptor termed BP80 or AtELP (Kirsch et al. 1994;
Ahmed et al. 1997). This receptor is thought to recognize
specific signals in the amino acid sequences of soluble cargo
proteins (Kirsch et al. 1996; Ahmed et al. 2000). Upon binding of these sequences to the receptor, the complex is incorporated into clathrin-coated vesicles (CCVs) that transport it
to the prevacuolar compartment (PVC). The PVC has also
been termed multivesicular body (MVB) or late endosome
(Tse et al. 2004), but for simplicity will be referred to as
the PVC in this discussion. It is thought that this incorporation occurs through the interaction of a tyrosine motif in the
cytosolic tail of BP80 with components of the clathrin coat
(Happel et al. 2004). The complex dissociates at the PVC,
likely because of a change in pH (Kirsch et al. 1994), allowing the receptor to recycle to the Golgi apparatus and collect
more cargo molecules. Evidence for this recycling has been
presented by (daSilva et al. 2005) using an Arabidopsis
BP80 homologue, and the distribution of the pea BP80 at
both the Golgi apparatus and PVC supports the hypothesis
(Fig. 2). Although much is known about transport of soluble
vacuolar proteins as far as the PVC, it is not clear how
cargo molecules are transported from the PVC to the vacuole, whether vesicular transport is involved or whether
the PVC itself fuses periodically with the vacuole and is regenerated through the fusion of Golgi-derived vesicles.
Sorting of some proteins to the PSV is also thought to be
receptor mediated, as a transmembrane protein with similarities to BP80, termed PV72, has been identified in the membrane of PAC vesicles (Shimada et al. 1997, 2002) and has
been shown to be capable of binding to storage proteins
(Watanabe et al. 2002). However, more recently, binding of
PV72 to a protease via a signal similar to those recognized
by BP80 was reported (Watanabe et al. 2004). This may reflect a double role in vacuolar sorting, perhaps mediated by
the presence of two binding sites as has been shown for the
yeast vacuolar sorting receptor VPS10 (Jørgensen et al.
1999). However, it may also be the case that the observed
interaction was due to ectopic expression of PV72, a seedspecific protein, in Arabidopsis leaf tissue. Both BP80 and
PV72 may recognize similar sequences, but as they are expressed in different tissues and developmental stages, different cargo proteins and vacuoles are present. This would
prevent missorting of proteases to the PSV or storage proteins to the lytic vacuole in planta.
Transport to and from the plasma membrane
The most distal location in the secretory pathway is the
plasma membrane, from which point soluble proteins can
be secreted into the extracellular space, whereas membraneanchored proteins may act as receptors for hormones and
other regulatory molecules (reviewed by Jürgens and Geldner 2002). It is not known whether transport from the transGolgi network (TGN) to the plasma membrane is achieved
by means of vesicular carriers, as although CCVs have been
identified at both the TGN and the plasma membrane (Lam
et al. 2001), these may be involved in other processes such
as endocytosis. The existence and function of a Rab GTPase
involved in protein transport between the TGN and plasma
membrane have been demonstrated (Zheng et al. 2005), providing an important starting point for studying this area of
the secretory pathway. Specific signals mediating protein
transport to the plasma membrane in plants have not been
identified, and it appears that secretion may be the default
destination for many proteins (reviewed by Jürgens 2004).
Fusions of signal peptides to non-plant proteins such as
phosphinothricine acetyl transferase (PAT) or green fluorescent protein (GFP) results in their secretion from the plant
cell (Denecke et al. 1990; Batoko et al. 2000). This supports
the hypothesis that the extracellular space is the default destination for proteins with no specific sorting signals in leaf
cells. However, it is not clear whether a similar mechanism
exists in tissues exhibiting polarized secretion, such as root
hairs and pollen tubes. Various effector molecules that are
involved in the transport pathway to the plasma membrane
in these tissues have been identified (Preuss et al. 2004; de
#
2006 NRC Canada
Hanton and Brandizzi
Graaf et al. 2005). Additionally, Preuss et al. (2004) have
demonstrated the existence of a compartment between the
TGN and plasma membrane in root hairs that is distinct
from the PVC. It is not yet known whether this compartment
has a function in anterograde or retrograde transport, or possibly in both. Further studies are also required to understand
whether proteins can be specifically targeted to the plasma
membrane.
Endocytosis in plants is a complex field (reviewed by
Holstein 2002; Samaj et al. 2004). Early studies showed evidence for the presence of coated pits and vesicles in plant
cells (Mersey et al. 1982; Joachim and Robinson 1984), suggesting that endocytosis could occur despite the turgor pressure of the central vacuole. Ultrastructural analyses
demonstrated the complexity of the endocytic pathway in
plants, and gave the first evidence of plant endosomes (Pesacreta and Lucas 1985; Fowke et al. 1991). More recently,
fluorescently tagged proteins have been used to shed light
on plant endocytosis. For example, it has been shown that
fluorescent fusions of the plant Rab5 homologues Ara6 and
Ara7 partially co-localize with the styryl dye FM4–64 (Ueda
et al. 2001), which was initially used as a marker for the endosome. However, more recent studies have demonstrated
that Ara7 and other Rab5 homologues also co-localize with
BP80 (Bolte et al. 2004a; Kotzer et al. 2004), which is
known to label the Golgi apparatus and PVC (Paris et al.
1997, see also Fig. 2). In addition to this, FM4–64 has been
shown to label compartments other than the endosome, including the PVC, Golgi apparatus, and vacuolar membrane
(Bolte et al. 2004b). These data indicate the involvement of
compartments other than the endosomes in endocytosis, consistent with a report from Tse et al. (2004), in which the authors propose that the PVC–MVB acts as a late endosome in
addition to its function in vacuolar transport. Evidence from
Ueda et al. (2004) indicates that two populations of endosomes exist in plants, based on co-localization studies with
Ara6 and Ara7; this suggests that both early and late endosomal compartments may be present, in which case cargo
could be transported from the early endosome to the PVC–
MVB–late endosome. This study suggested that Ara6, which
co-localizes with the PVC markers Syp21 and Syp22, is a
marker for the late endosome, while Ara7 may label an earlier endocytic compartment. However, Kotzer et al. (2004)
have shown that Ara7 co-localizes with BP80, which is also
known to label the PVC–late endosome. This discrepancy
may be due in part to the use of different expression systems. Kotzer et al. (2004) expressed Ara7 in tobacco leaf
epidermal cells, whereas the study by Ueda et al. (2004)
used protoplasts from Arabidopsis cell cultures. Further investigations are required to clarify the reasons for such differences.
Concluding remarks and future perspectives
Although our knowledge of the composition and function
of the plant secretory pathway has increased considerably in
recent years, much remains to be discovered. In addition to
the discrepancies discussed previously for ERES and their
Golgi association, or for the endocytic pathway in plants,
other topics remain to be investigated. For example, vesicle
targeting mechanisms in plants form a relatively new area of
527
research. Although 54 different soluble N-ethylmaleimidesensitive factor attachment protein receptors (SNAREs),
which have several functions including vesicle targeting (reviewed by Pratelli et al. 2004), have been identified in Arabidopsis (Sanderfoot et al. 2001; Uemura et al. 2004), in
many cases their functions remain unclear. Similarly, the
small GTPases of the Rab family have been implicated in
vesicle trafficking in plants (reviewed by Molendijk et al.
2004), but most have not been studied in detail. Interestingly, several of the 57 Rab GTPases predicted from the
Arabidopsis genome do not have a mammalian or yeast homologue (Rutherford and Moore 2002), making this a particularly exciting area of study.
The increased usage of live cell imaging techniques and
fluorescence microscopy, and new advances in these technologies (reviewed by Brandizzi et al. 2004) have allowed
the visualization of many aspects of the plant secretory pathway. These noninvasive methods are of great use to cell biologists in many fields, and complement more traditional
approaches. Future studies using both traditional and newer
techniques will provide accurate and quantitative data that
can be interpreted to increase still further our comprehension
of protein transport within the secretory pathway of plants.
Acknowledgements
This work was supported by grants awarded to F.B. from
the University of Saskatchewan, Canada Foundation for Innovation, and the Canada Research Chair fund. S.L.H. is
also indebted to the Department of Biology, University of
Saskatchewan, for a post-doctoral fellowship.
References
Ahmed, S.U., Bar-Peled, M., and Raikhel, N.V. 1997. Cloning and
subcellular location of an Arabidopsis receptor-like protein that
shares common features with protein-sorting receptors of eukaryotic cells. Plant Physiol. 114: 325–336. doi:10.1104/pp.114.1.
325.
Ahmed, S.U., Rojo, E., Kovaleva, V., Venkataraman, S., Dombrowski, J.E., Matsuoka, K., and Raikhel, N.V. 2000. The plant
vacuolar sorting receptor AtELP is involved in transport of
NH(2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J. Cell Biol. 149: 1335–1344. doi:10.1083/
jcb.149.7.1335.
Andreeva, A.V., Zheng, H., Saint-Jore, C.M., Kutuzov, M.A.,
Evans, D.E., and Hawes, C.R. 2000. Organization of transport
from endoplasmic reticulum to Golgi in higher plants. Biochem.
Soc. Trans. 28: 505–512.
Aoe, T., Cukierman, E., Lee, A., Cassel, D., Peters, P.J., and Hsu,
V.W. 1997. The KDEL receptor, ERD2, regulates intracellular
traffic by recruiting a GTPase-activating protein for ARF1.
EMBO J. 16: 7305–7316. doi:10.1093/emboj/16.24.7305.
Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S.,
Salama, N., Rexach, M.F., Ravazzola, M., Amherdt, M., and
Schekman, R. 1994. COPII: a membrane coat formed by Sec
proteins that drive vesicle budding from the endoplasmic reticulum. Cell, 77: 895–907. doi:10.1016/0092-8674(94)90138-4.
Bar-Peled, M., and Raikhel, N.V. 1997. Characterization of AtSEC12 and AtSAR1. Proteins likely involved in endoplasmic reticulum and Golgi transport. Plant Physiol. 114: 315–324.
doi:10.1104/pp.114.1.315.
Batoko, H., Zheng, H.Q., Hawes, C., and Moore, I. 2000. A rab1
GTPase is required for transport between the endoplasmic reti#
2006 NRC Canada
528
culum and golgi apparatus and for normal golgi movement in
plants. Plant Cell, 12: 2201–2218. doi:10.1105/tpc.12.11.2201.
Benghezal, M., Wasteneys, G.O., and Jones, D.A. 2000. The Cterminal dilysine motif confers endoplasmic reticulum localization to type I membrane proteins in plants. Plant Cell, 12:
1179–1201. doi:10.1105/tpc.12.7.1179.
Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A.,
and Hawes, C. 1998. Stacks on tracks: the plant Golgi apparatus
traffics on an actin/ER network. Plant J. 15: 441–447. doi:10.
1046/j.1365-313X.1998.00208.x.
Bolte, S., Brown, S., and Satiat-Jeunemaitre, B. 2004a. The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J. Cell Sci. 117:
943–954. doi:10.1242/jcs.00920.
Bolte, S., Talbot, C., Boutte, Y., Catrice, O., Read, N.D., and Satiat-Jeunemaitre, B. 2004b. FM-dyes as experimental probes for
dissecting vesicle trafficking in living plant cells. J. Microsc.
214: 159–173. doi:10.1111/j.0022-2720.2004.01348.x.
Brandizzi, F., Snapp, E.L., Roberts, A.G., Lippincott-Schwartz, J.,
and Hawes, C. 2002a. Membrane protein transport between the
endoplasmic reticulum and the Golgi in tobacco leaves is energy
dependent but cytoskeleton independent: evidence from selective
photobleaching. Plant Cell, 14: 1293–1309. doi:10.1105/tpc.
001586.
Brandizzi, F., Frangne, N., Marc-Martin, S., Hawes, C., Neuhaus,
J.M., and Paris, N. 2002b. The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell, 14: 1077–1092. doi:10.1105/tpc.
000620.
Brandizzi, F., Hanton, S., daSilva, L.L., Boevink, P., Evans, D.,
Oparka, K., Denecke, J., and Hawes, C. 2003. ER quality control can lead to retrograde transport from the ER lumen to the
cytosol and the nucleoplasm in plants. Plant J. 34: 269–281.
doi:10.1046/j.1365-313X.2003.01728.x.
Brandizzi, F., Irons, S.L., Johansen, J., Kotzer, A., and Neumann,
U. 2004. GFP is the way to glow: bioimaging of the plant endomembrane system. J. Microsc. 214: 138–158. doi:10.1111/j.
0022-2720.2004.01334.x.
Contreras, I., Ortiz-Zapater, E., Castilho, L.M., and Aniento, F.
2000. Characterization of Cop I coat proteins in plant cells. Biochem. Biophys. Res. Commun. 273: 176–182. doi:10.1006/bbrc.
2000.2918.
Contreras, I., Ortiz-Zapater, E., and Aniento, F. 2004a. Sorting signals in the cytosolic tail of membrane proteins involved in the
interaction with plant ARF1 and coatomer. Plant J. 38: 685–
698. doi:10.1111/j.1365-313X.2004.02075.x.
Contreras, I., Yang, Y., Robinson, D.G., and Aniento, F. 2004b.
Sorting signals in the cytosolic tail of pPlant p24 proteins involved in the interaction with the COPII coat. Plant Cell Physiol. 45: 1779–1786. doi:10.1093/pcp/pch200.
Crofts, A.J., and Denecke, J. 1998. Calreticulin and calnexin in
plants. Trends Plant Sci. 3: 396–399. doi:10.1016/S13601385(98)01312-0.
Crofts, A.J., Leborgne-Castel, N., Hillmer, S., Robinson, D.G.,
Phillipson, B., Carlsson, L.E., Ashford, D.A., and Denecke, J.
1999. Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell, 11: 2233–2248.
doi:10.1105/tpc.11.11.2233.
daSilva, L.L., Snapp, E.L., Denecke, J., Lippincott-Schwartz, J.,
Hawes, C., and Brandizzi, F. 2004. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory
units in plant cells. Plant Cell, 16: 1753–1771. doi:10.1105/tpc.
022673.
daSilva, L.L., Taylor, J.P., Hadlington, J.L., Hanton, S.L., Snow-
Can. J. Bot. Vol. 84, 2006
den, C.J., Fox, S.J., Foresti, O., Brandizzi, F., and Denecke, J.
2005. Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell, 17:
132–148. doi:10.1105/tpc.104.026351.
de Graaf, B.H., Cheung, A.Y., Andreyeva, T., Levasseur, K., Kieliszewski, M., and Wu, H.M. 2005. Rab11 GTPase-regulated
membrane trafficking is crucial for tip-focused pollen tube
growth in tobacco. Plant Cell, 17: 2564–2579. doi:10.1105/tpc.
105.033183.
Denecke, J., Botterman, J., and Deblaere, R. 1990. Protein secretion in plant cells can occur via a default pathway. Plant Cell,
2: 51–59. doi:10.1105/tpc.2.1.51.
Denecke, J., De Rycke, R., and Botterman, J. 1992. Plant and
mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J. 11: 2345–
2355.
d’Enfert, C., Gensse, M., and Gaillardin, C. 1992. Fission yeast and
a plant have functional homologues of the Sar1 and Sec12 proteins involved in ER to Golgi traffic in budding yeast. EMBO J.
11: 4205–4211.
Di Sansebastiano, G.P., Paris, N., Marc-Martin, S., and Neuhaus,
J.M. 1998. Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting
pathway. Plant J. 15: 449–457. doi:10.1046/j.1365-313X.1998.
00210.x.
Di Sansebastiano, G.P., Paris, N., Marc-Martin, S., and Neuhaus,
J.M. 2001. Regeneration of a lytic central vacuole and of neutral
peripheral vacuoles can be visualized by green fluorescent proteins targeted to either type of vacuoles. Plant Physiol. 126: 78–
86. doi:10.1104/pp.126.1.78.
Fowke, L.C., Tanchak, M.A., and Galway, M.E. 1991. Ultrastructural cytology of the endocytic pathway in plants. In Endocytosis, exocytosis and vesicle traffic in plants. Edited by
C.R. Hawes, J.O.D. Coleman, and D.E. Evans. Cambridge University Press, Cambridge. pp. 15–40.
Hanton, S.L., Bortolotti, L.E., Renna, L., Stefano, G., and Brandizzi, F. 2005a. Crossing the divide - transport between the endoplasmic reticulum and Golgi apparatus in plants. Traffic, 6:
267–277. doi:10.1111/j.1600-0854.2005.00278.x.
Hanton, S.L., Renna, L., Bortolotti, L.E., Chatre, L., Stefano, G.,
and Brandizzi, F. 2005b. Diacidic motifs influence the export of
transmembrane proteins from the endoplasmic reticulum in plant
cells. Plant Cell, 17: 3081–3093. doi:10.1105/tpc.105.034900.
Happel, N., Honing, S., Neuhaus, J.M., Paris, N., Robinson, D.G.,
and Holstein, S.E. 2004. Arabidopsis mu A-adaptin interacts
with the tyrosine motif of the vacuolar sorting receptor VSRPS1. Plant J. 37: 678–693. doi:10.1111/j.1365-313X.2003.
01995.x.
Hara-Nishimura, I., Shimada, T., Hatano, K., Takeuchi, Y., and
Nishimura, M. 1998. Transport of storage proteins to protein
storage vacuoles is mediated by large precursor-accumulating
vesicles. Plant Cell, 10: 825–836 . doi:10.1105/tpc.10.5.825.
Hawes, C., and Satiat-Jeunemaitre, B. 2005. The plant Golgi apparatus–going with the flow. Biochim. Biophys. Acta, 1744: 465–
480.
Hillmer, S., Movafeghi, A., Robinson, D.G., and Hinz, G. 2001.
Vacuolar storage proteins are sorted in the cis-cisternae of the
pea cotyledon Golgi apparatus. J. Cell Biol. 152: 41–50. doi:10.
1083/jcb.152.1.41.
Hohl, I., Robinson, D.G., Chrispeels, M.J., and Hinz, G. 1996.
Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J. Cell Sci. 109: 2539–2550.
Holstein, S.E. 2002. Clathrin and plant endocytosis. Traffic, 3:
614–620. doi:10.1034/j.1600-0854.2002.30903.x.
#
2006 NRC Canada
Hanton and Brandizzi
Jauh, G.Y., Fischer, A.M., Grimes, H.D., Ryan, C.A., Jr., and Rogers, J.C. 1998. delta-Tonoplast intrinsic protein defines unique
plant vacuole functions. Proc. Natl. Acad. Sci. USA, 95: 12995–
12999. doi:10.1073/pnas.95.22.12995.
Jauh, G.Y., Phillips, T.E., and Rogers, J.C. 1999. Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant
Cell, 11: 1867–1882. doi:10.1105/tpc.11.10.1867.
Joachim, S., and Robinson, D.G. 1984. Endocytosis of cationic ferritin by bean leaf protoplasts. Eur. J. Cell Biol. 34: 212–216.
Jørgensen, M.U., Emr, S.D., and Winther, J.R. 1999. Ligand recognition and domain structure of Vps10p, a vacuolar protein sorting receptor in Saccharomyces cerevisiae. Eur. J. Biochem. 260:
461–469. doi:10.1046/j.1432-1327.1999.00176.x.
Jürgens, G. 2004. Membrane trafficking in plants. Annu. Rev. Cell
Dev. Biol. 20: 481–504. doi:10.1146/annurev.cellbio.20.082503.
103057.
Jürgens, G., and Geldner, N. 2002. Protein secretion in plants: from
the trans-Golgi network to the outer space. Traffic, 3: 605–613.
doi:10.1034/j.1600-0854.2002.30902.x.
Kirsch, T., Paris, N., Butler, J.M., Beevers, L., and Rogers, J.C.
1994. Purification and initial characterization of a potential plant
vacuolar targeting receptor. Proc. Natl. Acad. Sci. USA, 91:
3403–3407.
Kirsch, T., Saalbach, G., Raikhel, N.V., and Beevers, L. 1996. Interaction of a potential vacuolar targeting receptor with aminoand carboxyl-terminal targeting determinants. Plant Physiol.
111: 469–474. doi:10.1104/pp.111.2.469.
Kotzer, A.M., Brandizzi, F., Neumann, U., Paris, N., Moore, I., and
Hawes, C. 2004. AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J. Cell Sci. 117:
6377–6389. doi:10.1242/jcs.01564.
Lam, B.C., Sage, T.L., Bianchi, F., and Blumwald, E. 2001. Role
of SH3 domain-containing proteins in clathrin-mediated vesicle
trafficking in Arabidopsis. Plant Cell, 13: 2499–2512. doi:10.
1105/tpc.13.11.2499.
Lee, H.I., Gal, S., Newman, T.C., and Raikhel, N.V. 1993. The
Arabidopsis endoplasmic reticulum retention receptor functions
in yeast. Proc. Natl. Acad. Sci. USA, 90: 11433–11437.
Levanony, H., Rubin, R., Altschuler, Y., and Galili, G. 1992. Evidence for a novel route of wheat storage proteins to vacuoles. J.
Cell Biol. 119: 1117–1128. doi:10.1083/jcb.119.5.1117.
McCartney, A.W., Dyer, J.M., Dhanoa, P.K., Kim, P.K., Andrews,
D.W., McNew, J.A., and Mullen, R.T. 2004. Membrane-bound
fatty acid desaturases are inserted co-translationally into the ER
and contain different ER retrieval motifs at their carboxy termini.
Plant J. 37: 156–173. doi:10.1111/j.1365-313X.2004.01949.x.
McCracken, A.A., and Brodsky, J.L. 2003. Evolving questions and
paradigm shifts in endoplasmic-reticulum-associated degradation
(ERAD). Bioessays, 25: 868–877. doi:10.1002/bies.10320.
Mersey, B.G., Fowke, L.C., Constabel, F., and Newcomb, E.H.
1982. Preparation of a coated vesicle-enriched fraction from
plant cells. Exp. Cell Res. 141: 459–463. doi:10.1016/00144827(82)90235-X.
Molendijk, A.J., Ruperti, B., and Palme, K. 2004. Small GTPases
in vesicle trafficking. Curr. Opin. Plant Biol. 7: 694–700.
doi:10.1016/j.pbi.2004.09.014.
Movafeghi, A., Happel, N., Pimpl, P., Tai, G.H., and Robinson,
D.G. 1999. Arabidopsis Sec21p and Sec23p homologs. Probable
coat proteins of plant COP-coated vesicles. Plant Physiol. 119:
1437–1446. doi:10.1104/pp.119.4.1437.
Muller, J., Piffanelli, P., Devoto, A., Miklis, M., Elliott, C., Ortmann, B., Schulze-Lefert, P., and Panstruga, R. 2005. Conserved
ERAD-Like quality control of a plant polytopic membrane protein. Plant Cell, 17: 149–163. doi:10.1105/tpc.104.026625.
529
Nicchitta, C.V. 2002. A platform for compartmentalized protein
synthesis: protein translation and translocation in the ER. Curr.
Opin. Cell Biol. 14: 412–416. doi:10.1016/S0955-0674(02)
00353-8.
Paris, N., Stanley, C.M., Jones, R.L., and Rogers, J.C. 1996. Plant
cells contain two functionally distinct vacuolar compartments.
Cell, 85: 563–572. doi:10.1016/S0092-8674(00)81256-8.
Paris, N., Rogers, S.W., Jiang, L., Kirsch, T., Beevers, L., Phillips,
T.E., and Rogers, J.C. 1997. Molecular cloning and further characterization of a probable plant vacuolar sorting receptor. Plant
Physiol. 115: 29–39. doi:10.1104/pp.115.1.29.
Pedrazzini, E., Giovinazzo, G., Bielli, A., de Virgilio, M., Frigerio,
L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A., and Vitale, A.
1997. Protein quality control along the route to the plant vacuole. Plant Cell, 9: 1869–1880. doi:10.1105/tpc.9.10.1869.
Pesacreta, T.C., and Lucas, W.J. 1985. Presence of a partiallycoated reticulum in angiosperms. Protoplasma, 125: 173–184.
doi:10.1007/BF01281235.
Phillipson, B.A., Pimpl, P., daSilva, L.L., Crofts, A.J., Taylor, J.P.,
Movafeghi, A., Robinson, D.G., and Denecke, J. 2001. Secretory
bulk flow of soluble proteins is efficient and COPII dependent.
Plant Cell, 13: 2005–2020. doi:10.1105/tpc.13.9.2005.
Pimpl, P., Movafeghi, A., Coughlan, S., Denecke, J., Hillmer, S.,
and Robinson, D.G. 2000. In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell, 12: 2219–2236.
doi:10.1105/tpc.12.11.2219.
Pratelli, R., Sutter, J.U., and Blatt, M.R. 2004. A new catch in the
SNARE. Trends Plant Sci. 9: 187–195. doi:10.1016/j.tplants.
2004.02.007.
Preuss, M.L., Serna, J., Falbel, T.G., Bednarek, S.Y., and Nielsen,
E. 2004. The Arabidopsis Rab GTPase RabA4b localizes to the
tips of growing root hair cells. Plant Cell, 16: 1589–1603.
doi:10.1105/tpc.021634.
Ritter, C., and Helenius, A. 2000. Recognition of local glycoprotein
misfolding by the ER folding sensor UDP-glucose:glycoprotein
glucosyltransferase. Nat. Struct. Biol. 7: 278–280.
Rutherford, S., and Moore, I. 2002. The Arabidopsis Rab GTPase
family: another enigma variation. Curr. Opin. Plant Biol. 5:
518–528. doi:10.1016/S1369-5266(02)00307-2.
Samaj, J., Baluska, F., Voigt, B., Schlicht, M., Volkmann, D., and
Menzel, D. 2004. Endocytosis, actin cytoskeleton, and signaling.
Plant Physiol. 135: 1150–1161. doi:10.1104/pp.104.040683.
Sanderfoot, A.A., Kovaleva, V., Bassham, D.C., and Raikhel, N.V.
2001. Interactions between syntaxins identify at least five
SNARE complexes within the Golgi/prevacuolar system of the
Arabidopsis cell. Mol. Biol. Cell, 12: 3733–3743.
Shimada, T., Kuroyanagi, M., Nishimura, M., and Hara-Nishimura,
I. 1997. A pumpkin 72-kDa membrane protein of precursor-accumulating vesicles has characteristics of a vacuolar sorting receptor. Plant Cell Physiol. 38: 1414–1420.
Shimada, T., Watanabe, E., Tamura, K., Hayashi, Y., Nishimura,
M., and Hara-Nishimura, I. 2002. A vacuolar sorting receptor
PV72 on the membrane of vesicles that accumulate precursors
of seed storage proteins (PAC vesicles). Plant Cell Physiol. 43:
1086–1095. doi:10.1093/pcp/pcf152.
Takeuchi, M., Tada, M., Saito, C., Yashiroda, H., and Nakano, A.
1998. Isolation of a tobacco cDNA encoding Sar1 GTPase and
analysis of its dominant mutations in vesicular traffic using a
yeast complementation system. Plant Cell Physiol. 39: 590–599.
Takeuchi, M., Ueda, T., Sato, K., Abe, H., Nagata, T., and Nakano,
A. 2000. A dominant negative mutant of sar1 GTPase inhibits
protein transport from the endoplasmic reticulum to the Golgi
apparatus in tobacco and Arabidopsis cultured cells. Plant J. 23:
517–525. doi:10.1046/j.1365-313x.2000.00823.x.
#
2006 NRC Canada
530
Törmäkangas, K., Hadlington, J.L., Pimpl, P., Hillmer, S., Brandizzi, F., Teeri, T.H., and Denecke, J. 2001. A vacuolar sorting
domain may also influence the way in which proteins leave the
endoplasmic reticulum. Plant Cell, 13: 2021–2032. doi:10.1105/
tpc.13.9.2021.
Toyooka, K., Okamoto, T., and Minamikawa, T. 2000. Mass transport of proform of a KDEL-tailed cysteine proteinase (SH-EP)
to protein storage vacuoles by endoplasmic reticulum-derived
vesicle is involved in protein mobilization in germinating seeds.
J. Cell Biol. 148: 453–464. doi:10.1083/jcb.148.3.453.
Tse, Y.C., Mo, B., Hillmer, S., Zhao, M., Lo, S.W., Robinson,
D.G., and Jiang, L. 2004. Identification of multivesicular bodies
as prevacuolar compartments in Nicotiana tabacum BY-2 cells.
Plant Cell, 16: 672–693. doi:10.1105/tpc.019703.
Ueda, T., Yamaguchi, M., Uchimiya, H., and Nakano, A. 2001.
Ara6, a plant-unique novel type Rab GTPase, functions in the
endocytic pathway of Arabidopsis thaliana. EMBO J. 20: 4730–
4741. doi:10.1093/emboj/20.17.4730.
Ueda, T., Uemura, T., Sato, M.H., and Nakano, A. 2004. Functional differentiation of endosomes in Arabidopsis cells. Plant J.
40: 783–789. doi:10.1111/j.1365-313X.2004.02249.x.
Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K.,
and Sato, M.H. 2004. Systematic analysis of SNARE molecules
in Arabidopsis: dissection of the post-Golgi network in plant
cells. Cell Struct. Funct. 29: 49–65. doi:10.1247/csf.29.49.
Ward, C.L., Omura, S., and Kopito, R.R. 1995. Degradation of
CFTR by the ubiquitin-proteasome pathway. Cell, 83: 121–127.
doi:10.1016/0092-8674(95)90240-6.
Can. J. Bot. Vol. 84, 2006
Watanabe, E., Shimada, T., Kuroyanagi, M., Nishimura, M., and
Hara-Nishimura, I. 2002. Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S
albumin. J. Biol. Chem. 277: 8708–8715. doi:10.1074/jbc.
M109346200.
Watanabe, E., Shimada, T., Tamura, K., Matsushima, R., Koumoto,
Y., Nishimura, M., and Hara-Nishimura, I. 2004. An ER-localized form of PV72, a seed-specific vacuolar sorting receptor,
interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves. Plant Cell Physiol. 45: 9–17. doi:10.1093/pcp/
pch012.
Yang, Y.D., Elamawi, R., Bubeck, J., Pepperkok, R., Ritzenthaler,
C., and Robinson, D.G. 2005. Dynamics of COPII vesicles and
the Golgi apparatus in cultured Nicotiana tabacum BY-2 cells
provides evidence for transient association of Golgi stacks with
endoplasmic reticulum exit sites. Plant Cell, 17: 1513–1531.
doi:10.1105/tpc.104.026757.
Yuasa, K., Toyooka, K., Fukuda, H., and Matsuoka, K. 2005.
Membrane-anchored prolyl hydroxylase with an export signal
from the endoplasmic reticulum. Plant J. 41: 81–94. doi:10.
1111/j.1365-313X.2004.02279.x.
Zheng, H., Camacho, L., Wee, E., Batoko, H., Legen, J., Leaver,
C.J., Malho, R., Hussey, P.J., and Moore, I. 2005. A Rab-E
GTPase mutant acts downstream of the Rab-D subclass in biosynthetic membrane traffic to the plasma membrane in tobacco
leaf epidermis. Plant Cell, 17: 2020–2036. doi:10.1105/tpc.105.
031112.
#
2006 NRC Canada