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Update on Cytoskeleton-Plasma Membrane-Cell Wall Continuum
Cytoskeleton-Plasma Membrane-Cell Wall Continuum in
Plants. Emerging Links Revisited1
František Baluška*, Jozef Šamaj, Przemyslaw Wojtaszek, Dieter Volkmann, and Diedrik Menzel
Institute of Botany, Department of Plant Cell Biology, Rheinische Friedrich-Wilhelms University of Bonn,
53115 Bonn, Germany (F.B., J.Š., P.W., D.V., D.M.); Institute of Plant Genetics and Biotechnology, Slovak
Academy of Sciences, Akademicka 2, SK–949 01 Nitra, Slovak Republic (J.Š.); Institute of Molecular Biology
and Biotechnology, Adam Mickiewicz University, 61–701 Poznań, Poland (P.W.); and Institute of Bioorganic
Chemistry, Polish Academy of Sciences, 61–704 Poznań, Poland (P.W.)
Eukaryotic cells typically deviate from spherical
shapes due to complex interactions between elements
of their cytoskeleton and the extracellular matrix
(ECM). Communication between the cytoskeleton
and ECM is one of the most characteristic features of
cellular mechanics and allows cells to respond effectively to various signals, especially mechanical stimuli. Cells devoid of the ECM and/or cytoskeleton
inevitably lose their polar shapes returning to the
default, preferentially spherical, shape (for plant
cells, see Smith, 2001; Baluška et al., 2003b). This loss
of cellular polarization prevents cells from their cellto-cell interactions and communication. This is true
for both animal and plant cells, even when modes of
ECM-cytoskeleton and cell-to-cell interactions are
based on contrasting principles in these two types of
multicellular organisms (Baluška et al., 2003b). Multicellularity in plants and animals has evolved independently. Animals and humans are truly multicellular organisms as their inherently motile cells
aggregate together and typically can associate with a
wide range of cell types (Critchley, 2000; Geiger and
Bershadsky, 2001). On the other hand, plants are
supracellular organisms because their immobile cells
divide via the phragmoplast-based incomplete cytokinesis that results in the formation of cytoplasmic
cell-to-cell channels known as plasmodesmata (Lucas
et al., 1993). Consequently, plant cells are not fully
separated, and both the plasma membrane and endoplasmic reticulum traverse cellular borders
through plasmodesmata. These membranes are physically interlinked into continuous membraneous system essentially spanning the whole plant (Lucas et
al., 1993). The ECM of plant cells, better known as cell
walls, is integrated into the apoplast—a structurally
coherent superstructure extending throughout the
plant body (Wojtaszek, 2001). Cell walls represent an
inherent part of plant cells (Wojtaszek, 2000) although plant protoplasts can rapidly and reversibly
1
This work was supported by the Alexander von Humboldt
Foundation (Bonn; to F.B., J.Š., and P.W.).
* Corresponding author; e-mail [email protected]; fax
49 –228 –739004.
www.plantphysiol.org/cgi/doi/10.1104/pp.103.027250.
482
retract from the cell wall during osmotic stressinduced plasmolysis (Oparka, 1994; Lang-Pauluzzi
and Gunning, 2000). In contrast, most animal and
human cells are truly “naked” and interact with the
ECM in its vicinity that is often produced by other
cells, occasionally at discrete domains known as focal
adhesions (Critchley, 2000) or tight/adherens junctions and desmosomes in the case of cell-to-cell contacts (Geiger and Bershadsky, 2001).
Entering the post-genomic era, contemporary cell
biology is becoming aware of epigenetic mechanisms
of cell differentiation (Goldman, 2003; Orlando,
2003). In particular, one of the new priorities in the
cell biology would be to understand how mechanical
forces regulate and integrate cellular activities (Ingber, 2003a, 2003b). It is well known that mechanical
forces are rapidly, and almost without loss of information, translated into biochemical messages (Riveline et al., 2001; Ingber, 2003a, 2003b). Moreover,
mechanical forces play essential roles in the control
of cellular behavior (Janmey, 1998; Geiger et al., 2001;
Gillespie and Walker, 2001; Riveline et al., 2001; Ingber, 2003a, 2003b; Ponta et al., 2003; Rørth, 2003).
Generally, cellular structure is inherently endowed
with information that can be both stored and handed
over to other structures via templating processes (for
plant cells, see Baluška et al., 1997, 2003b). Although
available data are rather scarce for higher plants, and
critical linker molecules between the cytoskeleton
and ECM are still missing (Pont-Lezica et al., 1993;
Wyatt and Carpita, 1993; Fowler and Quatrano, 1997;
Miller et al., 1997a, 1997b; Kohorn, 2000; Heath,
2001), it is increasingly obvious that cell shape and
mechanical forces dictate several processes among
which the control of division planes is one of the
most obvious (Lintilhac and Vesecky, 1984; Lynch
and Lintilhac, 1997; Green, 1999; Sipiczki et al., 2000;
Smith, 2001). The integrated cytoskeleton and its dynamic adhesion to the plasma membrane allow these
complex interactions between mechanical forces and
chemical signals (Critchley, 2000; Geiger and Bershadsky, 2001; Sheetz, 2001). What is still unknown
in plants is the molecular nature of linkers between
elements of the cytoskeleton and components of the
cell wall. Available Arabidopsis Genome Database
Plant Physiology, October 2003, Vol. 133, pp. 482–491, www.plantphysiol.org © 2003 American Society of Plant Biologists
Cytoskeleton-Plasma Membrane-Cell Wall Continuum
make it clear that plants lack true homologs of classical adhesion proteins of animal cells including integrin, talin, vinculin, filamin, ␣-actinin, and tensin
(Hussey et al., 2002). In this Update, we provide a
brief survey of linker molecules in animal cells and
highlight emerging plant-specific linkers. We hope
that our Update will stimulate more activity in this
exciting and very important area of research.
LINKER MOLECULES BETWEEN THE
CYTOSKELETON AND ECM IN ANIMAL CELLS
Integrins
Physical coupling between cytoskeleton and ECM
is relatively well understood in animal cells. Several
molecules are well known to act as linkers between
elements of the cytoskeleton and ECM components.
The most famous and best-understood are the integrins, which communicate signals between fibronectin, vitronectin, laminin, and other RGD-containing
ECM proteins and the actin cytoskeleton within the
cytoplasm. Integrins allow bidirectional signaling in
all multicellular eukaryotes with the exception of
plants and fungi (Burke, 1999; Hynes, 1999, 2002;
Geiger et al., 2001; Miranti and Brugge, 2002;
Schwartz and Ginsberg, 2002). Surprisingly, Drosophila sp. lacks classical integrin ECM ligands, such as
fibronectin and vitronectin, but there are other RGDcontaining ECM proteins in insects that interact with
integrins (Hynes and Zhao, 2000). At the cytoplasmic
side, integrins bind directly with several actinbinding proteins such as talin, vinculin, filamin, paxillin, ␣-actinin, and tensin (Calderwood et al., 2000;
Critchley, 2000; Geiger et al., 2001; Hynes, 2002;
Miranti and Brugge, 2002; Schwartz and Ginsberg,
2002; Sakai et al., 2003). These actin-binding proteins
then recruit the next cohort of actin-binding proteins
such as profilin, VASP, and Arps, which drive local
actin polymerization (Critchley, 2000; Craig and
Chen, 2003; Sakai et al., 2003). After receiving inputs
at the ECM-plasma membrane interface, integrins
convey this information downstream via several signal transducers including members of the Ras family
of small GTPases and mitogen-activated protein kinases (MAPKs; Juliano, 2002; Schwartz and Ginsberg,
2002). Additionally, integrins signal into the cell interior via focal adhesion kinase, p21-activated kinase,
phosphatidylinositol 3-kinase, integrin-linked kinase, Tyr kinase c-Src, adenylate cyclase, protein kinase A, LIM-kinase, and protein kinase C (Geiger et
al., 2001; Wu and Dedhar, 2001; Zamir and Geiger,
2001a, 2001b; Juliano, 2002; Ingber, 2003b; Sakai et al.,
2003).
Cadherins
Cadherins are calcium-dependent transmembrane
adhesion molecules that play a key role in the maintenance of tissue architecture (Adams and Nelson,
Plant Physiol. Vol. 133, 2003
1998) due to their homophilic cell-to-cell interactions
and abundant interactions with the dynamic actin
cytoskeleton (Kovacs et al., 2002b). Cadherins accumulate at specialized cell-to-cell adhesion domains
known as tight junctions, adherens junctions, and
desmosomes (Adams and Nelson, 1998). Cadherins
interact with the actin cytoskeleton and many signaling molecules like Rac/Rho families of small
GTPases and PI 3-kinase suggesting that cadherins
are, in fact, adhesion-activated-signaling receptors
(Noren et al., 2001; Braga, 2002; Kovacs et al., 2002a).
Several other signaling molecules interact with cadherins including Tyr kinases and phosphatases, lipid
kinases, heterotrimeric GTPases, and MAPKs (Pece
and Gutkind, 2000).
Immunoglobulin Superfamily, Selectins, and
Dystrophin-Glycoprotein Complexes
Like cadherins, these three less studied groups of
cell adhesion receptors also perform homophilic and
heterophilic interactions to hold adjacent cells together. Similarly to integrins and cadherins, they link
ECM with the actin cytoskeleton and employ MAPK
cascades for signal transduction (Hynes, 1999;
Juliano, 2002; McEver, 2002; Michele and Campbell,
2003).
Hyaluronan Receptors CD44 and RHAMM
CD44 and RHAMM are transmembrane glycoproteins present in most vertebrate cells. At the ECM
side, they interact with hyaluronan, but also with
collagen, laminin, and fibronectin. Within the cytoplasm, these transmembrane proteins interact with
the actin cytoskeleton (Culty et al., 1992; Lokeshwar
et al., 1994; Entwistle et al., 1996; Oliferenko et al.,
1999; Föger et al., 2000; Ponta et al., 2003). Hyaluronan receptors are linked to the actin cytoskeleton via
actin-binding proteins including those of the band 4.1
superfamily, ankyrin, and proteins of the ERM family counting ezrin, radixin, and moesin (Bretscher et
al., 2002; Legg et al., 2002; Ponta et al., 2003). Interestingly, CD44 and RHAMM act as receptors for
endocytosis-mediated internalization of hyaluronan
(Culty et al., 1992; Turley et al., 2002; Ponta et al.,
2003). These ECM-cytoskeleton linkers signal into the
cytoplasm via Tyr kinases, MAPKs, Rac1, PI 3-kinase,
and protein kinase C (Oliferenko et al., 2000; Legg et
al., 2002; Turley et al., 2002; Ponta et al., 2003).
Tetraspanin Proteins
Transmembrane proteins of the tetraspanin family,
with large extracellular loops and cytoskeleton interacting cytoplasmic tails, emerge as a new candidate
for the ECM-cytoskeleton linker in multicellular organisms (Lagaudrière-Gesbert et al., 1998; Boucheix
and Rubinstein, 2001; Hemler, 2001; Stipp et al.,
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Baluška et al.
2003). These adhesion proteins have multiple structural functions related to vesicle trafficking and signaling (Kobayashi et al., 2000; Chies et al., 2002;
Fradkin et al., 2002; Hübner et al., 2002). They interact with integrins and cadherins in addition to several other proteins (Yánez-Mó et al., 2000; Berditschevski, 2001). Interestingly, one class of
tetraspanin proteins known as the secretory carrier
membrane proteins, which is important for the synaptic vesicle recycling, is present also in higher
plants, but it is absent from unicellular eukaryotes
(Fernández-Chacón and Südhof, 2000; Hubbard et
al., 2000).
UNIQUE ROLE OF THE ACTIN CYTOSKELETON
IN ECM-CYTOSKELETON COMMUNICATION
A recurring theme common to ECM-cytoskeleton
linkers of animal cells is that these mechanotransducing transmembrane molecules communicate and interact preferentially with the actin cytoskeleton on
the cytoplasmic side of the plasma membrane
(Lagaudrière-Gesbert et al., 1998; Critchley, 2000;
Ponta et al., 2003; Sakai et al., 2003; Stipp et al., 2003).
Inherent association of the actin cytoskeleton with
the plasma membrane is due to interactions among
actin-binding proteins and phosphatidylinositolbisphosphate (PIP2), which localizes to the inner leaflet of the plasma membrane (Nebl et al., 2000; Caroni,
2001). Besides several actin-binding proteins, PIP2
binds also to transmembrane adhesion proteins like
CD44, ICAMs, and syndecan-4 (Heiska et al., 1998;
Couchman et al., 2002). Thus, it is not surprising that
adhesion of the actin cytoskeleton to the plasma
membrane is dependent on PIP2 (Raucher et al.,
2000). PIP2 was localized to discrete domains at the
plasma membrane of maize (Zea mays) root cells.
These resemble profilin-enriched domains and, intriguingly, the phospholipase C activator mastoparan
induced redistribution of PIP2 and remodeling of the
actin cytoskeleton (Baluška et al., 2001d).
Generally, the actin cytoskeleton has been optimized during eukaryotic evolution for acting as a
structural scaffold for diverse signaling complexes
(Juliano, 2002). Recent data from plants support the
concept whereby the dynamic actin cytoskeleton is
closely linked to the signaling cascades initiated at
the plasma membrane (Meagher et al., 1999; Volkmann and Baluška, 1999; Staiger, 2000; Staiger et al.,
2000; McCurdy et al., 2001; Hussey et al., 2002; Šamaj
et al., 2002).
EMERGING LINKER MOLECULES BETWEEN THE
CYTOSKELETON AND CELL WALLS IN PLANTS
Plant cells and, probably fungal cells, are unique in
the whole eukaryotic superkingdom in terms of the
linker molecules between the cytoskeleton and components of the ECM/cell walls. Despite the presence
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of proteins immunologically related to both integrins
and cadherins (Kaminskyj and Heath, 1994; Katembe
et al., 1997; Barthou et al., 1998; Canut et al., 1998;
Faik et al., 1998; Kiba et al., 1998; Baluška et al.,
1999b; Labouré et al., 1999; Laval et al., 1999; Nagpal
and Quatrano, 1999; Swatzell et al., 1999; Sun et al.,
2000), higher plants seem to lack true homologs of
these proteins (Arabidopsis Genome Initiative, 2000).
This situation might be surprising in the face of
rather well-conserved nature of the actin cytoskeleton (Meagher et al., 1999; Staiger et al., 2000; McCurdy et al., 2001; Hussey et al., 2002). One could
argue that the different organization of adhesion sites
in plants is due to the unique molecular nature of
plant cell walls. Generally, the animal ECM is proteinaceous, and protein fibrils are the prime mechanical devices. In contrast, carbohydrates are the major
building blocks of plant cell walls. This implies a
different type of intermolecular interaction for which
integrins and/or cadherins might not be adapted.
However, Drosophila sp. lacks vitronectin and fibronectin and still uses other RGD-containing ECM
proteins to link integrins with the cytoskeleton
(Hynes and Zhao, 2000). Although higher plant cells
also seem to use RGD-containing proteins to connect
their cell walls with the plasma membrane (Schindler
et al., 1989; Katembe et al., 1997; Barthou et al., 1998;
Canut et al., 1998; Faik et al., 1998; Kiba et al., 1998;
Labouré et al., 1999; Laval et al., 1999; Sun et al., 2000;
Mellersh and Heath, 2001), they seem to lack the true
homologs of integrins.
One hypothesis to explain the absence of integrins,
cadherins, and other animal-type linkers in plants is
that plant cells, especially root cells, are often exposed to hyperosmotic stress, which necessitates
rapid and reversible retractions of their protoplasts
from the cell walls, the so-called plasmolytic cycle
(Oparka and Crawford, 1994; Lang-Pauluzzi and
Gunning, 2000; Komis et al., 2003). To maintain mechanical integrity, osmotically stressed plant cells
must retract their protoplasts from their cell walls
almost immediately. Integrin- and cadherin-based
adhesion complexes are apparently too complex to
disintegrate rapidly. Moreover, the Arabidopsis genome lacks not only genes for integrins, but also
genes for actin-associated proteins acting as critical
linkers between integrins and the actin cytoskeleton
including talin, vinculin, filamin, ␣-actinin, and tensin (Hussey et al., 2002). Therefore, plant cells may
have designed other molecules and used other principles for the very dynamic interactions between cytoskeleton and cell walls. Bruce Kohorn discussed
putative plant-specific linker molecules, focusing on
the four most appealing candidates: cell wallassociated kinases (WAKs), arabinogalactan proteins
(AGPs), pectins, and cellulose synthases (Kohorn,
2000). Progress made during the last three years has
resulted in additional candidates including formins,
Plant Physiol. Vol. 133, 2003
Cytoskeleton-Plasma Membrane-Cell Wall Continuum
plant-specific myosins of the class VIII, phospholipase D, and callose synthases.
WAKs and Cell Wall Pectins
Among the emerging plant-specific linkers of the
cytoskeleton with plant cell walls, the WAKs appear
to be the most attractive candidate because they
have, in addition to cell wall and transmembrane
domains, a cytoplasmic Ser/Thr protein kinase domain (He et al., 1996, 1999; Kohorn, 2000, 2001;
Anderson et al., 2001; Wagner and Kohorn, 2001;
Lally et al., 2001). In contrast to the cytoplasmic and
transmembrane domains, which are well-conserved,
the extracellular domains of WAKs are the most variable among the five Arabidopsis WAK isoforms
(WAK1–5) and contain motifs typical for animal proteins such as epidermal growth factor repeats,
tenascin-like, collagen-like, and neurexin-like sequences (He et al., 1999; Anderson et al., 2001). So far,
the functional significance of these motifs remains
unknown, although epidermal growth factor repeats
suggest calcium-mediated dimerization of WAKs. Interestingly, the phosphorylated version of WAK1
was found to be firmly bound to plasma membraneassociated cell wall pectins (Kohorn, 2000, 2001;
Anderson et al., 2001; Wagner and Kohorn, 2001;
Cosgrove, 2000). Plasma membrane-associated pectins have adhesive properties (Mollet et al., 2000;
Iwai et al., 2002; Lord and Mollet, 2002) and undergo
endocytosis in meristematic root cells (Baluška et al.,
2002; Yu et al., 2002). Intriguingly, depriving cells of
boron, which cross-links RGII pectins in cell walls,
results in inhibition of endocytosis of cell wall pectins
(Yu et al., 2002). In addition, boron deprivation exerts
immediate impacts on the cytoskeleton (Yu et al.,
2001, 2003). Similarly, aluminum binds cell wall pectins (Horst et al., 1999), affects the cytoskeleton
(Sivaguru et al., 1999), and induces rapid expression
of WAKs (Sivaguru et al., 2003). Obviously, both
aluminum and boron bind cell wall pectins and affect
events at the cell wall-cytoskeleton interface (Horst et
al., 1999; Yu et al., 2002). All this suggests that complex interactions between pectins, boron, and the
cytoskeleton are important for the assembly of the
cell wall-cytoskeleton continuum as well as for its
maintenance via signal-mediated processes.
An intriguing possibility is that WAKs act as receptors for endocytosis of adhesive cell wall pectins.
Interestingly, WAKs released from cell walls after
pectinase treatments are still in a complex with cell
wall pectins, or their fragments, because antibodies
against pectins detect released WAKs on western
blots (Anderson et al., 2001; Wagner and Kohorn,
2001). This situation is analogous to endocytosis of
hyaluronan via CD44/RHAMM adhesion receptors
in animal cells (Culty et al., 1992; Turley et al., 2002;
Ponta et al., 2003). Plant pectins resemble hyaluronan
in many aspects: Both are abundant components of
Plant Physiol. Vol. 133, 2003
the ECM having structural as well as signaling functions; they both perform endocytic internalization;
and their smaller fragments, internalized presumably
via endocytosis, have important signaling roles at the
plasma membrane and within the cytoplasm (Van
Cutsem and Messiaen, 1994; Thain et al., 1995; Lee
and Spicer, 2000; Baluška et al., 2002).
Besides cell wall pectins, WAK1 also binds to a
glycin-rich cell wall protein AtGRP3 (Park et al.,
2001) and to the 2C-type protein phosphatase KAPP
in the cytoplasm forming an approximately 500-kD
signalosome complex (Anderson et al., 2001). There
are some additional data showing that glycine-rich
proteins (GRPs) could be bound to pectins. Thus,
pectinase activity could release WAKs directly or
through release of GRPs from complexes. Studies
using transgenic plants revealed that WAKs are essential for plant cell elongation (Lally et al., 2001;
Wagner and Kohorn, 2001). In addition to the WAKs,
recent database searches identified a large family of
WAK-like kinases that might also be relevant for
interactions between cell walls and the cytoskeleton
(Verica and He, 2002).
AGPs
Another emerging candidate for signalingmediated interactions between the cell wall and cytoskeleton of plant cells are the AGPs, which are
predicted to have both adhesive and signaling properties (Schultz et al., 1998, 2000; Šamaj et al., 1998a,
1998b, 1999, 2000; Majewska-Sawka and Nothnagel,
2000). Interestingly, AGPs bind to cell wall pectins
(Nothnagel, 1997), and they might interact also with
WAKs because they seem to localize to the same
domains at the plasma membrane of BY-2 protoplasts
(Gens et al., 2000). Although AGPs do not span the
plasma membrane, classical AGPs contain carboxylterminal glycosyl phosphatidylinositol (GPI) anchors
that keep them in tight association with the external
leaflet of the plasma membrane and allow interference with signaling (Schultz et al., 1998, 2000; Oxley
and Bacic, 1999; Svetek et al., 1999; Shi et al., 2003).
These GPI anchors can be cleaved by phospholipase
C in a signal-mediated manner (Sherrier et al., 1999;
Borner et al., 2002) allowing controlled release of
AGPs from the plasma membrane into the cell walls
and the surrounding medium.
AGPs can be precipitated with Yariv reagent,
which specifically binds the carbohydrate moiety of
AGPs. Yariv reagent induces depolarization and ballooning of cells in roots of Arabidopsis (Willats and
Knox, 1996). Moreover, Yariv also inhibits plant cell
growth and can even induce programmed cell death
implicating AGPs in diverse activities of plant cells
(Gao and Showalter, 1999; Majewska-Sawka and
Nothnagel, 2000). Interestingly, SOS5 is a plasma
membrane-associated AGP protein that contains
two-fasciclin-like domains and a C-terminal GPI an485
Baluška et al.
chor (Shi et al., 2003). Root cells of sos5 mutant have
thinner cell walls, aberrant cell shapes, and inhibited
expansion, resembling not only WAK mutants (Lally
et al., 2001; Wagner and Kohorn, 2001), but also
mutants of the actin cytoskeleton (Ramachandran et
al., 2000; Dong et al., 2001; Gilliland et al., 2003) as
well as seedlings dwarfed after long-term treatments
with latrunculin B (Baluška et al., 2001c) or having
aberrant F-actin distribution (Baluška et al., 2001a,b).
All this indicates that the actin cytoskeleton is probably affected in cells of sos5 mutant and that the SOS5
protein might signal from the cell wall-plasma membrane interface toward the actin cytoskeleton in the
cytoplasm. Importantly, both Yariv reagent and latrunculin B also inhibit cell elongation (Willats and
Knox, 1996; Baluška et al., 2001c).
Cellulose Synthase, Microtubules, and Phospholipase D
Cellulose synthases are additional transmembrane
proteins that produce cell wall polymers, span the
plasma membrane, and potentially interact with the
cytoskeleton. Traditionally, due to coalignments of
nascent cellulose microfibrils with cortical microtubules in growing plant cells, cellulose synthases were
considered to be a good candidate for linker molecule. However, it seems that interactions between
cellulose synthases and cortical microtubules are
more indirect (Wiedemeier et al., 2002; Sugimoto et
al., 2003). Recently, phospholipase D has emerged as
a hot candidate for a linker between cortical microtubules and the plasma membrane (Gardiner et al.,
2001; Potocký et al., 2003).
Formins
Unexpectedly, formins represent a new candidate
for putative ECM-cytoskeleton linker in plant cells.
Although these proteins are strictly cytoplasmic and
interact both with the actin- and tubulin-based cytoskeletal systems in eukaryotic cells, some plant
formins are predicted to span the plasma membrane.
Current bioinformatic analysis showed that plant
formins are not only abundant but that there is one
plant-specific group of formins (type-I; Deeks et al.,
2002) that contains a transmembrane domain followed by the ECM Pro-rich domain (Cvrckova, 2000;
Deeks et al., 2002). Importantly, the extracellular domain of plant type-I formins shows similarity to
structural cell wall proteins known as extensins
(Keller, 1993; Cvrckova, 2000). One could expect that
plant type-I formins act as ECM-cytoskeleton linkers
in plant cells because they possess the wellconserved actin cytoskeleton-binding domains FH1
and FH2 (Cvrckova, 2000; Deeks et al., 2002) and
therefore could organize the actin cytoskeleton (Ishizaki et al., 2001; Evangelista et al., 2002; Pruyne et
al., 2002; Sagot et al., 2002; Severson et al., 2002).
486
Unconventional Plant Myosin VIII and
Callose Synthase
Unconventional plant-specific myosin VIII (Reichelt et al., 1999; Reichelt and Kendrick-Jones, 2000) has
emerged as an attractive new cytoskeleton-cell wall
linker because this molecule was found to be accumulated at plasma membrane sites of high callose
depositions such as cell plate, plasmodesmata, and
pit-fields (Baluška et al., 1999a, 1999b, 2000a, 2001a;
Reichelt et al., 1999). A testable concept suggests that
myosin VIII binds directly, or via some further adaptor protein(s), to the callose synthase complexes
(Verma and Hong, 2001; Østergaard et al., 2003).
Because myosin VIII is linked to actin filaments
within the cytoplasm, such binding would inevitably
implicate that callose synthases act as one class of
cytoskeleton-cell wall linkers of plant cells. It is
known that callose synthesis is rapidly up-regulated
upon diverse stress situations (Sivaguru et al., 2000)
including mechanical stress (Jaffe et al., 2002). Moreover, plasma membrane-associated unconventional
myosins are often implicated in diverse sensing and
signaling processes (Mermall et al., 1998). Thus, one
could speculate that plant-specific myosin VIII acts as
a putative sensor for mechanical signals transmitted
through cell walls and impinging upon the plasma
membrane-spanning callose synthases (Verma and
Hong, 2001; Østergaard et al., 2003).
Plasmodesmata and Pit-Fields as Synaptic Adhesion
Domains of Plant Cells
During plasmolysis, retracting protoplasts remain
connected with the plasma membrane via several
cytoplasmic bridges known as Hechtian strands
(Oparka and Crawford, 1994; Lang-Pauluzzi and
Gunning, 2000; Komis et al., 2003). Although these
strands can associate with any domain at the plasma
membrane (Pont-Lezica et al., 1993), they adhere
preferentially at sites where plasmodesmata are inserted, especially if these are grouped into large pitfields (Oparka, 1994; Oparka and Crawford, 1994).
Intriguingly, plasmodesmata/pit-fields are enriched
with F-actin and myosin VIII in some cells of maize
root apices (Baluška et al., 2000a, 2000b, 2001a). We
suggest that plasmodesmata/pit-fields, similarly to
adherens junctions and desmosomes, represent
plant-specific adhesive domains due to putative interactions between callose, callose synthases, myosin
VIII, F-actin, and membranes of the cortical endoplasmic reticulum. The end poles of elongating plant
cells have abundant plasmodesmata, are equipped
with several putative linker molecules reviewed here
(Fig. 1; Baluška et al., 2003b), and perform actindependent endocytosis and recycling of PIN1 (Geldner et al., 2001, 2003) as well as of adhesive cell wall
pectins (Fig. 1; Baluška et al., 2002). Recently, we
proposed that these actin-based adhesion domains at
end poles may represent plant synapses specialized
Plant Physiol. Vol. 133, 2003
Cytoskeleton-Plasma Membrane-Cell Wall Continuum
Figure 1. Schematic presentation of emerging linkers between the cytoskeleton and cell walls in plant cells. We depict here
idealized cross-wall of a root cell with one plasmodesmos (PD) traversed by an element of endoplasmic reticulum (ER).
Adhesive pectins (in orange color) in the cell wall (CW) are known to line the outer face of the plasma membrane (PM) and
to accomplish endocytosis-driven recycling (orange circles). Pectins can directly interact with WAKs, other receptor-like
kinases, and arabinogalactan-proteins. Putative linkers are numbered (see below) and are suggested to interact, directly or
via unknown adaptor molecules, either with actin filaments (green lines) or with microtubules (black lines). Unconventional
myosin of the class VIII (red circles) accumulates within plasmodesmata and may serve as an adaptor between the actin
filaments and callose synthase. Putative linkers between the plant cytoskeleton and cell wall include: 1, WAK; 2,
arabinogalactan-protein (AGP); 3, callose synthase; 4, plant-specific myosin of the class VIII; 5, other receptor-like kinase;
6, formin; 7, cellulose synthase; 8, phospholipase D. The question marks refer to hypothetical interactions.
for polar transport of auxin (Baluška et al., 2003a,
2003b).
FUTURE PROSPECTS
WAKs interacting with pectins emerge as the most
attractive candidate for the plant-specific cytoskeleton-cell wall linker. Unfortunately, nothing is known
about possible interactions of WAKs with the cytoskeleton. WAKs belong to the large family of receptor-like protein kinases (RLKs) that are very abundant
in plants. For instance, 2.5% of the Arabidopsis genome is represented by RLK genes (Shiu and Bleecker,
2001). RLKs can be classified according to predicted
extracellular domains. Another interesting class of
RLKs, with 38 putative genes, consists of lectin receptor protein kinases, which are predicted to bind cell
wall lectins (Hervé et al., 1999; Shiu and Bleecker,
2001). Interestingly, lectin receptor protein kinases can
be activated by pectin oligomers (Riou et al., 2002).
It is becoming increasingly clear that adhesion domains perform mechanosensory functions in eukaryotic cells (Geiger and Bershadsky, 2001; Riveline et
al., 2001). Physical state and local mechanical properties of the ECM are effectively sensed by plasma
membrane-spanning linker molecules accumulated
at these adhesion domains. Linker molecules then
process this information and signal it, via diverse
signal-transducing molecules associated with the dynamic cytoskeleton, preferentially actin-based, furPlant Physiol. Vol. 133, 2003
ther down into the cytoplasm and toward the nucleus
(Katz et al., 2000; Ingber, 2003a, 2003b). This allows
the orchestration of diverse cellular activities according to physical properties of the ECM.
Mechanosensing properties of adhesion domains
are extremely appealing especially for higher plants,
which are known to be very sensitive toward mechanical signals (Bögre et al., 1996; Monshausen and
Sievers, 1998). Retracting protoplasts of plasmolyzing cells are connected to cellular peripheries via
Hechtian strands. These adhesive structures are often
anchored at plasmodesmata and pit-fields that are
enriched with callose, plant-specific myosin of the
class VIII, and calreticulin (Baluška et al., 1999a,
1999b, 2001a). Also, there are reports showing that
mechanical stress affects gating of plasmodesmata
(Oparka and Prior, 1992). All of these data converge
toward a model according to which positive feedback
loops between integrated cytoskeleton and biochemical/mechanical signals at specialized adhesion domains of eukaryotic cells drive cell growth, differentiation, and cell-to-cell communication not only in
animals and humans, but also in supracellular plants.
Received May 22, 2003; returned for revision June 23, 2003; accepted June 30, 2003.
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