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 occurrence of plant cell surface molecules, predominantly multicellular organisms are undoubtedly highly complex. glycoproteins, have been correlated with developmental In animal systems extensive information has been ob- stages, tissues or cell types. tained about molecules of the cell surface and extracellu- lar matrix that are involved in cell interactions and developmental processes (Edelman, 1986; Ekblom et al. The molecules of the plant cell surface 1986; Gallagher, 1989). In mature plant tissues, specific cell surface changes are known and can be related to Often thought of as a relatively inert structural box within specific functions and cell types, such as cutin at the outer which the protoplast resides, the plant cell wall can surface of plants, suberin in secondary protective tissue, perhaps more accurately be regarded as the major com- the thickened walls of collenchyma cells and the asym- ponent of a dynamic extracellular matrix, albeit more metrically thickened walls of guard cells. However, knowl- confining and displaying more rigidity than that of animal edge of specific interactions or modulations at the surfaces cells (Roberts, 1989). The great complexity of polysacchar- of plant cells during the primary stages of plant cell ides that account for much of the wall has been, and organization, i.e. in meristems and during embryogenesis, continues to be, elucidated by chemical means, but knowl- is lacking. edge of any compositional differences relating to the early events of morphogenesis is fragmentary (Bacic et al. 1988). It is, of course, at this level of cell interactions and the Cell wall proteins can contribute up to a tenth of all wall organization of cells into organisms that plant cells dis- material, but the nature of their interaction, attachment, play some of their most obvious differences from animal developmental or biochemical (other than enzymic) func- cells. A developing meristem, such as that of a plant root, tion and relation to overall cell wall architecture remains is a striking phenomenon in that the whole developmental uncertain (Cassab and Varner, 1988). A striking charac- pathway can be encountered at one time in the maturing teristic of many of the wall proteins is the presence of high files of cells occurring proximally to the meristematic levels of hydroxyproline, a feature of collagens of the initials. However, the distinctive developmental features animal extracellular matrix. In the thirty years since of plants - cell immobility, rigid walls, growth dependent hydroxyproline was shown to occur in plant cell walls upon the plane of cell division and cell expansion - have (Lamport and Northcote, 1960) various classes of hydroxy- not been conducive to the investigation of the molecular proline-rich glycoproteins (HRGPs) have been discerned, properties of the plant cell surface in relation to the but still remain broadly categorized into three groups - organization and formation of the tissue pattern within the extensins, the arabinogalactan proteins and the Sola- such a system. Little is known of the local variations in the naceous lectins (Showalter and Varner, 1989). Some of the molecular condition of the cell wall that must be important defining characteristics of these and other developmen- for the direction and nature of cell expansion, or of the tally regulated proteins of the plant extracellular matrix nature of molecular links of the plant cytoskeleton with are shown in Table 1 and the current knowledge of the components of the plasma membrane and the cell surface. structure of the genes encoding these proteins is to be Although the extracellular zone of plant tissues can be found in the reviews by Varner and Lin (1989) and viewed as a unified space with cell walls in intimate Showalter and Varner (1989). contact, and the presence of plasma membrane-lined plasmodesmata permits a correspondingly unified intra- cellular space, virtually nothing is known of the need for or occurrence of interactions between neighbouring cells, Developmental patterns both within and between cell lineages, across the milieu of The extensins are the most studied of the HRGPs. They the cell wall and their influence on cell development and gene expression. have been characterized by a repetitive Ser-(Hyp)4 peptide sequence, and have been shown to occur as rod-like A useful starting point for any investigation of the structures, stabilized by glycosylation (Showalter and molecular mechanisms leading to the formation of com- Varner, 1989). This may be related to a structural role in plex structures, such as those of a plant, is the identifi- strengthening walls at the completion of cell expansion by cation of molecules that display restricted patterns of the formation of a cross-linked insoluble matrix. Several occurrence within the developing system. What follows is forms of extensin can occur in the same tissue, for example a survey of the currently known instances in which the up to four in tomato (Showalter and Varner, 1989), but Journal of Cell Science 96, 657-561 (1990) Printed in Great Britain © The Company of Biologists Limited 1990 557 Table 1. Structural characteristics of the major groups of developmentally regulated proteins of the plant cell surface Peptide sequences Carbohydrate (%) Main protein-carbohydrate linkages Extensins Ser-(Hyp)4 -50 Hyp-Ara, Ser-Gal Arabinogalactan proteins1"2 Ala-Hyp -90 Hyp-Gal, Ser-Gal, Hyp-Ara Proline-rich proteins3 Pro-Pro-Val-X-Y 0/? 4 Glycine-rich proteins (Giy-X)n 0 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 al. 1989). PRP mRNAs were detected in all organs and also resolved. Antibodies generated to soybean coat extensin, in cultured cells, and SbPRPl and SbPRP2 display con- have been used to localize extensin specifically to the trasting gradients of expression in the developing hypoco- mature sclerenchyma tissue of seed coats, which may tyl of the soybean seedling (Hong et al. 1989). Subsequent indicate a protective function (Cassab and Varner, 1987). analysis of the PRP gene family has indicated highly These same antibodies, utilized in a nitrocellulose print- conserved regions, perhaps related to the yet unknown ing technique possibly only allowing visualization of function of these molecules (Hong et al. 1990). PRPs are soluble extensin and not the insolubilized form, is sugges- thought to be non- or only slightly glycosylated (Hong et tive of tissue variation and association of extensin with the al. 1990) and thus distinct from the extensins, although vascular tissue of bean hypocotyl and the epidermal and the emerging knowledge of the structural variation of the vascular tissue of pea epicotyls (Cassab and Varner, 1987; protein components of the extensins indicates similarities Cassab et al. 1988). Although these observations have (Li et al. 1990). A study of the specific cells expressing been supported by immunolocalization studies using a these genes and their products will be of great interest. monoclonal antibody directed against extensin (Meyer et The search for genes specifically expressed during legume al. 1988) the precise cell types reactive with the antibodies nodule formation has led to the isolation of the ENOD12 have not been reported. In a complementary study anti- gene, encoding a proline-rich protein, similar to the bodies, generated against a carrot extensin, have been soybean PRPs discussed above (Scheres et al. 1990) and in used to locate the antigen in the cell wall of phloem of the fact it has been observed that this gene is not nodule- carrot storage root, the source of the immunogen (Staf- specific, but is also expressed in stem tissue and that the strom and Staehelin, 1988). It is of interest in this study expression is restricted to a zone of cortical cells surround- that extensin appeared to occur throughout the cell wall, ing the vascular tissues (Scheres et al. 1990). but with significantly less in the region of the middle The genes encoding GRPs also display highly localized lamella. A striking observation, also with the same anti- expression, occuring only in the protoxylem cells of the bodies, was that no antigen could be detected in the vascular system of the bean hypocotyl (Keller et al. 1989). primary root of the carrot seedling (Stafstrom and Staehe- There is an indication that this glycoprotein is closely lin, 1988). It is not clear from these two sets of studies associated with lignin deposition and may be insolubil- whether the observed patterns of localization indicate the ized, by means of tyrosine linkages, later in development. restricted occurrence of extensin or reflect tissue variation Arabinogalactan proteins (AGPs), as major components in the antigenic components of extensins; both possi- of plant exudates and secretions, have been studied exten- bilities suggesting developmental regulation. Antibodies sively in terms of their chemistry (Clarke et al. 1979; to non-glycosylated epitopes are capable of the specific Fincher et al. 1983), but are also known to occur in all recognition of distinct extensins (Kieliszewski and Lam- plant tissues and in organ-specific forms (Van Hoist and port, 1986). Clarke, 1986). The recent generation of monoclonal anti- Although graminaceous monocots generally contain low bodies to the plasma membrane of plant cells has led to levels of HRGPs, a threonine-rich HEGP, homologous observations that glycoproteins associated with the with dicot extensins, has been isolated from maize cell plasma membrane contain carbohydrate components that cultures (Kieliszewski and Lamport, 1987; Kieliszewski et also occur on soluble AGP proteoglycans (i.e. contain al. 1990) and evidence has accumulated that related common epitopes; Pennell et al. 1989; Knox et al. 1989). molecules are developmentally regulated within maize The expression of these epitopes shows strict developmen- tissues (Hood et al.