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pb2613.qxd 11/26/1999 9:29 AM Page 521 521 If walls could talk Commentary Janet Braam The plant cell wall is very complex, both in structure and function. The wall components and the mechanical properties of the wall have been implicated in conveying information that is important for morphogenesis. Proteoglycans, fragments of polysaccharides and the structural integrity of the wall may relay signals that influence cellular differentiation and growth control. Furthering our knowledge of cell wall structure and function is likely to have a profound impact on our understanding of how plant cells communicate with the extracellular environment. Addresses Biochemistry and Cell Biology, Rice University, Houston, TX 77251-1892, USA; e-mail: [email protected] thallus and rhizoid cells of Fucus [4]. The wall can therefore restrict and maintain cellular differentiation. Surprisingly and significantly, thallus or rhizoid daughter cells switch developmental fate when they physically contact the wall remnants of laser-ablated cells of the other cell type [4]. For example, thallus daughter cells that come into close contact with the remains of rhizoid cell walls take on rhizoid cell identity. Because close association of the cell wall appears to be required for the cell identity switch, it is likely that the wall components of the two cell types differ, and that at least a subset of these characteristic distinctions function as differentiation signals. The identities and modes of action of these wall molecules remain unknown. Current Opinion in Plant Biology 1999, 2:521–524 1369-5266/99/$ — see front matter © 1999 Elsevier Science Ltd. All rights reserved. Abbreviation AGP arabinogalactan protein Introduction Plant development requires coordination and communication among the cells of various organs. The identity of cells is strongly influenced by their position during plant morphogenesis rather than by their developmental lineage [1]. Furthermore, the extent and orientation of cellular expansion must be synchronized with that of neighboring cells because the walls between them act as structural restraints to movement. Neighboring plant cells communicate through plasmodesmata (the regulated intercellular channels that connect the plasma membranes, the endoplasmic reticulum membranes and lumens, and the cytosol of adjacent cells) [2]. Many integral plasma membrane proteins also have features that typify receptors capable of transducing external ligand binding into intracellular messages [3]. In addition, plant hormones move through tissues as signals. Apoplast factors can also act as signals and, in addition, the structural properties of the wall may serve to relay messages to the cell interior. In this review we discuss the evidence for the involvement of two molecules, a proteoglycan and a cellwall polysaccharide fragment, in cell–to–cell signaling. In addition, we discuss the potential role of mechanical strain in triggering cellular responses that maintain cell expansion rates and turgor. Intercellular signals from walls during embryogenesis The cell wall of the marine alga Fucus has a profound ability to control the differentiation potential of developing cells. Only embryonic cells from which the walls are removed are totipotent and able to give rise to both the Antibodies that recognize specific wall components are known to identify differing epitopes among distinct cell types or developmental stages [5]. These findings are consistent with the idea that walls harbor differentiation markers. Whether these markers are active components that regulate and maintain cellular identity, or whether their presence is just a consequence of the morphogenetic events has yet to be determined. As in Fucus, the embryogenesis of higher plants might depend on components of the extracellular matrix. Evidence has come from studies of somatic embryogenesis, a process that resembles embryogenesis in which the somatic cells of mature plants undergo redifferentiation in vitro and can give rise to fertile plants. Differences in wall composition, released proteins and the relative adhesiveness of cell-to-cell interactions have been shown to exist between cell clusters and correlate with their embryogenic potential [6–8]. The finding that the use of ‘conditioned’ media, on which embryogenic cells have previously been cultured, is important for differentiation indicates that soluble factors secreted from cells can have a profound developmental impact [9–11]. The arabinogalactan proteins One class of extracellular matrix molecules implicated in the regulation of somatic embryogenesis is the arabinogalactan proteins (AGPs). AGPs can be classed as proteoglycans because they are composed of more than 90% carbohydrate, mostly L-arabinose and D-galactose. Although AGPs are rich in hydroxyproline, alanine, serine and threonine, their protein backbones are quite diverse, and each backbone may be differentially modified by the addition of a polysaccharide [12–15]. The full structural characterization of AGPs may therefore be a difficult task. One class of AGPs, known as the ‘classical’ type because they were the first to be defined, have the potential to be anchored in membranes by glycosyl phosphatidyl inositol pb2613.qxd 11/26/1999 9:29 AM 522 Page 522 Commentary (GPI) anchors [16]. In animal cells, such anchors can potentially direct the proteins to particular membrane faces [17] or, through interactions with integral membrane proteins, might enable signal transduction from the extracellular matrix to the cell interior [18]. AGPs have complex and restricted localization patterns; their presence correlates with embryogenic potential, proliferative state or developmental stage [5,19]. The application of media conditioned by the culturing of embryogenic cells that thereby harbors AGPs, or of AGPs selected by specific antibodies, can enhance the embryogenic potential of other cells. In contrast using media containing AGPs or adding specific antibody-purified AGPs from nonembryogenic cells can decrease the number of embryos formed [11,15]. These data suggest that the distinct AGPs present in the media might be the active component which influences cellular differentiation. The β-glucosyl Yariv reagent, which selectively interacts with AGPs, has been used as a tool to probe the in planta function of AGPs. The incubation of cells or tissues with the Yariv reagent results in alterations to cell growth and division, consistent with the idea that AGPs have important functions in these processes [19]. It is likely, however, that the use of the Yariv reagent results in the disruption of wall structure through the cross-linking of AGPs. The direct consequences of the loss of AGPs has not, therefore, been clearly assessed. Mutations in AGP structural genes, or in genes whose functions are required for appropriate AGP modification, will be the ultimate tools for elucidating AGP function in vivo. Whether AGPs function through a structural or signaling mechanism is unknown. Because AGPs can be freely released from cell walls it is thought that they might not contribute to the structural integrity of the wall. AGPs can form complexes when leaves are excised, or when the proteoglycans are exposed to H2O2; they might therefore contribute to wall cross-linking under conditions of oxidative stress [20]. Although it is possible that the minor protein portion of AGP may function through interactions with other wall components, it is probable that most of the protein backbone is sterically blocked by the attached polysaccharides. The polysaccharide extensions of AGPs have the potential to form a gel-like matrix in association with water. Some hydrated carbohydrate moieties that are present in the extracellular matrix of animal cells are thought to function as cell chaperones in that they sterically block interactions between cells in a regulated fashion [21]. These polysaccharides determine when interactions take place and whether plasticity of associations is possible. AGPs might act in a similar manner; that is, AGPs might be recruited during wall remodeling or assembly, and may facilitate appropriate interactions among the extracellular domains of transmembrane proteins or cell-wall components. Cell-wall fragments Fragments of wall structural polymers can influence cellular behaviors [22–25]. For example, oligogalacturans can signal pathogen attack and can also influence the growth and differentiation of both flowers and roots in thin layer cultures. Fragments of xyloglucan have also been shown to either enhance growth or inhibit auxininduced growth, depending upon the level and specific structure of the added xyloglucan oligosaccharide. Our current understanding of the presence and action of xyloglucan endotransglycosylases (XETs) might help to explain the effects of high concentrations (>1 micromolar) of xyloglucan oligosaccharides. Through transglycosylation to xyloglucan polymers present in the wall, the oligosaccharides can act to shorten the lengths of the xyloglucan chains, reducing xyloglucan tethering of cellulose microfibrils and enhancing wall loosening [26,27]. Whether xyloglucan oligosaccharides participate in wallloosening mechanisms during cell expansion of untreated tissues has not been demonstrated. Nanomolar concentrations of specific xyloglucan oligosaccharides bearing fucose sidechains can interfere with growth [22–25]. The specific requirement of the fucose moiety, and the ability of the oligosaccharide to act at low concentrations strongly suggests this effect is distinct from the growth-enhancing effects of high concentration of xyloglucan oligosaccharides. The mechanism of growth inhibition is unknown but peroxidase activation has been implicated [28]. Xyloglucan oligosaccharides have been detected in media on which cells have been cultured; their presence is consistent with the proposed function in signaling. However, definitive evidence for a role for xyloglucan oligosaccharides as endogenous growth regulators would entail the demonstration of a loss of function when such oligosaccharides are not available. The cloning of a gene that encodes the fucosyl transferase that modifies xyloglucan [29] may be the important first step in a genetic approach to this problem. Plants that have mutations in this gene might reveal the consequences of the inability to generate these specific xyloglucan oligosaccharides. Interpretations of phenotype will, however, be complicated by the absence of the fucosyl groups on the xyloglucan polymers, which may affect their ability to act as wall structural components. Given that xyloglucan polysaccharides are a major component of the dicotyledenous cell wall, it is possible that oligosaccharides are recognized through a previously unknown mechanism. Although there might be a specific receptor for the oligosaccharides, it is also possible that the oligosaccharides act by displacing xyloglucan polymers from their binding sites, or by competing as substrates for molecules that modify the wall, such as expansins. The oligosaccharides could alter the structure pb2613.qxd 11/26/1999 9:29 AM Page 523 If walls could talk Braam of the wall in this way; such structural changes may signal through mechanotransduction pathways. Mechanical force It is well recognized that the cell wall is essential for maintaining the mechanical integrity of plants and for controlling the expansion of cells. The cell wall’s mechanical resistance to stretching and the osmotic gradient across the plasma membrane lead to the generation of turgor pressure within the cell. Turgor pressure imposes 10–100 MPa of stress upon the walls [30]. The perception of changes in wall tension may signal the regulation of processes that contribute to the maintenance of cellular homeostasis. For example, plant cells have a remarkable capacity to maintain a constant expansion rate, even when subjected to osmotic stress or to other perturbations that alter turgor pressure. Solute uptake is also closely correlated with expansion rate. Changes in wall tension might therefore be used as feedback signals to maintain homeostasis. One possible mechanism is that wall tension is sensed through mechanical deformations of the wall–membrane connections that enable signal transductions to the cell interior. Evidence that supports the involvement of the cell wall in signaling responses to mechanical forces comes from a number of sources. Gravisensing in the internodal cells of Chara corallina is sensitive to enzymes that digest major wall components and to peptides that are known to interact with animal cell integrins [31]. Fischer and Schopfer [32] interfered experimentally with the induced tropic curvature of maize (Zea mays) coleoptiles and found that microtubule orientation followed the direction of the induced mechanical strain rather than reoriented as a function of the gravitropic or phototropic signal transduction pathway. These results are consistent with the results of Lynch and Lintilhac [33] and Hernández and Green [34] who showed that applying mechanical forces or constraints to plant tissues can alter their planes of division and developmental patterning. Applying cell-wall-modifying protein, expansin, to shoot apical meristems results in the inappropriate formation of leaf primordia-like extensions [35]. Expansins are thought to act by releasing the hydrogen-bonding interactions between the cellulose and hemicellulose components of the wall and, in this way, to contribute to wall loosening [30]. The morphogenetic alterations caused by exogenous expansin most likely result from expansin evoked changes in the material properties of the wall. These experiments are an elegant demonstration of how modifying the properties of the plant cell wall, through altering arrangements or interactions of wall polysaccharides, can have a fundamental role in plant morphogenesis. Conclusions Plant cells may have versatile mechanisms to communicate with neighboring cells. The roles of unusual signals, 523 such as wall proteoglycans, fragments of wall polysaccharides and mechanical deformations of the wall are becoming more evident. The elucidation of the how these signals are generated and perceived will have a profound impact on our understanding of plant cell functions. 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