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If walls could talk
Commentary
Janet Braam
The plant cell wall is very complex, both in structure and
function. The wall components and the mechanical properties
of the wall have been implicated in conveying information that
is important for morphogenesis. Proteoglycans, fragments of
polysaccharides and the structural integrity of the wall may
relay signals that influence cellular differentiation and growth
control. Furthering our knowledge of cell wall structure and
function is likely to have a profound impact on our
understanding of how plant cells communicate with the
extracellular environment.
Addresses
Biochemistry and Cell Biology, Rice University, Houston,
TX 77251-1892, USA; e-mail: [email protected]
thallus and rhizoid cells of Fucus [4]. The wall can therefore restrict and maintain cellular differentiation.
Surprisingly and significantly, thallus or rhizoid daughter
cells switch developmental fate when they physically
contact the wall remnants of laser-ablated cells of the
other cell type [4]. For example, thallus daughter cells
that come into close contact with the remains of rhizoid
cell walls take on rhizoid cell identity. Because close association of the cell wall appears to be required for the cell
identity switch, it is likely that the wall components of
the two cell types differ, and that at least a subset of these
characteristic distinctions function as differentiation signals. The identities and modes of action of these wall
molecules remain unknown.
Current Opinion in Plant Biology 1999, 2:521–524
1369-5266/99/$ — see front matter © 1999 Elsevier Science Ltd.
All rights reserved.
Abbreviation
AGP
arabinogalactan protein
Introduction
Plant development requires coordination and communication among the cells of various organs. The identity of
cells is strongly influenced by their position during plant
morphogenesis rather than by their developmental lineage [1]. Furthermore, the extent and orientation of
cellular expansion must be synchronized with that of
neighboring cells because the walls between them act as
structural restraints to movement. Neighboring plant cells
communicate through plasmodesmata (the regulated
intercellular channels that connect the plasma membranes, the endoplasmic reticulum membranes and
lumens, and the cytosol of adjacent cells) [2]. Many integral plasma membrane proteins also have features that
typify receptors capable of transducing external ligand
binding into intracellular messages [3]. In addition, plant
hormones move through tissues as signals. Apoplast factors can also act as signals and, in addition, the structural
properties of the wall may serve to relay messages to the
cell interior. In this review we discuss the evidence for the
involvement of two molecules, a proteoglycan and a cellwall polysaccharide fragment, in cell–to–cell signaling. In
addition, we discuss the potential role of mechanical strain
in triggering cellular responses that maintain cell expansion rates and turgor.
Intercellular signals from walls during
embryogenesis
The cell wall of the marine alga Fucus has a profound
ability to control the differentiation potential of developing cells. Only embryonic cells from which the walls are
removed are totipotent and able to give rise to both the
Antibodies that recognize specific wall components are
known to identify differing epitopes among distinct cell
types or developmental stages [5]. These findings are consistent with the idea that walls harbor differentiation
markers. Whether these markers are active components
that regulate and maintain cellular identity, or whether
their presence is just a consequence of the morphogenetic
events has yet to be determined.
As in Fucus, the embryogenesis of higher plants might
depend on components of the extracellular matrix.
Evidence has come from studies of somatic embryogenesis, a process that resembles embryogenesis in which the
somatic cells of mature plants undergo redifferentiation in
vitro and can give rise to fertile plants. Differences in wall
composition, released proteins and the relative adhesiveness of cell-to-cell interactions have been shown to exist
between cell clusters and correlate with their embryogenic
potential [6–8]. The finding that the use of ‘conditioned’
media, on which embryogenic cells have previously been
cultured, is important for differentiation indicates that soluble factors secreted from cells can have a profound
developmental impact [9–11].
The arabinogalactan proteins
One class of extracellular matrix molecules implicated in
the regulation of somatic embryogenesis is the arabinogalactan proteins (AGPs). AGPs can be classed as
proteoglycans because they are composed of more than
90% carbohydrate, mostly L-arabinose and D-galactose.
Although AGPs are rich in hydroxyproline, alanine, serine
and threonine, their protein backbones are quite diverse,
and each backbone may be differentially modified by the
addition of a polysaccharide [12–15]. The full structural
characterization of AGPs may therefore be a difficult task.
One class of AGPs, known as the ‘classical’ type because
they were the first to be defined, have the potential to be
anchored in membranes by glycosyl phosphatidyl inositol
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Commentary
(GPI) anchors [16]. In animal cells, such anchors can potentially direct the proteins to particular membrane faces [17]
or, through interactions with integral membrane proteins,
might enable signal transduction from the extracellular
matrix to the cell interior [18].
AGPs have complex and restricted localization patterns;
their presence correlates with embryogenic potential, proliferative state or developmental stage [5,19]. The
application of media conditioned by the culturing of
embryogenic cells that thereby harbors AGPs, or of AGPs
selected by specific antibodies, can enhance the embryogenic potential of other cells. In contrast using media
containing AGPs or adding specific antibody-purified
AGPs from nonembryogenic cells can decrease the number of embryos formed [11,15]. These data suggest that the
distinct AGPs present in the media might be the active
component which influences cellular differentiation.
The β-glucosyl Yariv reagent, which selectively interacts
with AGPs, has been used as a tool to probe the in planta
function of AGPs. The incubation of cells or tissues with
the Yariv reagent results in alterations to cell growth and
division, consistent with the idea that AGPs have important functions in these processes [19]. It is likely, however,
that the use of the Yariv reagent results in the disruption of
wall structure through the cross-linking of AGPs. The
direct consequences of the loss of AGPs has not, therefore,
been clearly assessed. Mutations in AGP structural genes,
or in genes whose functions are required for appropriate
AGP modification, will be the ultimate tools for elucidating AGP function in vivo.
Whether AGPs function through a structural or signaling
mechanism is unknown. Because AGPs can be freely
released from cell walls it is thought that they might not
contribute to the structural integrity of the wall. AGPs can
form complexes when leaves are excised, or when the proteoglycans are exposed to H2O2; they might therefore
contribute to wall cross-linking under conditions of oxidative stress [20]. Although it is possible that the minor
protein portion of AGP may function through interactions
with other wall components, it is probable that most of the
protein backbone is sterically blocked by the attached
polysaccharides. The polysaccharide extensions of AGPs
have the potential to form a gel-like matrix in association
with water. Some hydrated carbohydrate moieties that are
present in the extracellular matrix of animal cells are
thought to function as cell chaperones in that they sterically block interactions between cells in a regulated
fashion [21]. These polysaccharides determine when
interactions take place and whether plasticity of associations is possible. AGPs might act in a similar manner; that
is, AGPs might be recruited during wall remodeling or
assembly, and may facilitate appropriate interactions
among the extracellular domains of transmembrane proteins or cell-wall components.
Cell-wall fragments
Fragments of wall structural polymers can influence cellular behaviors [22–25]. For example, oligogalacturans
can signal pathogen attack and can also influence the
growth and differentiation of both flowers and roots in
thin layer cultures. Fragments of xyloglucan have also
been shown to either enhance growth or inhibit auxininduced growth, depending upon the level and specific
structure of the added xyloglucan oligosaccharide. Our
current understanding of the presence and action of
xyloglucan endotransglycosylases (XETs) might help to
explain the effects of high concentrations (>1 micromolar)
of xyloglucan oligosaccharides. Through transglycosylation to xyloglucan polymers present in the wall, the
oligosaccharides can act to shorten the lengths of the
xyloglucan chains, reducing xyloglucan tethering of cellulose microfibrils and enhancing wall loosening [26,27].
Whether xyloglucan oligosaccharides participate in wallloosening mechanisms during cell expansion of untreated
tissues has not been demonstrated.
Nanomolar concentrations of specific xyloglucan oligosaccharides bearing fucose sidechains can interfere with
growth [22–25]. The specific requirement of the fucose
moiety, and the ability of the oligosaccharide to act at low
concentrations strongly suggests this effect is distinct from
the growth-enhancing effects of high concentration of
xyloglucan oligosaccharides. The mechanism of growth
inhibition is unknown but peroxidase activation has been
implicated [28].
Xyloglucan oligosaccharides have been detected in media
on which cells have been cultured; their presence is consistent with the proposed function in signaling. However,
definitive evidence for a role for xyloglucan oligosaccharides as endogenous growth regulators would entail the
demonstration of a loss of function when such oligosaccharides are not available. The cloning of a gene that
encodes the fucosyl transferase that modifies xyloglucan
[29] may be the important first step in a genetic approach
to this problem. Plants that have mutations in this gene
might reveal the consequences of the inability to generate these specific xyloglucan oligosaccharides.
Interpretations of phenotype will, however, be complicated by the absence of the fucosyl groups on the
xyloglucan polymers, which may affect their ability to act
as wall structural components.
Given that xyloglucan polysaccharides are a major component of the dicotyledenous cell wall, it is possible that
oligosaccharides are recognized through a previously
unknown mechanism. Although there might be a specific receptor for the oligosaccharides, it is also possible that
the oligosaccharides act by displacing xyloglucan polymers from their binding sites, or by competing as
substrates for molecules that modify the wall, such as
expansins. The oligosaccharides could alter the structure
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If walls could talk Braam
of the wall in this way; such structural changes may signal
through mechanotransduction pathways.
Mechanical force
It is well recognized that the cell wall is essential for
maintaining the mechanical integrity of plants and for
controlling the expansion of cells. The cell wall’s
mechanical resistance to stretching and the osmotic gradient across the plasma membrane lead to the generation
of turgor pressure within the cell. Turgor pressure imposes 10–100 MPa of stress upon the walls [30]. The
perception of changes in wall tension may signal the regulation of processes that contribute to the maintenance of
cellular homeostasis. For example, plant cells have a
remarkable capacity to maintain a constant expansion
rate, even when subjected to osmotic stress or to other
perturbations that alter turgor pressure. Solute uptake is
also closely correlated with expansion rate. Changes in
wall tension might therefore be used as feedback signals
to maintain homeostasis. One possible mechanism is that
wall tension is sensed through mechanical deformations
of the wall–membrane connections that enable signal
transductions to the cell interior. Evidence that supports
the involvement of the cell wall in signaling responses to
mechanical forces comes from a number of sources.
Gravisensing in the internodal cells of Chara corallina is
sensitive to enzymes that digest major wall components
and to peptides that are known to interact with animal
cell integrins [31]. Fischer and Schopfer [32] interfered
experimentally with the induced tropic curvature of
maize (Zea mays) coleoptiles and found that microtubule
orientation followed the direction of the induced
mechanical strain rather than reoriented as a function of
the gravitropic or phototropic signal transduction pathway. These results are consistent with the results of
Lynch and Lintilhac [33] and Hernández and Green [34]
who showed that applying mechanical forces or constraints to plant tissues can alter their planes of division
and developmental patterning.
Applying cell-wall-modifying protein, expansin, to shoot
apical meristems results in the inappropriate formation
of leaf primordia-like extensions [35]. Expansins are
thought to act by releasing the hydrogen-bonding interactions between the cellulose and hemicellulose
components of the wall and, in this way, to contribute to
wall loosening [30]. The morphogenetic alterations
caused by exogenous expansin most likely result from
expansin evoked changes in the material properties of
the wall. These experiments are an elegant demonstration of how modifying the properties of the plant cell
wall, through altering arrangements or interactions of
wall polysaccharides, can have a fundamental role in
plant morphogenesis.
Conclusions
Plant cells may have versatile mechanisms to communicate with neighboring cells. The roles of unusual signals,
523
such as wall proteoglycans, fragments of wall polysaccharides and mechanical deformations of the wall are
becoming more evident. The elucidation of the how these
signals are generated and perceived will have a profound
impact on our understanding of plant cell functions.
Acknowledgements
I thank the National Science Foundation, the National Aeronautics and Space
Administration, the Department of Energy and the United States
Department of Agriculture for their support of my research on plant cell walls.
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