Download Holding it all together? Candidate proteins for the plant Golgi matrix

Holding it all together? Candidate proteins for the plant
Golgi matrix
Maita Latijnhouwers1, Chris Hawes2 and Claudine Carvalho2
A combination of electron microscopy and fluorescence
microscopy has provided us with a global picture of the
structure of the plant Golgi apparatus. However, the
components that shape this structure remain elusive. In
other organisms, members of the golgin family of coiled-coil
proteins are essential for Golgi structure and organisation.
Putative Arabidopsis and rice homologues of some golgin
family members can be identified using database searches.
Likewise, the heterogeneous group of multi-subunit-tethering
complexes is responsible for crucial transport steps that affect
Golgi structure and cisternal organisation in animals and
yeasts. The Arabidopsis genome harbours possible
homologues for the majority of the subunits of these
complexes, suggesting that they also operate in the plant
kingdom.
Addresses
1
Cell-to-Cell Communication programme, Scottish Crop Research
Institute, Invergowrie, Dundee DD2 5DA, UK
2
Research School of Biological & Molecular Sciences, Oxford
Brookes University, Headington, Oxford OX3 BP, UK
Corresponding author: Latijnhouwers, Maita
([email protected])
Current Opinion in Plant Biology 2005, 8:1–8
This review comes from a themed issue on
Cell Biology
Edited by Patricia C Zambryski and Karl Oparka
1369-5266/$ – see front matter
# 2005 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2005.09.014
The structure and function of the plant Golgi
The Golgi apparatus in plants plays crucial roles in the
glycosylation of proteins and lipids and in the production
of polysaccharides for cell wall biosynthesis. Proteins are
imported from the endoplasmic reticulum (ER), entering
the Golgi apparatus on the cis side. On their way through
the organelle to its opposite face, the trans Golgi, proteins
and lipids may be processed by Golgi-resident enzymes
that modify attached glycan chains [2,3]. The products
are sorted and packaged into vesicles for transport to the
vacuole or to the plasma membrane. This sorting mainly
occurs in the trans Golgi or the trans-Golgi network
(TGN), a vesiculo-tubular structure that has a certain
degree of autonomy and is located at the trans-side of the
Golgi. The TGN may also receive vesicles travelling in
the opposite direction, which enter the Golgi apparatus
from endosomal compartments, although this pathway
has to date received very little attention in plants.
In mammalian cells the Golgi stacks are very often
arranged end-to-end around the nucleus. In plant cells,
however, the Golgi apparatus consists of stacks of cisternae that are distributed throughout the cytoplasm. The
use of fluorescent marker proteins has revealed that, in
some cell types, the stacks are highly motile and move
along ER strands [4–6]. Actin-depolymerising drugs have
been used to show that Golgi distribution and motility is
actin-dependent [4]. The structural relationship between
the ER and the Golgi apparatus in plants is still a matter
for debate [6–8], but a key difference between the Golgi
of plants and other eukaryotes is that the ER and Golgi
often appear connected in plants [8–10]. For that reason,
we could predict that a set of (structural) proteins is
involved in maintaining this close ER–Golgi relationship
in plants.
Introduction
How the plant Golgi apparatus can maintain its structure
of discrete, motile and polarised stacks of membranebounded cisternae is an intriguing question. The Golgi
matrix of mammalian cells has been characterised in
much more detail than that in plants. Its most notable
element is the existence of a class of coiled-coil proteins,
called golgins, which define the structure of the Golgi and
also play a role in the tethering of vesicles. In this review,
these proteins are taken as the starting point in the search
for possible factors that give the plant Golgi its structure
and organisation. At the same time, it is worth reiterating a
note of caution: models of Golgi structure and function
that are derived from mammalian and yeast systems must
be interpreted with care and investigated experimentally
before applying them to plants [1].
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COPLBI 295
What holds the stacks together?
Each Golgi stack consists of five to eight cisternae [3],
depending on cell type. The existence of some sort of
surrounding matrix that holds these together has been
postulated [1,3]. Earlier electron microscopy studies identified a zone surrounding plant Golgi stacks from which
ribosomes were absent, suggesting the presence of a
matrix that has a higher density than the surrounding
cytoplasm [11]. Although the existence and nature of this
so-called ribosome-exclusion zone remains to be determined, it could be envisaged that it is involved in maintaining the integrity of the stack. A second component of
the Golgi apparatus that probably assists in holding the
cisternae together are ‘intercisternal elements’. These
electron-opaque, fibrous elements have a regular strucCurrent Opinion in Plant Biology 2005, 8:1–8
2 Cell biology
ture and are mainly detected between the trans cisternae
of plant Golgi stacks (Figure 1; [3,12]).
associated with Arabidopsis Golgi and might be required
to tether the stacks to the actin cytoskeleton [19].
In the mammalian Golgi apparatus, the first indication
that cisternal adhesion is dependent on proteinaceous
substances came from in vitro studies of stacks from rat
liver cells. Golgi stacks disintegrated into individual
cisternae after treatment with proteinase K, chymotrypsin, subtilisin or elastase but remained intact after treatment with carboxypeptidase, trypsin or amylase [13].
Detergent extraction of Golgi stacks leaves an insoluble
structure that is referred to as the Golgi ‘ghost’ or ‘skeleton’. In animal cells, this skeleton has been reported to
contain cytoskeletal components, including spectrin and
ankyrin-like proteins. Spectrins are structural proteins
that form networks parallel to membrane surfaces that
maintain the structure and integrity of membrane sheets
[14]. The introduction of dominant negative isoforms of
the Golgi-located, spectrin-like protein Syne-1 caused the
collapse of the Golgi complex and the perturbation of
various trafficking pathways [15,16]. It remains to be
firmly established whether cytoskeletal proteins have a
structural role in plant Golgi organisation. One report has,
however, identified a spectrin-like protein that is associated with Golgi vesicles in an alga [17]. More recently, a
kinesin 13a protein has been reported to be associated
with Golgi stacks in the cortical cytoplasm of Arabidopsis
leaves, but this protein is not responsible for movement
[18]. An actin-associated protein, KATAMARI1, is also
Golgins
Recently, a family of proteins called golgins that are
important for maintaining the integrity of the Golgi
apparatus has been identified in animals and yeast
(Figure 2). Golgins are large proteins with extensive
coiled-coil domains [20–22]. The coiled-coil is a very
common protein motif that consists of heptad repeats,
which form amphipatic a-helices that twist into a supercoil and form a long rod-like structure [23]. Long coiledcoil proteins often have structural roles; for example, in
nuclear organisation, as scaffolding proteins in centrosomes, or as part of the cytoskeleton [24]. Some golgins
have carboxy-terminal domains, such as the GRIP and the
GRAB (GRIP-related Arf-binding) domains, that show
significant conservation across kingdoms. The GRAB
domain was recently shown to bind activated ADP-ribosylation factor 1 (ARF1) [25], a small GTPase that is
involved in, amongst numerous other processes, the formation of coat protein complex I (COPI)-coated vesicles
[26]. The GRIP domain binds a related GTPase called
ARF-like1 (ARL1), which is located on the trans Golgi or
TGN [27–29]. The interaction of these domains with
their respective GTPases is required for these golgins to
be recruited to the Golgi.
An indication that golgins have an important structural
role in the Golgi apparatus was postulated by Seemann
Figure 1
Electron micrograph showing a Golgi stack from a tobacco root meristem cell, high-pressure frozen and freeze-substituted. The micrograph
shows intercisternal elements (arrows) between the trans-cisternae. The scale bar represents 100 nm. Reproduced from [1] with permission
from Blackwell Publishing.
Current Opinion in Plant Biology 2005, 8:1–8
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Candidate proteins for the plant Golgi matrix Latijnhouwers, Hawes and Carvalho 3
Figure 2
Golgins and multi-subunit tethering complexes in the mammalian Golgi apparatus. The diagram shows the distribution of known golgins and
Golgi-related multi-subunit tethering complexes in the secretory and endosomal pathway in mammalian cells. The golgins are presented in
normal black type and the multi-subunit tethering complexes are in bold. The underlined golgins have a putative homologue in plants.
et al. [30]. These authors showed that the mammalian
golgins GM130, p115 and Giantin were present in the
Golgi ‘skeleton’ that remained after treatment with Brefeldin A, a fungal metabolite that causes most Golgiresident enzymes to be transferred to the ER [30].
Further evidence comes from observations that Golgi
stacks in a cell line with undetectable levels of the golgin
GM130 are disassembled into dispersed vesicles when
incubated at higher temperatures (39.5 8C), and can be
rescued by transfection with GM130 [31]. Depletion of
another golgin, Golgin-84, results in the fragmentation of
the Golgi ribbon into separate stacks [32]. The golgins
GM130 and Golgin-45 bind to proteins called Golgi
reassembly stacking proteins (GRASPs), presumably as
a way to associate these golgins with the membrane [22].
GRASPs are required for the stacking of Golgi cisternae
after mitosis, as was shown in experiments using the
injection of antibodies that recognise these proteins
[33,34].
Apart from their role in the stacking of cisternae, golgins
are important in vesicle tethering. This is the initial
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attachment of vesicles to target membranes, a process
that takes place before fusion. Tethering is suggested to
provide the first level of recognition and specificity to
vesicle binding and to accelerate vesicle fusion by the
machinery involving SNARE proteins [35,36]. It is presently hypothesised that Giantin acts in a complex
together with p115 and GM130 to form a long tether
that binds COPI vesicles to cis Golgi membranes
[21,22,37]. Another, more recently discovered golgin
tether, is composed of the mammalian golgins Golgin84 and CASP [38]. This tether bound COP1 vesicles
that contain cargo that is different from that of the p115bound COPI vesicles, possibly reflecting the different
trafficking processes catalysed by these different tethers
[38].
The two functions of golgins, in the tethering and the
stacking of cisternae, might be intimately related, given
that correct vesicle binding and fusion are central to
maintaining the size and composition of cisternae. It
has also been suggested that golgins hold cisternae
Current Opinion in Plant Biology 2005, 8:1–8
4 Cell biology
together by forming bridges or networks between them
[21], in much the same way as they form tethers between
vesicles and cisternae. Interestingly, Saccharomyces cerevisiae has at least five members of the golgin family but its
Golgi apparatus is unstacked, implying that golgins perform essential roles beyond cisternal stacking.
Golgins in plants
Given the importance of golgins in mammals and yeasts,
it is possible to envisage a significant role for proteins of
this family in plant Golgi. Conventional BLAST searches
of both the Arabidopsis and rice genomes using the
mammalian golgins as query sequences detected proteins
that have sequence similarity to a subset of the mammalian or yeast golgins (Table 1). Because the coiled-coil
domains show very low levels of sequence conservation in
this class of proteins, most of the possible plant homologues were identified on the basis of the presence of
other conserved domains.
The first 250 amino acids of the golgin p115 share 40%
identity (63% similarity) with the same region in the
Arabidopsis protein that is encoded by open reading frame
(ORF) At3 g27530. This region forms a globular head to
the rod-like structure that is formed by the central region
of the protein [39] and binds a guanine-nucleotide
exchange factor (GEF) for ARF [40], which might explain
the high degree of sequence conservation in this area. In
the proteins that are encoded by the ORFs At3 g61570
and At2 g46180, carboxy-terminal GRAB domains were
identified that share 32% and 30% identity (62% and 64%
similarity), respectively, to the GRAB domain of the
mammalian golgin GMAP210 [25]. These two proteins
share 70% amino acid identity. The existence of two
genes that encode GRAB domain proteins in the Arabidopsis genome is likely to be a result of a recent gene
duplication event, as the rice genome only contains one
such gene. A carboxy-terminal domain of the protein that
is encoded by ORF At5 g66030 is 50% identical to the
GRIP domain of Golgin-97. A fusion protein that consists
of the this putative Arabidopsis GRIP domain and green
fluorescent protein (GFP) was recently reported to colocate with the Golgi marker a-Mannosidase I on Golgi
stacks in transformed tobacco protoplasts [41], showing
that this domain targets the Golgi. Hence, this protein
was named AtGRIP. A full-length AtGRIP–GFP fusion
protein also co-located with Golgi markers and is thought
to target the far trans face of the Golgi (Figure 3). Moreover, the GRIP domain of AtGRIP interacts directly with
an Arabidopsis homologue of the small GTPase ARL1
(Arf-like 1) [42].
Proteins that are encoded by two ORFs (At1 g18190 and
At2 g19950) were identified as possible golgins on the
basis of sequence similarity between their carboxy-termini and the carboxy-terminal transmembrane (TM)
region of Golgin-84 (46% and 50% identity in the TM
region, respectively) [24,43]. Similarly, the carboxyl ter-
Table 1
Human and yeast golgins and their potential homologues from Arabidopsis and rice.
Human
Yeast
Arabidopsis 1
Rice 1
Domains other than coiled-coil
Reference(s)
p115
GMAP210
Uso1
RUD3
LOC Os12 g35360
LOC Os08 g29730
–
GRAB
[52]
[25,53,54]
Golgin-97
Golgin-245
GCC88
GCC185
Golgin-84
Imh1
–
–
–
–
At3 g27530
At3 g61570
At2 g46180
At5 g66030 (AtGRIP) 2
N.D. 2
N.D. 2
N.D. 2
At2 g19950
GRIP
GRIP
GRIP
GRIP
TM
[55]
[56,57]
[58]
[58]
[24,59]
CASP
Giantin
GM130
TMF
Bicaudal-D1/2
Golgin-45
Golgin-67
Golgin-160
COY1
–
–
Sgm1
–
–
–
–
At1 g18190
At3 g18480 (AtCASP)
N.D.
N.D.
At1 g79830
N.D.
N.D.
N.D.
N.D.
TM
TM
–
–
–
–
–
–
[24,43,44]
[37]
[60,61]
[45,62]
[63]
[64]
[65]
[61,66]
LOC Os07
N.D. 2
N.D. 2
N.D. 2
LOC Os03
LOC Os03
LOC Os03
LOC Os04
LOC Os03
N.D.
N.D.
LOC Os05
N.D.
N.D.
N.D.
N.D.
g28940 2
g54130
g54110 3
g54110 3
g55810
g50300
g48620
N.D. = not detected.
Arabidopsis locus names: The Arabidopsis Information Resource (TAIR; www.Arabidopsis.org). Rice locus identifiers: TIGR Rice Genome
Annotation (http://www.tigr.org/tdb/e2k1/osa1/index.shtml).
2
The family of GRIP domain proteins, comprising four golgin-like proteins in mammals, is represented by only one protein in Arabidopsis and rice.
3
This gene is split into two loci in the rice genome of Oryza sativa spp. japonica cv. Nipponbare. A retrotransposon is inserted in the gene towards the
carboxy-terminus, leaving the gene in two parts. There are, however, sequences in the TIGR expressed sequence tag (EST) database that represent
the full-length gene (NP906530 in TIGR or AK067648 in National Center for Biotechnology Information [NCBI]).
1
Current Opinion in Plant Biology 2005, 8:1–8
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Candidate proteins for the plant Golgi matrix Latijnhouwers, Hawes and Carvalho 5
Figure 3
Tobacco epidermal cell stably expressing the transmembrane domain of
rat sialyl transferase fused to monomeric Red Fluorescent Protein
(shown in red). The transiently expressed fusion protein AtGRIP–GFP
(shown in green) labels one end of the stacks. In the same study, it was
shown that the cis Golgi t-SNARE Memb11–YFP labels the opposite
end, indicating that AtGRIP–GFP is a trans Golgi protein. Reproduced
from [42], courtesy of Blackwell Publishing.
minus of the protein encoded by ORF At3 g18480 shows
homology to the TM domain of human CASP (58%
identity) [24,43]. The similarity between these two proteins is, however, also evident in other regions of the
protein. The membrane topologies of At1 g18190, At2
g19950 and At3 g18480 resemble those of Golgin-84 and
of CASP, which possess large amino-terminal cytoplasmic
domains and very short carboxy-terminal tails in the Golgi
cisternal lumen. When fused to GFP, the protein encoded
by ORF At3 g18480 does indeed locate to the Golgi, and
the carboxy-terminal 124 amino acids of this protein are
sufficient to target GFP to the Golgi stacks. Moreover,
mutagenesis of a conserved tyrosine in the TM domain of
this protein disrupted the Golgi targeting of this protein
[44]. The golgin TMF has no conspicuous domains other
than the coiled-coil regions, the most carboxy-terminal of
which was reported to bind the small GTPase Rab6 [45]
and is conserved in the yeast homologue Sgm1p. The
carboxy-terminus of the protein encoded by ORF At1
g79830 shows clear similarity to the Rab6-binding region
in TMF and Sgm1p [45].
Although the Arabidopsis and rice ORFs that are presented in Table 1 were identified only on the basis of
sequence similarity with mammalian golgins, they might
prove very valuable in characterising plant Golgi organisation. Of course, the plant Golgi apparatus differs sigwww.sciencedirect.com
nificantly from its yeast and mammalian counterparts, and
studying the roles of golgins might reveal alternative,
plant-specific functions. In some cases, it was not possible
to detect any proteins with significant protein similarity in
the Arabidopsis or rice genomes. Of these, Giantin and
GM130 probably play a role in binding COPI vesicles to
the cis cisternae. Of course, these golgins might be
specific for mammalian cells, or alternatively, their
sequence might have diverged to such an extent in plants
that they are no longer recognised in searches using
conventional BLAST algorithms. Another protein family
that is particularly notable for its apparent absence in
plant Golgi are the GRASP stacking proteins, whose
interaction with the golgins is largely responsible for
the organisation of mammalian Golgi. Again, this might
reflect the differences in the organisation of these two
types of Golgi. The plant genome might contain additional, plant-specific, golgin-type proteins that lack
detectable similarity to mammalian or yeast golgins,
although it will be a more arduous task to find such
proteins. To do so, organelle-specific proteomics might
be a very useful strategy [46].
Tethering protein complexes
Long coiled-coil proteins are not the only vesicle-tethering factors in eukaryotic cells. Several multi-subunit
protein complexes have been identified in mammals
and yeast in the past decade that are involved in the
recognition and tethering of vesicles, and probably in
other aspects of vesicle trafficking. In addition, they
might perform certain structural roles in the Golgi apparatus. The complexes, called conserved oligomeric Golgi
(COG) and transport protein particles (TRAPP I and
TRAPPII), facilitate ER–Golgi and intra-Golgi transport.
DSL1 is important for Golgi–ER retrograde transport,
and the Golgi-associated retrograde protein (GARP) complex accommodates retrograde transport from endosomes
to the Golgi/TGN (reviewed in [36,47,48]). The Exocyst
and HOPS (Class C) complexes are tethering complexes
that are involved in post-Golgi trafficking events and will
not be discussed further. In contrast to the coiled-coil
tethers, which bind exclusively to activated GTP-bound
GTPases, some of the multi-subunit complexes have
GEF activity and are involved in the activation of Rab
proteins. On the basis of this, Sacher et al. [49] hypothesised that multi-subunit tethering complexes act in the
initial phase of the vesicle recognition and docking process to activate small GTPases such as Rab proteins.
Activated Rabs might subsequently recruit coiled-coil
tethers to facilitate vesicle binding and SNAREs (soluble
N-ethylmaleimide-sensitive factor attachment protein
[SNAP] receptors) to complete the fusion process [49].
The COG complex consists of eight subunits that are
divided into two sub-complexes. Each of the subunits
possesses short regions that are predicted to be involved
in coiled-coil formation. Arabidopsis homologues can be
recognised for each of the COG subunits, with levels of
Current Opinion in Plant Biology 2005, 8:1–8
6 Cell biology
Table 2
Golgi tethering complex subunits from human and yeast and their possible homologues from Arabidopsis.
Complex
COG
TRAPP I
TRAPP II
GARP
Dsl1
Name of human subunit
Name of yeast subunit
COG1
COG2
COG3
COG4
COG5
COG6
COG7
COG8
TRAPPC3
TRAPPC1
TRAPPC8
TRAPPC2
TRAPPC4
TRAPPC5
TRAPPC6A
TRAPPC7
TRAPPC9
TRAPPC10
–
Vps52
Vps53
Vps54
ZW10
RINT-1
BNIP1
COG1
COG2
COG3
COG4
COG5
COG6
COG7
COG8
Bet3
Bet5
Trs85
Trs20
Trs23
Trs31
Trs33
Trs65
Trs120
Trs130
Vps51
Vps52
Vps53
Vps54
Dsl1
Tip20
Sec20
Possible Arabidopsis
homologue 1
Size in amino acids 1
At5
At4
At1
At4
At1
At1
At5
At5
At5
At1
At5
At1
At5
At5
At3
g16300
g24840
g73430
g01400
g67930
g31780
g51430
g11980
g54750
g51160
g16280
g80500
g02280
g58030
g05000
N.D.
N.D.
N.D.
N.D.
At1 g71300
At1 g50500
At4 g19490
N.D.
N.D.
N.D.
% identity to
corresponding
human protein 2
1068
756
745
1117
832
706
836
569
186
169
1265
81
141
195
173
20
27
34
21
29
31
23
32
51
37
20
28
34
46
29
701
798
1054
26
24
20
1
Arabidopsis locus names and protein sizes according to protein annotation by The Arabidopsis Information Resource (TAIR; www.Arabidopsis.org).
2
Percentage protein identity was determined using ClustalW (Pôle BioInformatique Lyonnais; http://pbil.ibcp.fr/htm/index.php).
amino acid identity ranging between 20% and 34%
(Table 2). Fusion proteins between the putative Arabidopsis COG5 and COG8 homologues (ORFs At1 g67930
and At5 g11980, respectively) and GFP located to Golgi
stacks in tobacco epidermal cells (M Latijnhouwers et al.,
unpublished), substantiating the significance of the
BLAST approach to identify homologues of mammalian
Golgi transport proteins. Similarly, the TRAPP I complex
appears to be conserved in Arabidopsis, as proteins that
have sequence similarity to each of the seven subunits
were detected (amino-acid identity ranging between 20%
and 51%). The TRAPP II complex contains the same
subunits as TRAPP I but has three additional subunits
(TRAPPC7, TRAPPC9 and TRAPPC10). No proteins
with similarity to these three subunits have been identified in Arabidopsis, suggesting that this complex only
exists as one isoform in plants.
At least three of the four subunits of the GARP complex
seem to be conserved in Arabidopsis [50]. A hemizygous
Arabidopsis line with a T-DNA insertion in the gene that
encodes a protein with similarity to VPS52 (named POKY
POLLEN TUBE[POK]) has short pollen tube growth. A
POK–GFP fusion protein localised to Golgi stacks in
onion cells, suggesting a conserved function for the
GARP complex in plants [50]. The DSL1 complex
Current Opinion in Plant Biology 2005, 8:1–8
was only recently described in mammals [51]. It is not,
or only poorly, conserved in plants.
Conclusions
The golgins and multi-subunit transport complexes have
emerged as important players in mammalian and yeast
Golgi structure and function. As the organisation and
distribution of the plant Golgi apparatus differs from that
in animal and yeast cells, we might find that plant proteins
with similarity to the mammalian or yeast golgins or
transport complexes have different functions in the plant
Golgi. Exploring their functions in plant cells, however,
opens up a new avenue for investigating the structure and
function of the Golgi stack, anterograde and retrograde
cargo transport, the relationship of the Golgi stack with
the endoplasmic reticulum and the unique patterns of
movement displayed by individual Golgi stacks. Thus,
although caution should be taken when extrapolating
findings from the animal to the plant system, the animal
Golgi system has given us a launching pad from which to
start to understand that in plants.
Acknowledgements
We thank the Biotechnology and Biological Sciences Research Council
(BBSRC) and the Scottish Executive Environment and Rural Affairs
Department (SEERAD) for supporting for this work. Ulla Neumann is
acknowledged for the electron micrograph (Figure 1).
www.sciencedirect.com
Candidate proteins for the plant Golgi matrix Latijnhouwers, Hawes and Carvalho 7
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