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COMMENTARY Emerging patterns of organization at the plant cell surface PAUL KNOX Department of Cell Biology, John Innes Institute, Colney Lane, Noiwich NR4 7UH, UK The processes involved in the coordinated development of multicellular organisms are undoubtedly highly complex. In animal systems extensive information has been obtained about molecules of the cell surface and extracellular matrix that are involved in cell interactions and developmental processes (Edelman, 1986; Ekblom et al. 1986; Gallagher, 1989). In mature plant tissues, specific cell surface changes are known and can be related to specific functions and cell types, such as cutin at the outer surface of plants, suberin in secondary protective tissue, the thickened walls of collenchyma cells and the asymmetrically thickened walls of guard cells. However, knowledge of specific interactions or modulations at the surfaces of plant cells during the primary stages of plant cell organization, i.e. in meristems and during embryogenesis, is lacking. It is, of course, at this level of cell interactions and the organization of cells into organisms that plant cells display some of their most obvious differences from animal cells. A developing meristem, such as that of a plant root, is a striking phenomenon in that the whole developmental pathway can be encountered at one time in the maturing files of cells occurring proximally to the meristematic initials. However, the distinctive developmental features of plants - cell immobility, rigid walls, growth dependent upon the plane of cell division and cell expansion - have not been conducive to the investigation of the molecular properties of the plant cell surface in relation to the organization and formation of the tissue pattern within such a system. Little is known of the local variations in the molecular condition of the cell wall that must be important for the direction and nature of cell expansion, or of the nature of molecular links of the plant cytoskeleton with components of the plasma membrane and the cell surface. Although the extracellular zone of plant tissues can be viewed as a unified space with cell walls in intimate contact, and the presence of plasma membrane-lined plasmodesmata permits a correspondingly unified intracellular space, virtually nothing is known of the need for or occurrence of interactions between neighbouring cells, both within and between cell lineages, across the milieu of the cell wall and their influence on cell development and gene expression. A useful starting point for any investigation of the molecular mechanisms leading to the formation of complex structures, such as those of a plant, is the identification of molecules that display restricted patterns of occurrence within the developing system. What follows is a survey of the currently known instances in which the Journal of Cell Science 96, 657-561 (1990) Printed in Great Britain © The Company of Biologists Limited 1990 occurrence of plant cell surface molecules, predominantly glycoproteins, have been correlated with developmental stages, tissues or cell types. The molecules of the plant cell surface Often thought of as a relatively inert structural box within which the protoplast resides, the plant cell wall can perhaps more accurately be regarded as the major component of a dynamic extracellular matrix, albeit more confining and displaying more rigidity than that of animal cells (Roberts, 1989). The great complexity of polysaccharides that account for much of the wall has been, and continues to be, elucidated by chemical means, but knowledge of any compositional differences relating to the early events of morphogenesis is fragmentary (Bacic et al. 1988). Cell wall proteins can contribute up to a tenth of all wall material, but the nature of their interaction, attachment, developmental or biochemical (other than enzymic) function and relation to overall cell wall architecture remains uncertain (Cassab and Varner, 1988). A striking characteristic of many of the wall proteins is the presence of high levels of hydroxyproline, a feature of collagens of the animal extracellular matrix. In the thirty years since hydroxyproline was shown to occur in plant cell walls (Lamport and Northcote, 1960) various classes of hydroxyproline-rich glycoproteins (HRGPs) have been discerned, but still remain broadly categorized into three groups the extensins, the arabinogalactan proteins and the Solanaceous lectins (Showalter and Varner, 1989). Some of the defining characteristics of these and other developmentally regulated proteins of the plant extracellular matrix are shown in Table 1 and the current knowledge of the structure of the genes encoding these proteins is to be found in the reviews by Varner and Lin (1989) and Showalter and Varner (1989). Developmental patterns The extensins are the most studied of the HRGPs. They have been characterized by a repetitive Ser-(Hyp)4 peptide sequence, and have been shown to occur as rod-like structures, stabilized by glycosylation (Showalter and Varner, 1989). This may be related to a structural role in strengthening walls at the completion of cell expansion by the formation of a cross-linked insoluble matrix. Several forms of extensin can occur in the same tissue, for example up to four in tomato (Showalter and Varner, 1989), but 557 Table 1. Structural characteristics of the major groups of developmentally regulated proteins of the plant cell surface Peptide sequences Extensins Arabinogalactan proteins1"2 Proline-rich proteins34 Glycine-rich proteins Ser-(Hyp)4 Ala-Hyp Pro-Pro-Val-X-Y (Giy-X)n Carbohydrate (%) -50 -90 0/? 0 Main protein-carbohydrate linkages Hyp-Ara, Ser-Gal Hyp-Gal, Ser-Gal, Hyp-Ara Source references: ' Showalter and Vamer (1989); 3 Gleeson et al. (1989); 3 Hong et al. (1990); * Keller et al. (1989). whether this reflects differences in location has not been resolved. Antibodies generated to soybean coat extensin, have been used to localize extensin specifically to the mature sclerenchyma tissue of seed coats, which may indicate a protective function (Cassab and Varner, 1987). These same antibodies, utilized in a nitrocellulose printing technique possibly only allowing visualization of soluble extensin and not the insolubilized form, is suggestive of tissue variation and association of extensin with the vascular tissue of bean hypocotyl and the epidermal and vascular tissue of pea epicotyls (Cassab and Varner, 1987; Cassab et al. 1988). Although these observations have been supported by immunolocalization studies using a monoclonal antibody directed against extensin (Meyer et al. 1988) the precise cell types reactive with the antibodies have not been reported. In a complementary study antibodies, generated against a carrot extensin, have been used to locate the antigen in the cell wall of phloem of the carrot storage root, the source of the immunogen (Stafstrom and Staehelin, 1988). It is of interest in this study that extensin appeared to occur throughout the cell wall, but with significantly less in the region of the middle lamella. A striking observation, also with the same antibodies, was that no antigen could be detected in the primary root of the carrot seedling (Stafstrom and Staehelin, 1988). It is not clear from these two sets of studies whether the observed patterns of localization indicate the restricted occurrence of extensin or reflect tissue variation in the antigenic components of extensins; both possibilities suggesting developmental regulation. Antibodies to non-glycosylated epitopes are capable of the specific recognition of distinct extensins (Kieliszewski and Lamport, 1986). Although graminaceous monocots generally contain low levels of HRGPs, a threonine-rich HEGP, homologous with dicot extensins, has been isolated from maize cell cultures (Kieliszewski and Lamport, 1987; Kieliszewski et al. 1990) and evidence has accumulated that related molecules are developmentally regulated within maize tissues (Hood et al. 1988; Stiefel et al. 1988). Analysis of mRNA has indicated abundant expression in developing tissues such as the maize root tip and coleoptile node, but not in mature root or shoot tissues (Stiefel et al. 1988). The protein has recently been immunolocalized to the cell wall of maize root tips, and evidence indicates that its occurrence correlates with cell division rather than elongation (Ludevid et al. 1990). Further analyses of the protein structure of extensins indicates that in sugar beet the Ser(Hyp)4 block appears to be split, indicating an unusually high interspecific variability for a putative structural molecule (Li et al. 1990). Other than the extensins, two further classes of cell wall protein genes have been studied. These are the prolinerich proteins (PRPs) and the glycine-rich proteins (GRPs). The gene family encoding the PRPs of soybean show a strikingly complex pattern of organ-specific and developmentally regulated expression (Hong et al. 1989; Datta et 558 P. Knox al. 1989). PRP mRNAs were detected in all organs and also in cultured cells, and SbPRPl and SbPRP2 display contrasting gradients of expression in the developing hypocotyl of the soybean seedling (Hong et al. 1989). Subsequent analysis of the PRP gene family has indicated highly conserved regions, perhaps related to the yet unknown function of these molecules (Hong et al. 1990). PRPs are thought to be non- or only slightly glycosylated (Hong et al. 1990) and thus distinct from the extensins, although the emerging knowledge of the structural variation of the protein components of the extensins indicates similarities (Li et al. 1990). A study of the specific cells expressing these genes and their products will be of great interest. The search for genes specifically expressed during legume nodule formation has led to the isolation of the ENOD12 gene, encoding a proline-rich protein, similar to the soybean PRPs discussed above (Scheres et al. 1990) and in fact it has been observed that this gene is not nodulespecific, but is also expressed in stem tissue and that the expression is restricted to a zone of cortical cells surrounding the vascular tissues (Scheres et al. 1990). The genes encoding GRPs also display highly localized expression, occuring only in the protoxylem cells of the vascular system of the bean hypocotyl (Keller et al. 1989). There is an indication that this glycoprotein is closely associated with lignin deposition and may be insolubilized, by means of tyrosine linkages, later in development. Arabinogalactan proteins (AGPs), as major components of plant exudates and secretions, have been studied extensively in terms of their chemistry (Clarke et al. 1979; Fincher et al. 1983), but are also known to occur in all plant tissues and in organ-specific forms (Van Hoist and Clarke, 1986). The recent generation of monoclonal antibodies to the plasma membrane of plant cells has led to observations that glycoproteins associated with the plasma membrane contain carbohydrate components that also occur on soluble AGP proteoglycans (i.e. contain common epitopes; Pennell et al. 1989; Knox et al. 1989). The expression of these epitopes shows strict developmental regulation. In the root meristems of the Umbelliferae the expression of the J1M4 epitope is a very early developmental event and reflects the position of certain developing lineages in relation to the overall emerging tissue pattern of the root, rather than a specific cell type (see Fig. 1A; and Knox et al. 1989). The MAC 207 epitope has been shown to occur at the surface of all cells in pea other than cell lineages in the developing flower leading to male and female gametes and is only re-expressed at the surface of cells during later stages of embryo development (Pennell and Roberts, 1990). Monoclonal antibodies to carbohydrate antigens, that may indeed be cell surface arabinogalactan proteins, indicate spatial distinctions in the tobacco flower, where epitopes are restricted to small discrete groups of cells in diverse floral tissues (Evans et al. 1988). The current implication of these observations is that carbohydrate elaboration or modification on a common glycoprotein core results in the restricted expressions Fig. 1. The expression of a cell surface arabinogalactan protein epitope (J4e), recognized by monoclonal antibody JIM4, is developmentally restricted. A. Expression of J4e by epidermal (e) and certain pericycle (p) and stele cells at the parsley root apex, visualized by JIM4-immunofluore8cence. The transverse section is approximately 100 /on from the root initials. Bar, 100 jan. B. A diagram of the cells comprising the root section seen in A in which the shape of cells characteristic of the developing tissues can be seen and related to the JIM4 reactive cells. The arrow indicates the extent of the stele and the alignment of the band of developing xylem. Heavy lines indicate emerging boundaries between epidermis (e) and cortex (c) and between cortex and stele. C. JIM4 binding to cells only at the periphery of a large proembryogenic mass of carrot callus cells as seen by immunofluorescence labelling of a cross-section. Bar, 100 /an. D. The proembryogenic mass can be seen to be a solid ball of cells in a phase-contrast image of the same section as shown in C. of subclasses of cell surface glycoproteins of the AGP class and that patterns of expression reflect aspects of plant cell and lineage identity. There is very little information available on the protein core of AGPs (Showalter and Varner, 1989), although a recent report indicates Ala-Hyp repeats in a ryegrass AGP (Gleeson et al. 1989). In contrast to the extensins, current evidence indicates great variation in the carbohydrate components of AGPs, with a diversity of saccharide linkage on the galactan backbone. It appears to be modifications or differences in this arabinogalactan component that the monoclonal antibodies recognize. The observation that these cell surface AGPs are modified in relation to cell position in the relatively unorganized clumps of cultured cells (for example, JTM4 binds only to certain cells at the surface of a clump of carrot callus, as shown in Fig. 1C) further suggests a fundamental role in plant cell organization for this class of glycoproteins (Stacey et al. 1990) and suggests specific expression of this set of glycoproteins in response to an unknown factor or factors. These may be the variant physical tension within tissues or gradients of metabolites, such as hormones, that may also be involved in the formation of tissue patterns. The precise function of these glycoproteins is unknown, Plant cell surface 559 but the observed patterns of expression, their location at the plasma membrane and the known ability of AGPs to react with Yariv antigens (Fincher et al. 1983) may indicate a role involving molecular recognition and cellcell interaction in relation to cell identity or position. An extracellular glycoprotein, rich in aspartic acid, serine, threonine and possessing N-linked oligosaccharide chains, has been found in the conditioned medium of auxin-supplied carrot cells and has been immunolocalized to both the epidermis and endodermis of the carrot root and to the epidermis of the carrot petiole (Satoh and Fujii, 1988). Significantly, it could not be located in the root apex before differentiation of the vascular tissues. A highly localized expression of a gene encoding a cell wall HRGP in tobacco has been noted in mature pericycle and endodermal cells in regions that will give rise to lateral root meristems (Keller and Lamb, 1989). This expression is transient; not being expressed when the root has fully burst beyond the cortex and epidermis of the main root axis or in the main root meristem itself (Keller and Lamb, 1989). This wall glycoprotein may also be involved in a structural strengthening of the cell wall, required as the lateral root penetrates the outer tissues of the main root. presence of pectin, and its esterification, are regulated in certain root apices in a manner that reflects the major tissue boundaries, suggests that this important polysaccharide of the plant cell wall may also play some role in the more complex processes that comprise plant cell development. I thank Clive Lloyd and Keith Roberts for critical comments that have influenced the final form of this essay. References BACIC, A., HARRIS, P. J. AND STONE, B. A. (1988). Structure and function of plant cell wallB. In The Biochemistry of Plants (ed. P. K. Stumpf and E. E. Conn), vol. 14, pp. 297-371. Academic Press, San Diego. CASSAB, G. I. AND VARNER, J. E. (1987). Immunocytolocalization of extensin in developing soybean seed coats by immunogold-silver staining and by tissue printing on nitrocellulose paper. J. Cell Biol. 105, 2581-2588. CASSAB, G. I., LIN, J.-J., LIN, L.-S. AND VARNER, J. E. (1988). Ethylene effect on extensin and peroxidase distribution in the Bubapical region of pea epicotyls. PI. Physiol. 88, 522-524. CASSAB, G. I. AND VARNER, J. E. (1988). Cell wall proteins A. Rev. PI. Physiol. PI. molec. Biol. 38, 321-353. CLARKE, A. E., ANDERSON, R. L. AND STONE, B. A. (1979). Form and function of arabinogalactans and arabinogalactan proteins. Phytochemistry 18, 521-540. DATTA, K., SCHMIDT, A. AND MARCUS, A. (1989). 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The functions of these molecules remain uncertain and although no mutants involving their deletion or modification have emerged they would be of great use in this regard. The role and nature of recognition events and any interactions between these classes of cell surface proteins or with wall polysaccharides require elucidation. Many of these cell surface molecules have carbohydrate components and the arabinogalactan proteins have lectin-like capacities, that may indicate a function related to the deposition of wall polysaccharides (Pennell et al. 1989). Knowledge of the chemical structure of the epitope recognized by antibodies such as JIM4 will be of great interest. The potential for interaction of the carbohydrate structures, polysaccharides, glycoproteins and proteoglycans, to be found at the plant cell surface is immense. 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