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UPDATE ON CYTOSKELETON-PLASMA MEMBRANE-CELL WALL CONTINUUM

Cytoskeleton-Plasma Membrane-Cell Wall Continuum in Plants. Emerging Links Revisited¹

Frantiek Baluka^*, Jozef amaj, 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.., 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..); Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University, 61-701 Pozna, Poland (P.W.); and Institute of Bioorganic Chemistry, Polish Academy of Sciences, 61-704 Pozna, 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; Baluka et al., 2003b). This loss of cellular polarization prevents cells from their cell-to-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 (Baluka 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 retract from the cell wall during osmotic stress-induced 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 Baluka 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 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

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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 RGD-containing ECM proteins in insects that interact with integrins (Hynes and Zhao, 2000). At the cytoplasmic side, integrins bind directly with several actin-binding 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, 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., 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

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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 phosphatidylinositol-bisphosphate (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 (Baluka 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 Baluka, 1999; Staiger, 2000; Staiger et al., 2000; McCurdy et al., 2001; Hussey et al., 2002; amaj et al., 2002).

	EMERGING LINKER MOLECULES BETWEEN THE CYTOSKELETON AND CELL WALLS IN PLANTS

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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 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; Baluska 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 wall-associated 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-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 membrane-associated 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 (Baluska 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 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; Baluska 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 signaling-mediated 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; amaj 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 carboxyl-terminal 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 anchor (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 (Baluska et al., 2001c) or having aberrant F-actin distribution (Baluska 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; Baluska 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; Potock 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 well-conserved 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).

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 (Baluska 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 (Baluska 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; Baluska et al., 2003b), and perform actin-dependent endocytosis and recycling of PIN1 (Geldner et al., 2001, 2003) as well as of adhesive cell wall pectins (Fig. 1; Baluska et al., 2002). Recently, we proposed that these actin-based adhesion domains at end poles may represent plant synapses specialized for polar transport of auxin (Baluska et al., 2003a, 2003b).

View larger version (23K): [in this window] [in a new window]   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.

	FUTURE PROSPECTS

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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, further 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 (Baluska 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.

	FOOTNOTES

 
www.plantphysiol.org/cgi/doi/10.1104/pp.103.027250.

¹ This work was supported by the Alexander von Humboldt Foundation (Bonn; to F.B., J.S., and P.W.).

^* Corresponding author; e-mail baluska{at}uni-bonn.de; fax 49-228-739004.

	LITERATURE CITED

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Adams CL, Nelson WJ (1998) Cytomechanics of cadherin-mediated cell-cell adhesion. Curr Opin Cell Biol 10: 572-577[CrossRef][Web of Science][Medline]

Anderson CM, Wagner TA, Perret M, He Z-H, He D, Kohorn BD (2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47: 197-206[CrossRef][Web of Science][Medline]

Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815[CrossRef][Medline]

Baluska F, Barlow PW, Volkmann D (2000a) Actin and myosin VIII in developing root cells. In CJ Staiger, F Baluska, D Volkmann, PW Barlow, eds, Actin: A Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 457-476

Baluska F, Busti E, Dolfini S, Gavazzi G, Volkmann D (2001a) Lilliputian mutant of maize shows defects in organization of actin cytoskeleton. Dev Biol 236: 478-491[CrossRef][Web of Science][Medline]

Baluska F, Cvrcková F, Kendrick-Jones J, Volkmann D (2001b) Sink plasmodesmata as gateways for phloem unloading: myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 126: 39-46[Free Full Text]

Baluska F, Hlavacka A, amaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells: insights from brefeldin A-induced compartments. Plant Physiol 130: 422-443[Abstract/Free Full Text]

Baluska F, Jásik J, Edelmann HG, Salajová T, Volkmann D (2001c) Latrunculin B induced plant dwarfism: plant cell elongation is F-actin dependent. Dev Biol 231: 113-124[CrossRef][Web of Science][Medline]

Baluska F, amaj J, Menzel D (2003a) Polar transport of auxin: carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13: 282-285[CrossRef][Web of Science][Medline]

Baluska F, amaj J, Napier R, Volkmann D (1999a) Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 19: 481-488[CrossRef][Web of Science][Medline]

Baluska F, amaj J, Volkmann D (1999b) Proteins reacting with cadherin and catenin antibodies are present in maize showing tissue-, domain-, and development-specific associations with ER membranes and actin microfilaments in root cells. Protoplasma 206: 174-187

Baluska F, Volkmann D, Barlow PW (1997) Nuclear components with microtubule organizing properties in multicellular eukaryotes: functional and evolutionary considerations. Int Rev Cytol 175: 91-135[Web of Science][Medline]

Baluska F, Volkmann D, Barlow PW (2000b) Actin-based domains of the 'cell periphery complex' and their associations with polarized 'cell bodies' in higher plants. Plant Biol 2: 253-267[CrossRef]

Baluska F, von Witsch M, Peters M, Hlavaècka A, Volkmann D (2001d) Mastoparan alters subcellular distribution of profilin and remodels F-actin cytoskeleton in cells of maize root apices. Plant Cell Physiol 42: 912-922[Abstract/Free Full Text]

Baluska F, Wojtaszek P, Volkmann D, Barlow PW (2003b) The architecture of polarized cell growth: the unique status of elongating plant cells. BioEssays 25: 569-576[CrossRef][Web of Science][Medline]

Barthou H, Petitprez M, Brière C, Souvré A, Alibert G (1998) RGD-mediated membrane-matrix adhesion triggers agarose-induced embryoid formation in sunflower protoplasts. Protoplasma 206: 143-151[CrossRef][Web of Science]

Berditschevski F (2001) Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 114: 4143-4151[Abstract/Free Full Text]

Bretscher A, Edwards K, Fehon RG (2002) ERM proteins and Merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3: 586-599[CrossRef][Web of Science][Medline]

Bögre L, Ligterink W, Heberle-Bors E, Hirt H (1996) Mechanosensors in plants. Nature 383: 489-490[CrossRef][Medline]

Borner GHH, Sherrier DJ, Stevens TJ, Arkin IT, Dupree P (2002) Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a genomic analysis. Plant Physiol 129: 486-499[Abstract/Free Full Text]

Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci 58: 1189-1205[CrossRef][Web of Science][Medline]

Braga V (2002) Cell-cell adhesion and signalling. Curr Opin Cell Biol 14: 546-556[CrossRef][Web of Science][Medline]

Burke RD (1999) Invertebrate integrins: structure, function, and evolution. Int Rev Cytol 191: 257-284[Web of Science][Medline]

Calderwood DA, Shattil SJ, Ginsberg MH (2000) Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J Biol Chem 275: 22607-22610[Free Full Text]

Canut H, Carrasco A, Galaud J-P, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16: 63-71[CrossRef][Web of Science][Medline]

Caroni P (2001) Actin cytoskeleton regulation through modulation of PI(4, 5)P₂ rafts. EMBO J 20: 4332-4336[CrossRef][Web of Science][Medline]

Chies R, Nobbio L, Edomi P, Schenone A, Schneider C, Brancolini C (2002) Alterations in the Arf6-regulated plasma membrane endosomal recycling pathway in cells overexpressing the tetraspan protein Gas3/PMP22. J Cell Sci 116: 987-999

Couchman JR, Vogt S, Lim S-T, Lim Y, Oh E-S, Prestwich GD, Theibert A, Lee W, Woods A (2002) Regulation of inositol phospholipid binding and signaling through syndecan-4. J Biol Chem 277: 49296-49303[Abstract/Free Full Text]

Craig SW, Chen H (2003) Lamellipodia protrusion: moving interactions of vinculin and Arp2/3. Curr Biol 13: R236-R238[Medline]

Critchley DR (2000) Focal adhesions: the cytoskeletal connection. Curr Opin Cell Biol 12: 133-139[CrossRef][Web of Science][Medline]

Cosgrove D (2000) Plant cell walls: wall-associated kinases and cell expansion. Curr Biol 11: R558-R559

Culty M, Nguyen HA, Underhill CB (1992) The hyaluronan receptor (CD44) participates in the uptake and degradation of hyaluronan. J Cell Biol 116: 1055-1062[Abstract/Free Full Text]

Cvrckova F (2000) Are plant formins integral membrane proteins? Genome Biol 1: 001.1-001.7

Deeks MJ, Hussey PJ, Davies B (2002) Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 7: 492-498[CrossRef][Medline]

Dong C-H, Xia G-X, Hong Y, Ramachandran S, Kost B, Chua N-H (2001) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13: 1333-1346[Abstract/Free Full Text]

Entwistle J, Hall CL, Turley EA (1996) HA receptors: regulators of signalling to the cytoskeleton. J Cell Biochem 61: 569-577[CrossRef][Web of Science][Medline]

Evangelista M, Pruyne M, Amberg DC, Boone C, Bretscher A (2002) Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 4: 32-41[CrossRef][Web of Science][Medline]

Faik A, Labouré AM, Gulino D, Mandaron P, Falconet D (1998) A plant surface protein sharing structural properties with animal integrins. Eur J Biochem 253: 552-559[Medline]

Fernández-Chacón R, Südhof TC (2000) Novel SCAMPs lacking NPF repeats: ubiquitous and synaptic vesicle-specific forms implicate SCAMPs in multiple membrane-trafficking functions. J Neurosci 20: 7941-7950[Abstract/Free Full Text]

Föger N, Marhaba R, Zöller M (2000) Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells. J Cell Sci 114: 1169-1178

Fowler JE, Quatrano RS (1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu Rev Cell Dev Biol 13: 697-743[CrossRef][Web of Science][Medline]

Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN (2002) Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci USA 99: 13663-13668[Abstract/Free Full Text]

Gao M, Showalter AM (1999) Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. Plant J 19: 321-331[CrossRef][Web of Science][Medline]

Gardiner JC, Harper JDI, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13: 2143-2158[Abstract/Free Full Text]

Geiger B, Bershadsky A (2001) Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 13: 584-592[CrossRef][Web of Science][Medline]

Geiger B, Bershadsky A, Pankov R, Yamada KM (2001) Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2: 793-805[CrossRef][Web of Science][Medline]

Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230[CrossRef][Web of Science][Medline]

Geldner N, Friml J, Stierhof Y-D, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425-428[CrossRef][Medline]

Gens JS, Fujiki M, Pickard BG (2000) Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212: 115-134[CrossRef][Web of Science][Medline]

Gillespie PG, Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413: 194-202[CrossRef][Medline]

Gilliland LU, Pawloski L, Kandasamy MK, Meagher RB (2003) The Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. Plant J 33: 319-328[CrossRef][Web of Science][Medline]

Goldman MA (2003) The epigenetics of the cell. Genome Biol 4: 309[CrossRef][Medline]

Green PB (1999) Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms. Am J Bot 86: 1059-1076[Abstract/Free Full Text]

He Z-H, Cheeseman I, He D, Kohorn BD (1999) A cluster of five cell wall-associated kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis Plant Mol Biol 39: 1189-1196

He Z-H, Fujiki M, Kohorn BD (1996) A cell wall-associated receptor-like protein kinase. J Biol Chem 271: 19789-19793[Abstract/Free Full Text]

Heath IB (2001) Bridging the divide: cytoskeleton-plasma membrane-cell wall interactions in growth and development. In RJ Howard, NAR Gows, eds, The Mycota VIII. Biology of the Fungal Cell. Springer-Verlag, Berlin, pp 201-223

Heiska L, Alfthan K, Gronholm M, Vilja P, Vaheri A, Carpen O (1998) Association of ezrin with intracellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2): regulation by phosphatidylinositol 4, 5-bisphosphate. J Biol Chem 273: 21893-21900[Abstract/Free Full Text]

Hemler ME (2001) Specific tetraspanin functions. J Cell Biol 155: 1103-1107[Abstract/Free Full Text]

Hervé C, Serres J, Dabos P, Canut H, Barre A, Rougé P, Lescure B (1999) Characterization of the Arabidopsis lecRK-a genes: members of a superfamily encoding putative receptors with an extracellular domain homologous to legume lectins. Plant Mol Biol 39: 671-682[CrossRef][Web of Science][Medline]

Horst WJ, Schmohl N, Kollmeier M, Baluska F, Sivaguru M (1999) Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215: 163-174[CrossRef]

Hubbard C, Singleton D, Rauch M, Jaysinghe S, Cafiso D, Castle D (2000) The secretory carrier membrane protein family: structure and membrane topology. Mol Biol Cell 11: 2933-2947[Abstract/Free Full Text]

Hübner K, Windoffer R, Hutter H, Leube RE (2002) Tetraspan vesicle membrane proteins: synthesis, subcellular localization, and functional properties. Int Rev Cytol 214: 103-159[Web of Science][Medline]

Hussey PJ, Allwood EG, Smertenko AP (2002) Actin-binding proteins in the Arabidopsis genome database: properties of functionally distinct plant actin-depolymerizing factors/cofilins. Philos Trans R Soc Lond B 357: 791-798[Abstract/Free Full Text]

Hynes RO (1999) Cell adhesion: old and new questions. Trends Cell Biol 9: M33-M37[CrossRef][Web of Science][Medline]

Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687[CrossRef][Web of Science][Medline]

Hynes RO, Zhao Q (2000) The evolution of cell adhesion. J Cell Biol 150: F89-F95

Ingber DE (2003a) Tensegrity: I. Cell structure and hierarchical systems biology. J Cell Sci 116: 1157-1173[Abstract/Free Full Text]

Ingber DE (2003b) Tensegrity: II. How structural networks influence cellular information-processing networks. J Cell Sci 116: 1397-1408[Abstract/Free Full Text]

Ishizaki T, Morishima Y, Okamoto M, Furuyashiki M, Kato T, Narumiya S (2001) Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nat Cell Biol 3: 8-14[CrossRef][Web of Science][Medline]

Iwai H, Masaoka N, Ishii T, Satoh S (2002) A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem. Proc Nat Acad Sci USA 99: 16319-16324[Abstract/Free Full Text]

Jaffe MJ, Leopold AC, Staples RC (2002) Thigmo responses in plants and fungi. Am J Bot 89: 375-382[Abstract/Free Full Text]

Janmey PA (1998) The cytoskeleton and cell signalling: component localization and mechanical coupling. Physiol Rev 78: 763-781[Abstract/Free Full Text]

Juliano RL (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42: 283-323[CrossRef][Web of Science][Medline]

Kaminskyj SGW, Heath IB (1994) Integrin and spectrin homologues and cytoplasm-wall adhesion in tip growth. J Cell Sci 108: 849-856

Katembe WJ, Swatzell CJ, Makaroff CA, Kiss JZ (1997) Immunolocalization of integrin-like proteins in Arabidopsis and Chara. Physiol Plant 99: 7-14[CrossRef][Medline]

Katz BZ, Zamir E, Bershadsky A, Kam Z, Yamada KM, Geiger B (2000) Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Mol Biol Cell 11: 1047-1060[Abstract/Free Full Text]

Keller B (1993) Structural cell wall proteins. Plant Physiol 101: 1127-1130[Medline]

Kiba A, Sugimoto M, Toyoda K, Ichinose Y, Yamada T, Shiraishi T (1998) Interaction between cell wall and plasma membrane via RGD motif is implicated in plant defense responses. Plant Cell Physiol 39: 1245-1249[Abstract/Free Full Text]

Kobayashi T, Vischer UM, Rosnoblet C, Lebrand C, Lindsay M, Parton RG, Kruithof EKO, Gruenberg J (2000) The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell 11: 1829-1843[Abstract/Free Full Text]

Kohorn BD (2000) Plasma membrane-cell wall contacts. Plant Physiol 124: 31-38[Free Full Text]

Kohorn BD (2001) Waks: cell wall associated kinases. Curr Opin Cell Biol 13: 529-533[CrossRef][Web of Science][Medline]

Komis G, Apostolakos P, Galatis B (2003) Actomyosin is involved in the plasmolytic cycle: gliding movement of the deplasmolyzing protoplast. Protoplasma 221: 245-256[Medline]

Kovacs EM, Ali RG, McCormack AJ, Yap AS (2002a) E-cadherin homophilic ligation directly signals through Rac and PI3-kinase to regulate adhesive contacts. J Biol Chem 277: 6708-6718[Abstract/Free Full Text]

Kovacs EM, Goodwin RG, Ali AD, Paterson AD, Yap AS (2002b) Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol 12: 379-382[CrossRef][Web of Science][Medline]

Labouré AM, Faik A, Mandaron P, Falconet D (1999) RGD-dependent growth of maize calluses and immunodetection of an integrin-like protein. FEBS Lett 442: 123-128[CrossRef][Web of Science][Medline]

Lagaudrière-Gesbert C, Lebel-Binay S, Hubeau C, Frandelizi D, Conjeaud H (1998) Signaling through the tetraspanin CD82 triggers its association with the cytoskeleton leading to sustained morphological changes and T cell activation. Eur J Immunol 28: 4332-4344[CrossRef][Medline]

Lally D, Ingmire P, Tong H-Y, He Z-H (2001) Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. Plant Cell 13: 1317-1332[Abstract/Free Full Text]

Lang-Pauluzzi I, Gunning BES (2000) A plasmolytic cycle: the fate of cytoskeletal elements. Protoplasma 212: 174-185[CrossRef][Web of Science]

Laval V, Chabannes M, Carriere M, Canut H, Barre A, Rouge P, Pont-Lezica R, Galaud J (1999) A family of Arabidopsis plasma membrane receptors presenting animal beta-integrin domains. Biochim Biophys Acta 1435: 61-70[CrossRef][Medline]

Lee JY, Spicer AP (2000) Hyaluronan: a multifunctional, megaDalton, stealth molecule. Curr Opin Cell Biol 12: 581-586[CrossRef][Web of Science][Medline]

Legg JW, Lewis CA, Parsons M, Ng T, Isacke CM (2002) A novel PKC-regulated mechanism controls CD44-ezrin association and directional cell motility. Nat Cell Biol 4: 399-407[CrossRef][Web of Science][Medline]

Lintilhac PM, Vesecky TB (1984) Stress-induced alignment of division plane in plant tissues in vitro. Nature 307: 363-364[CrossRef]

Lokeshwar VB, Fregien N, Bourguignon LYW (1994) Ankyrin-binding domain of CD44(GP85) is required for the expression of hyaluronic acid-mediated adhesion function. J Cell Biol 126: 1099-1109[Abstract/Free Full Text]

Lord EM, Mollet J-C (2002) Plant cell adhesion: A bioassay facilitates discovery of the first pectin biosynthetic gene. Proc Natl Acad Sci USA 99: 15843-15845[Free Full Text]

Lucas WJ, Ding B, van der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 125: 435-476[CrossRef][Web of Science]

Lynch TM, Lintilhac PM (1997) Mechanical signals in plant development: a new method for single cell studies. Dev Biol 181: 246-256[CrossRef][Web of Science][Medline]

Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122: 3-9[Free Full Text]

McCurdy DW, Kovar DR, Staiger CJ (2001) Actin and actin-binding proteins in higher plants. Protoplasma 215: 89-104[CrossRef][Web of Science][Medline]

McEver RP (2002) Selectins: lectins that initiate cell adhesion under flow. Curr Opin Cell Biol 14: 581-586[CrossRef][Web of Science][Medline]

Meagher RB, McKinney EC, Kandasamy MK (1999) Isovariant dynamics expand and buffer the responses of complex systems: the diverse plant actin gene family. Plant Cell 11: 995-1006[Free Full Text]

Mellersh DG, Heath MC (2001) Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 13: 413-424[Abstract/Free Full Text]

Mermall V, Post PL, Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279: 527-533[Abstract/Free Full Text]

Michele DE, Campbell KP (2003) Dystrophin-glycoprotein complex: posttranslational processing and dystroglycan function. J Biol Chem 278: 15457-15460[Free Full Text]

Miller D, de Ruijter NCA, Emons AMC (1997a) From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J Exp Bot 48: 1881-1896

Miller D, Hable W, Gottwald J, Ellard-Ivey M, Demura T, Lomax T, Carpita N (1997b) Connections: the hard wiring of the plant cell for perception, signaling, and response. Plant Cell 9: 2105-2117[Medline]

Miranti CK, Brugge JS (2002) Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol 4: 83-90[CrossRef][Web of Science][Medline]

Mollet J-C, Park S-Y, Nothnagel EA, Lord EM (2000) A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12: 1737-1749[Abstract/Free Full Text]

Monshausen GB, Sievers A (1998) Weak mechanical stimulation causes hyperpolarisation in root cells of Lepidium. Bot Acta 111: 303-306

Nagpal P, Quatrano RS (1999) Isolation and characterization of cDNA clone from Arabidopsis thaliana with partial sequence similarity to integrins. Gene 230: 33-40[CrossRef][Web of Science][Medline]

Nebl T, Oh SW, Luna EJ (2000) Membrane cytoskeleton: PIP₂ pulls the strings. Curr Biol 10: R351-R354[CrossRef][Web of Science][Medline]

Noren NK, Niessen CM, Gumbiner BM, Burridge K (2001) Cadherin engagement regulates Rho family GTPases. J Biol Chem 276: 33305-33308[Abstract/Free Full Text]

Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174: 195-291[Web of Science][Medline]

Oliferenko S, Kaverina I, Small JV, Huber LA (2000) Hyaluronic acid (HA) binding to CD44 activates Rac1 and induces lamellipodia outgrowth. J Cell Biol 148: 1159-1164[Abstract/Free Full Text]

Oliferenko S, Paiha K, Harder T, Gerke V, Scwärzler C, Schwarz H, Beug H, Günthert U, Huber LA (1999) Analysis of CD44-containing lipid rafts: recruitment of annexin II and stabilization by the actin cytoskeleton. J Cell Biol 146: 843-854[Abstract/Free Full Text]

Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytol 126: 571-591[CrossRef]

Oparka KJ, Crawford JW (1994) Behavior of plasma membrane, cortical endoplasmic reticulum and plasmodesmata during plasmolysis of onion epidermal cells. Plant Cell Environ 17: 163-171[CrossRef]

Oparka KJ, Prior DAM (1992) Direct evidence for pressure-generated closure of plasmodesmata. Plant J 2: 741-750[Web of Science]

Orlando V (2003) Polycomb, epigenomes, and control of cell identity. Cell 112: 599-606[CrossRef][Web of Science][Medline]

Østergaard L, Petersen M, Mattsson O, Mundy J (2003) An Arabidopsis callose synthase. Plant Mol Biol 49: 559-566

Oxley D, Bacic A (1999) Structure of the glycosylphasphatidylinositol anchor of an arabinogalactan protein from Pyrus communis suspension-cultured cells. Proc Natl Acad Sci USA 25: 14246-14251

Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-Martins G, Park OK (2001) Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine rich protein AtGRP-3. J Biol Chem 276: 26688-26693[Abstract/Free Full Text]

Pece S, Gutkind JS (2000) Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J Biol Chem 275: 41227-41233[Abstract/Free Full Text]

Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4: 33-45[CrossRef][Web of Science][Medline]

Pont-Lezica RF, McNally JG, Pickard BG (1993) Wall-to-membrane linkers in onion epidermis: some hypotheses. Plant Cell Environ 16: 111-123[CrossRef]

Potock M, Eliás M, Profotová B, Novotná Z, Valentová O, Hársky V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217: 122-130[Web of Science][Medline]

Pruyne M, Evangelista M, Yang C, Bi E, Zigmond S, Bretscher A, Boone C (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615[Abstract/Free Full Text]

Ramachandran S, Christensen HEM, Ishimaru Y, Dong C-H, Chao-Ming W, Cleary AL, Chua N-H (2000) Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol 124: 1637-1647[Abstract/Free Full Text]

Raucher D, Stauffer T, Chen W, Shen K, Guo S, York JD, Sheetz MP, Meyer T (2000) Phosphatodylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100: 221-228[CrossRef][Web of Science][Medline]

Reichelt S, Kendrick-Jones J (2000) Myosins. In CJ Staiger, F Baluska, D Volkmann, PW Barlow, eds, Actin: A Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 29-44

Reichelt S, Knight AE, Hodge TP, Baluska F, amaj J, Volkmann D, Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19: 555-569[CrossRef][Web of Science][Medline]

Riou C, Hervé C, Pacquit V, Dabos P, Lescure B (2002) Expression of an Arabidopsis lectin kinase receptor gene, lecRK-a1, is induced during senescence, wounding and in response to oligogalacturonic acids. Plant Physiol Biochem 40: 431-438[CrossRef]

Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD (2001) Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153: 1175-1185[Abstract/Free Full Text]

Rørth P (2003) Communication by touch: role of cellular extensions in complex animals. Cell 112: 595-598[CrossRef][Web of Science][Medline]

Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4: 626-631[Web of Science][Medline]

Sakai T, Li S, Docheva D, Grashoff C, Sakai K, Kostka G, Braun A, Pfeifer A, Yurchenco PD, Fässler R (2003) Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev 17: 926-940[Abstract/Free Full Text]

amaj J, Baluska F, Bobák M, Volkmann D (1998a) Extracellular matrix surface networks of embryogenetic units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep 18: 369-374[CrossRef]

amaj J, Baluska F, Volkmann D (1998b) Cell-specific expression of two arabinogalactan-protein epitopes recognized by monoclonal antibodies JIM8 and JIM13 in maize roots. Protoplasma 204: 1-12

amaj J, Braun M, Baluska F, Ensikat H-J, Tsumuraya Y, Volkmann D (1999) Arabinogalactan-protein epitopes at the surface of maize roots: LM2 epitope is specific to root hairs. Plant Cell Physiol 40: 874-883[Abstract/Free Full Text]

amaj J, Ovecka M, Hlavacka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L et al. (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip-growth. EMBO J 21: 3296-3306[CrossRef][Web of Science][Medline]

amaj J, amajová O, Peters M, Baluska F, Lichtscheidl IK, Knox JP, Volkmann D (2000) Immunolocalization of LM2 arabinogalactan-protein epitope associated with endomembranes of plant cells. Protoplasma 212: 186-196[CrossRef][Web of Science]

Schindler M, Meiners S, Cheresh DA (1989) RGD-dependent linkage between plant cell wall and plasma membrane: consequences for growth. J Cell Biol 108: 1955-1965[Abstract/Free Full Text]

Schultz C, Gilson P, Oxley D, Youl J, Bacic A (1998) GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci 3: 426-431[CrossRef][Web of Science]

Schultz C, Johnson KL, Currie G, Bacic A (2000) The classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12: 1751-1768[Abstract/Free Full Text]

Schwartz MA, Ginsberg MH (2002) Networks and crosstalk: integrin signaling spreads. Nat Cell Biol 4: E65-E68[CrossRef][Web of Science][Medline]

Severson AF, Baillie DL, Bowerman B (2002) A formin homology protein and a profilin are required for cytokinesis and Arp2/3-independent assembly of cortical microfilaments in C. elegans. Curr Biol 12: 2066-2075[CrossRef][Web of Science][Medline]

Sheetz MP (2001) Cell control by membrane-cytoskeleton adhesion. Nat Rev Mol Cell Biol 2: 392-396[CrossRef][Web of Science][Medline]

Sherrier DJ, Prime TA, Dupree P (1999) Glycosylphosphatidylinositol-anchored cell-surface proteins from Arabidopsis. Electrophoresis 20: 2027-2035[CrossRef][Web of Science][Medline]

Shi H, Kim YS, Guo Y, Stevenson B, Zhu J-K (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15: 19-32[Abstract/Free Full Text]

Shiu S-H, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98: 10763-10768[Abstract/Free Full Text]

Sipiczki M, Yamaguchi M, Grallert A, Takeo K, Zilahi E, Bozsik A, Miklos I (2000) Role of cell shape in determination of the division plane in Schizosaccharomyces pombe: random orientation of septa in spherical cells. J Bacteriol 182: 1693-1701[Abstract/Free Full Text]

Sivaguru M, Baluska F, Volkmann D, Felle H, Horst WJ (1999) Impacts of aluminum on cytoskeleton of maize root apex: short-term effects on distal part of transition zone. Plant Physiol 119: 1073-1082[Abstract/Free Full Text]

Sivaguru M, Ezaki B, He Z-H, Tong H, Osawa H, Baluska F, Volkmann D, Matsumoto H (2003) Aluminum induced gene expression and protein localization of cell wall-associated receptor kinase in Arabidopsis thaliana. Plant Physiol 132: 2256-2266[Abstract/Free Full Text]

Sivaguru M, Fujiwara T, Yang Z, Osawa H, amaj J, Baluska F, Mori T, Volkmann D, Maeda T, Matsumoto H (2000) Aluminum-induced 1-3--glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata: a new mechanism of Al toxicity in plants. Plant Physiol 124: 991-1018[Abstract/Free Full Text]

Smith LG (2001) Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2: 33-39[CrossRef][Web of Science][Medline]

Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 257-288[CrossRef][Web of Science]

Staiger CJ, Baluska F, Volkmann D, Barlow PW (2000) Actin: A Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic Publishers, Dordrecht, The Netherlands

Stipp CS, Kolesnikova TV, Hemler ME (2003) Functional domains in tetraspanin proteins. Trends Biochem Sci 28: 106-112[CrossRef][Web of Science][Medline]

Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO (2003) Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15: (in press)

Svetek J, Yadav MP, Nothnagel EA (1999) Presence of a glycosylphasphatidylinositol lipid anchor on rose arabinogalactan proteins. J Biol Chem 274: 14724-14733[Abstract/Free Full Text]

Swatzell LJ, Edelmann RE, Makaroff CA, Kiss JZ (1999) Integrin-like proteins are localized to plasma membrane fractions, not plastids, in Arabidopsis. Plant Cell Physiol 40: 173-183[Abstract/Free Full Text]

Sun Y, Qian H, Xu X, Yen L, Sun D (2000) Integrin-like proteins in the pollen tube: detection, localization and function. Plant Cell Physiol 41: 1136-1142[Abstract/Free Full Text]

Thain JF, Gubb IR, Wildon DC (1995) Depolarization of tomato leaf cells by oligogalacturonide elicitors. Plant Cell Environ 18: 211-214[CrossRef]

Turley EA, Noble PW, Bourguignon LYW (2002) Signaling properties of hyaluronan receptors. J Biol Chem 277: 4589-4592[Free Full Text]

Van Cutsem P, Messiaen J (1994) Biological effects of pectin fragments in plant cells. Acta Bot Neerl 43: 231-245

Verica JA, He Z-H (2002) The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiol 129: 455-459[Free Full Text]

Verma DPS, Hong Z (2001) Plant callose synthase complexes. Plant Mol Biol 47: 693-701[CrossRef][Web of Science][Medline]

Volkmann D, Baluska F (1999) The actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47: 135-154[CrossRef][Web of Science][Medline]

Wagner TA, Kohorn BD (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13: 303-318[Abstract/Free Full Text]

Wiedemeier AMD, Judy-March JE, Hocart CH, Wasteneys GO, Williamson RE, Baskin TI (2002) Mutant alleles of Arabidopsis RADIALLY SWOLLEN 4 and 7 reduce growth anisotropy without altering the transverse orientation of cortical microtubules or cellulose microfibrils. Development 129: 4821-4830

Willats WGT, Knox JP (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of -glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J 9: 919-925[CrossRef][Web of Science][Medline]

Wojtaszek P (2000) Genes and plant cell walls: a difficult relationship. Biol Rev 75: 437-475[Medline]

Wojtaszek P (2001) Organismal view of a plant and a plant cell. Acta Biochim Polon 48: 443-451[Medline]

Wu C, Dedhar S (2001) Integrin linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 155: 505-510[Abstract/Free Full Text]

Wyatt SE, Carpita NC (1993) The plant cytoskeleton-cell wall continuum. Trends Cell Biol 3: 413-417[CrossRef][Medline]

Yánez-Mó M, Tejedor R, Rousselle P, Sánchez-Madrid F (2000) Tetraspanins in intercellular adhesion of polarized epithelial cells: spatial and functional relationship to integrins and cadherins. J Cell Sci 114: 577-587

Yu Q, Baluska F, Jasper F, Menzel D, Volkmann D, Goldbach HE (2003) Short-term boron deprivation enhances levels of cytoskeletal proteins in maize, but not zucchini, root apices. Physiol Plant 117: 1-9[CrossRef]

Yu Q, Hlavacka A, Matoh T, Volkmann D, Menzel D, Goldbach HE, Baluska F (2002) Short-term boron deprivation inhibits endocytosis of cell wall pectins in meristematic cells of maize and wheat root apices. Plant Physiol 130: 415-421[Abstract/Free Full Text]

Yu Q, Wingender R, Schulz M, Baluska F, Goldbach H (2001) Short-term boron deprivation induces increased expression of cytoskeletal proteins in Arabidopsis roots. Plant Biol 6: 1-6

Zamir E, Geiger B (2001a) Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sci 114: 3583-3590

Zamir E, Geiger B (2001b) Components of cell-matrix adhesions. J Cell Sci 114: 3577-3579

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