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Plant cell expansion: scaling the wall
Frédéric Nicol and Herman Höfte∗
The regulation of plant cell size and shape is poorly
understood at the molecular level. Recently, two loci required
for normal cell expansion in Arabidopsis were cloned. They
both encode enzymes involved in the construction of the cell
wall. These studies are the first promising examples of the
use of Arabidopsis molecular genetics for the study of wall
synthesis and assembly during plant cell elongation.
Addresses
INRA, Laboratoire de Biologie Cellulaire, Route de St-Cyr, 78026
Versailles Cédex, France
∗e-mail: [email protected]
Current Opinion in Plant Biology 1998, 1:12–17
http://biomednet.com/elecref/1369526600100012
 Current Biology Ltd ISSN 1369-5266
Abbreviations
EGase endo-1,4-β-d-glucanase
EST
expressed sequence tag
DCB
dichlorobenzonitrile
TC
terminal complex
Introduction
Cell expansion plays a crucial role in plant development.
The shape of plant organs and the function of the tissues
are to a large extent dependent on the regulation of the
size and the shape of the constituent cells. Cell size itself
may also act as a signal to trigger cell division [1,2] or even
differentiation [3].
Our current understanding of the molecular basis of
cell enlargement has been extensively covered in recent
reviews [4–6] and some key features are summarised in
Figure 1. Briefly, the rigidity of a plant cell is the result of
the osmotically induced turgor pressure which can be built
up by virtue of the cell wall strength. Since, in a growing
cell, the turgor pressure generally remains constant,
cell enlargement must be the result of the controlled
expansion of the primary wall. The growing plant cell wall
is a polymeric structure, consisting of crystalline cellulose
microfibrils coated with hemicellulose chains which are
embedded in a highly hydrated pectin matrix with small
amounts of protein. The direction of cell expansion
is thought to be controlled by the orientation of the
cellulose microfibrils. In growing cells these microfibrils
are laid down transversely to the axis of elongation, thus
forming a spring-like structure reinforcing the cell laterally
and favouring longitudinal expansion. Control of the
orientation of cellulose has been attributed to the cortical
microtubules, which are normally aligned in the same
orientation as the cellulose microfibrils and may guide
the cellulose synthase complexes [7]. Consistent with
this model, anisotropic growth is abolished upon chemical
inhibition of cellulose synthesis or microtubule polymerisation [8]. Hemicelluloses and pectins are synthesised in
the Golgi apparatus and transported in vesicles to the cell
surface. Upon secretion into the apoplast, hemicelluloses
bind tightly to cellulose and are thought to link the
microfibrils in a stress-resistant network. Cell expansion
requires the constant rearrangement of the bonds within
this network, to allow the movement of wall polymers and
the incorporation of new wall material into the existing
architecture. According to the acid growth theory, the
cell wall pH plays a coordinating role in this process [9].
Activation of the H+ ATPase under influence of auxin, and
maybe other growth factors, lowers the wall pH. This, in
turn, stimulates the highly pH-dependent activity of three
classes of wall proteins potentially involved in rearranging
wall polymers: expansins, xyloglucan endotransglycosylases and endo-1,4-β-D-glucanases (Figure 1). Increasing
the pH would arrest cell expansion by inhibiting the
activities of these proteins and by inhibiting the activation
of enzymes thought to be involved in wall cross-linking.
The role of polysaccharide biosynthesis and vesicular
transport in the control of cell expansion is not understood
[10]. Also, our knowledge of how growth factors, light,
mechanical stimuli, nutrition and cell–cell interactions
influence the extent and direction of cell enlargement
remains very rudimentary.
The study of Arabidopsis molecular genetics now sheds
new light on this research area: we will devote the majority
of this review to new insights obtained from two cell
wall mutants that encode a cellulose synthase subunit
and an unusual endo 1,4-β-glucanase. We will then go
on to discuss other cell expansion mutants with potential
wall defects and the importance of cellulose synthase-like
genes.
A cellulose synthase mutant
Cellulose is composed of unbranched polymers of 1,4β-D-linked glucose residues that form crystalline arrays
of many parallel chains which make up microfibrils
[11]. All available evidence suggests that cellulose is
synthesised at the plasma membrane, presumably by
a multisubunit protein complex, the so-called terminal
complex (TC), which can be visualised as hexameric
rosettes on freeze-fractured membranes [12]. Despite
much effort, plant cellulose synthase has so far resisted
purification, in part due to its low in vitro activity
[13]. A major step forward was the identification of
a family of candidate genes for the catalytic subunit
of cellulose synthase through expressed sequence tag
(EST) sequencing [14]. (For recent reviews on cellulose
synthesis, see [15,16]). During the past year a further
breakthrough was reported with the positional cloning of
Plant cell expansion Nicol and Höfte
13
Figure 1
Plasma membrane
Elongation
Cytosol
Plasma membrane / Cell wall interface
Golgi apparatus
Cellulose synthase complex
Membrane bound endo-1, 4-β-D-glucanase
Lateral view
Top view
Cellulose microfibril
Soluble endo-1, 4-β-glucanase
H+/ATPase
Xyloglucan EndoTransglycosylase
Expansin
Xyloglucans
Secretory vesicles
Schematic representation of some of the cellular processes thought to be involved in cell expansion in an elongating dicotyledonous cell,
adapted from Cosgrove [10]. Cellulose microfibrils are thought to be synthesised by plasma membrane-bound hexameric cellulose synthase
complexes. All other cell wall polysaccharides are synthesised in the Golgi apparatus and transported in vesicles to the cell surface. Xyloglucans
are tightly bound to microfibrils by hydrogen bonds and form cross-links between them, thus constituting a load-bearing network. Only a
small number of xyloglucan chains are represented for simplicity. In elongating cells, the microfibrils are deposited perpendicular to the axis
of elongation, forming a spring-like structure that reinforces lateral walls and favours longitudinal growth. Expansins are thought to act at the
xyloglucan–cellulose interface and promote movement of the polymers; endo-1,4-β-D-glucanases cleave xyloglucans, whereas xyloglucan
endotransglycosylases cleave xyloglucan and join the newly generated reducing end to other xyloglucan chains represented by an arrow in the
figure. The increase in wall surface then leads to the uptake of water and solutes, which results in an increase in volume. Cell growth arrests as
soon as the wall pH increases, for instance through inhibition of the proton ATPase, which would inhibit cell wall loosening proteins, and activate
a set of enzymes potentially involved in cross-linking the wall, for example pectin-methyl esterases (PMEs) or peroxidases.
a member of this gene family from a cellulose-deficient
mutant in Arabidopsis, as discussed below.
Williamson and colleagues [17] carried out a screen for
temperature-sensitive mutants that showed exaggerated
radial expansion of root cells at the restrictive temperature (31˚C), reminiscent of the phenotype obtained
after treatment with the cellulose synthesis inhibitor
dichlorobenzonitrile (DCB). Mutants identifying four Root
Swelling (RSW) loci indeed show a significant reduction of
the amount of crystalline cellulose found in cell walls when
grown at 31˚C. Recently, the positional cloning of one of
the loci, RSW1, was carried out (unpublished data). RSW1
encodes a 122 kDa protein, with a low but significant
sequence similarity (about 30% amino acid identity) to the
catalytic subunit of bacterial cellulose synthases [18–20].
RSW1 is also highly similar to the products of two cDNAs
(CelA1 and CelA2) that had been previously identified
14
Growth and development
through random EST sequencing of a cDNA library from
maturing cotton fibres [14]. In addition to the sequence
similarity, two other observations suggest that CELA1
indeed encodes a catalytic subunit of cellulose synthase.
First, the mRNA levels of CELA1 were strongly induced
in fibre cells at the onset of massive cellulose synthesis
during secondary wall formation, and second, a fragment
of CELA1 expressed in Escherichia coli specifically bound
UDP-glucose, the substrate for cellulose synthase, in a
magnesium-dependent way.
What can we learn from the rsw1 mutant phenotype?
Mutant plants grown at 31˚C show increased radial expansion in all cell types investigated, including tip-growing
cells such as trichomes and root hairs ([17] and personal
communication). RSW1, therefore, seems to be required
for primary wall synthesis in all cells. It is not clear to
what extent secondary wall formation is affected as well.
Shifting the temperature from 18˚C to 31˚C causes the
disappearance of the hexameric rosettes in the plasma
membrane as shown by freeze etching. At the same
time, over 50% reduction in the production of crystalline
cellulose can be observed. Unexpectedly, a 1,4-β-linked
glucan that behaves in all aspects as a noncrystalline
polymer accumulates. Indeed, this glucan, in contrast to
crystalline cellulose, co-extracts with the wall pectins in
ammonium oxalate, and is susceptible to hydrolysis by
trifluoroacetic acid, or an endo-cellulase/1,4-β-glucosidase
mixture. The simplest interpretation of these results
is that the mutation prevents the assembly of glucan
chains into microfibrils but does not inhibit glucan
synthesis per se. At the restrictive temperature the mutant
synthase complexes would disassemble to monomers.
The monomers of the catalytic subunit would still be
catalytically active, but the synthesis of 1,4-β-glucan chains
at dispersed sites would prevent microfibril assembly.
In summary, the mutant phenotype of Arabidopsis rsw1
together with the observations on cotton CelA1 now
strongly support the idea that CELA1 and the closely
related protein RSW1 are both bona fide catalytic subunits
of cellulose synthase.
What can we learn from the RSW1 sequence? The
hypothetical structure of RSW1 is shown in Figure 2. The
protein has two amino-terminal and six carboxy-terminal
predicted membrane spanning domains, with a large central domain which is presumably cytosolic. Experiments
with epitope-tagged cotton CELA1 expressed in yeast
provided evidence for the cytosolic orientation of the
amino terminus and the extracellular orientation of the
last loop (D Delmer, personal communication). Within the
central domain one can distinguish four regions conserved
in all processive glycosyl transferases in plants and
bacteria; these regions contain three conserved aspartic
acid residues and a QXXRW motif (single-letter code
for amino acids) which are thought to be critical for
catalysis and UDP-glucose binding [11]. The cysteine-rich
amino terminus has two predicted zinc finger domains
forming a LIM-like motif: a structural zinc-binding motif
potentially involved in protein-protein interactions, found
in animals and plants [21]. The amino terminal domain of
CELA1 produced in E. coli as a glutathione-S-transferase
fusion protein effectively binds zinc with a protein : Zn
stoichiometry of 1:2 (D Delmer, personal communication).
This domain shows sequence similarity to two bZIP
transcription factors from soybean (unpublished data) and
is most likely involved in protein–protein interactions.
Having identified RSW1 and related genes, the rapid
isolation of the other subunits of the cellulose synthase
complex using yeast two-hybrid or biochemical techniques
can be expected. Also the regulation of cellulose synthesis,
crystallisation and orientation during cell enlargement and
secondary wall formation can now be addressed more
easily.
An unusual endo-1,4-β-D-glucanase mutant
The recessive mutation korrigan (kor) was identified in
a screen for short hypocotyl mutants of Arabidopsis [22].
As with rsw1, kor cells show reduced elongation and
increased radial cell expansion. The mutation affects
all cell types examined, except for the tip-growing
root hairs, trichomes and pollen tubes. Judged from
analysis of sections of fixed material; mutant primary cell
walls are thicker and have a highly undulated surface.
In contrast to wild-type walls, no layered structure of
cellulose microfibrils can be distinguished in kor walls,
and aggregates of polysaccharides containing cellulosic
material accumulate at the cytoplasmic side of the cell wall
([22] and our unpublished data).
The T-DNA-tagged Kor gene was cloned and encodes
a member of the endo-1,4-β-D-glucanase (EGase) family
([22] and our unpublished data). EGases form an ancient
class of enzymes present in plants, bacteria, fungi
and animals that hydrolyse 1,4-β linkages adjacent to
nonsubstituted glucose residues. In contrast to bacterial
and fungal EGases which can degrade crystalline cellulose,
plant EGases lack a cellulose binding domain and only
degrade noncrystalline 1,4-β-glucans in vitro. The exact
in vivo substrate is not known, but it is thought to
be xyloglucan [23]. Plant EGases are encoded by large
gene families: Arabidopsis expresses at least ten different
EGase genes ([22] and our unpublished data). The
expression of plant EGase genes is tightly regulated
and the expression patterns suggest a role for these
enzymes in plant development. The expression of one
group of genes is ethylene-inducible and correlated with
massive wall degradation during fruit ripening and leaf
abscission [23]. The expression of a second class of
EGase genes appears to be correlated with the more
subtle hydrolytic processes thought to take place during
the rearrangement of polysaccharides in growing cells
[23–25]. The hypothetical mode of action of EGases in
cell expansion could be either to promote wall loosening,
thereby acting cooperatively with expansins [5], or to
Plant cell expansion Nicol and Höfte
15
Figure 2
Cell walls
Cytosol
D
Zn2+
W
R
L
V
Q
Zn2+
HVR
D
PCR
D
Zinc finger domain
DDD, QVLRW Conserved motif and residues of processive b-glycosyl transferases
Plant conserved region (PCR)
Highly Variable Region (HVR)
Current Opinion in Plant Biology
Predicted membrane topology and other structural features of RSW1. The protein has two amino-terminal and six carboxy-terminal predicted
membrane-spanning domains. In the centre, a large, most likely cytosolic, domain can be distinguished containing four regions conserved for
all processive glycosyl transferases in plants and bacteria, and which are predicted to be critical for UDP-glucose binding and catalysis in
bacterial CelA. The three critical aspartic acid (D) residues and the QXXRW motif in these regions are indicated. Also in the central domain,
two plant-specific regions of unknown function can be distinguished, a plant conserved region (PCR) and a highly variable region (HVR).
The cytosolic orientation of the amino terminus and the extracellular orientation of the last loop have been experimentally confirmed for the
cotton CELA1 (D Delmer, personal communication). The amino terminus contains two zinc-finger domains, which are most likely involved in
protein–protein interactions.
contribute to the incorporation of new microfibrils in
the growing wall. The mRNA induction kinetics of an
auxin-inducible isoform, CEL7, expressed in the tomato
hypocotyl, indicates that the increased expression is not
required for the rapid growth response to auxin, and
suggests rather that the enzyme has a role in sustained
growth [26].
In contrast to other plant EGases, the KOR sequence
predicts an integral membrane protein with a short amino
terminus in the cytosol and an external catalytic domain
(type II topology). Free flow electrophoresis analysis localised the protein mainly in plasma-membrane-enriched
fractions, with a minor portion in internal membranes
that were enriched for a tonoplast marker. CEL3, a
tomato EGase highly similar to KOR, was also localised
in plasma-membrane-enriched membrane fractions and in
a membrane fraction comigrating with Golgi markers in a
linear sucrose gradient [27•].
KOR mRNAs are present in all plant tissues, and in
germinating seedlings appear concomitantly with the onset
of hypocotyl elongation. For the tomato homologue, CEL3,
mRNA levels are not influenced by external addition
of auxin, ethylene or brassinosteroids [27•]. We can
only speculate on the significance of the membrane
location. A membrane-bound enzyme may be more easily
targeted either to the inside of the wall or to specific
wall domains (for instance, to the longitudinal walls of
elongating cells). Alternatively, a membrane location may
16
Growth and development
allow the abundance of the enzyme in the cell wall to
be precisely controlled, for instance through endocytosis.
Also, a membrane anchor may allow the targeting of a
fraction of the protein to the Golgi apparatus where the
enzyme might have a role in the priming of the synthesis
of xyloglucans, the polysaccharides that bind to cellulose
and form the major load bearing network of the primary
wall [27•]. Finally, a membrane-associated EGase may
in fact be a part of the cellulose synthase complex and
play a role in the synthesis of cellulose. Indeed, the
only other known example of a membrane-bound EGase
was reported for Agrobacterium tumefaciens, where the gene
(CelC) is part of the cellulose synthase operon [20,28]. In
Agrobacterium CelC is essential for cellulose synthesis as
shown by transposon mutagenesis, and the authors provide
evidence for a role of this protein in the polymerisation
of lipid-linked oligosaccharides to cellulose. The existence
of lipid-linked intermediates for cellulose synthesis in
bacteria and certainly for plants remains controversial
but so far has not been ruled out [15]. The unordered
accumulation of cellulosic material in kor mutant walls is
not incompatible with a role for this enzyme in an as yet
unidentified step in the biosynthesis or crystallisation of
cellulose.
In summary the results show a crucial role for a membranebound EGase in cell elongation and normal wall assembly,
and raise new interesting questions as to its function that
can now be experimentally addressed.
More cell expansion mutants
A number of increased radial cell expansion mutants
presenting phenotypes very similar to that of rsw1 and
kor have been described. Recessive mutants identifying
three other root-swelling loci (RSW2, RSW3, RSW5) show,
like rsw1, a temperature-sensitive reduction in cellulose
accumulation (R Williamson, personal communication).
Other mutants of this class were described as conditional
root expansion (CORE) mutants [29]. These mutants
identify six loci (POMPOM1 [POM1], POMPOM2 [POM2],
COBRA [COB], LION’S TAIL [LIT], QUILL [QUI] and
CUDGE [CUD]); lit and qui mutants are respectively allelic
to rsw2 (R Williamson, personal communication) and
procuste1 (prc1) [30]; H Höfte and P Benfey, unpublished
data). The cloning of at least some of these loci is
expected ultimately to identify other structural proteins of
the cellulose synthase complex or regulators of cellulose
synthesis or deposition. The recessive mutant prc (qui)
shows, in addition to its root phenotype, an increased
and uncoordinated radial expansion in hypocotyls, but
only in dark-grown seedlings. Light, through the action
of phytochrome, completely rescues the hypocotyl-growth
defect [30]. PRC1 may therefore represent a link between
phytochrome control of cell elongation and cell wall
assembly. Several other mutants show defects in cellulose
synthesis, but specifically during secondary wall formation
[31,32], indicating that this process requires specialised
sets of genes not required in growing cells. Other
mutants with altered wall polysaccharide composition were
described by Reiter and colleagues [33–35] and reviewed
elsewhere [36].
Gene-families encoding cellulose synthases
or related enzymes
Inspection of sequence databases shows that RSW1, CelA1
and CelA2 are members of a large gene family present
in dicots and monocots. So far, at least seventeen related
genes have been identified among ESTs and genomic
sequences from Arabidopsis [37] (S Cutler, personal
communication). In view of this high apparent redundancy,
it is surprising that a mutation in the single gene RSW1
causes such a strong phenotype in all cell types.
In addition, a class of more distantly related genes, the
cellulose-synthase-like, or Csl, genes, represented by at
least nine genes in Arabidopsis, can be distinguished
(S Cutler, personal communication). The Csl products
contain seven or eight predicted membrane-spanning
domains, and also contain the three conserved aspartic
acid residues and the QXXRW motif, characteristic of
processive glycosyl transferases [11]. The overall sequence
similarity with CELA is low, for instance, CSL1 shows
about 25% amino acid identity with CELA. CelA products
are in fact more related to their bacterial homologues
than to Csl, suggesting that their divergence preceded the
appearance of eukaryotes in evolution. It is conceivable
that CSLs are processive glycosyl transferases involved in
the biosynthesis of other 1,4-β- or 1,3-β-linked polysaccharides in plants [37] and may represent a subset of the
estimated several hundred enzymes that are required to
produce the complete set of wall polysaccharides [38]. The
use of reverse genetics is expected to clarify the role of
these different family members in wall biosynthesis.
Conclusions
With the help of Arabidopsis molecular genetics, a corner of
the veil covering the cellular processes involved in polysaccharide biosynthesis and assembly in the growing primary
wall has been lifted. The temperature-sensitive rsw1
mutants identify beyond reasonable doubt the catalytic
subunit of the cellulose synthase complex. The cloning of
the gene encoding a plasma membrane-associated EGase
essential for cell elongation and normal wall assembly has
added an intriguing new element to the cell elongation
machinery, with a role for the EGase either in the
rearrangement of wall polymers or in the synthesis or
crystallisation of cellulose. These findings will greatly
accelerate the identification of other proteins of the
cellulose synthase complex and the molecular dissection
of cellulose synthesis. The functional study of these
proteins and other CELA family members, together with
the cloning of the genes identified by other radial cell
expansion mutants, may revolutionise our understanding
of cell-wall-associated processes involved in the expansion
of plant cells.
Plant cell expansion Nicol and Höfte
Acknowledgements
The authors wish to thank Richard Williamson and Tony Arioli, Debby
Delmer, Sean Cutler, Marie-Therès Hauser and Philip Benfey for allowing
us to cite their unpublished results. We apologise to those colleagues
working in the field whose work could not be mentioned due to space
limitations, and thank Heather McKann, Ageeth Van Tuinen and Rachel
Cowling for critical reading of the manuscript. Our research was in part
financed by a grant, ACC-SV number 9501006 from the Ministère de la
Recherche et de la Technologie to Herman Höfte.
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•
Brummell DA, Catala C, Lashbrook CC, Bennett AB: A
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This paper describes CEL3, the first membrane-bound endo 1,4-β-glucanase found in plants. The gene was cloned from tomato and its product
detected in the plasma membrane with a minor fraction in the Golgi apparatus. The gene appears to be the ortholog of KORRIGAN a locus required
for cell elongation and normal cell wall architecture in Arabidopsis (Nicol et
al. 1997).