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Home , Plant development

COMMENTARY Emerging patterns of organization at the surface

PAUL KNOX

Department of Cell , 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 , 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 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 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 , such as that of a plant , 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 . 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 coats, which may tyl of the soybean (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 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 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. 1988; Stiefel et al. 1988). Analysis of tal regulation. In the root meristems of the Umbelliferae mRNA has indicated abundant expression in developing the expression of the J1M4 epitope is a very early develop- tissues such as the maize root tip and node, but mental event and reflects the position of certain develop- not in mature root or tissues (Stiefel et al. 1988). The ing lineages in relation to the overall emerging tissue protein has recently been immunolocalized to the cell wall pattern of the root, rather than a specific cell type (see of maize root tips, and evidence indicates that its occur- Fig. 1A; and Knox et al. 1989). The MAC 207 epitope has rence correlates with cell division rather than elongation been shown to occur at the surface of all cells in pea other (Ludevid et al. 1990). Further analyses of the protein than cell lineages in the developing leading to male structure of extensins indicates that in sugar beet the Ser- and female gametes and is only re-expressed at the surface (Hyp)4 block appears to be split, indicating an unusually of cells during later stages of development (Pen- high interspecific variability for a putative structural nell and Roberts, 1990). Monoclonal antibodies to carbo- molecule (Li et al. 1990). hydrate antigens, that may indeed be cell surface arabino- Other than the extensins, two further classes of cell wall galactan proteins, indicate spatial distinctions in the protein genes have been studied. These are the proline- tobacco flower, where epitopes are restricted to small rich proteins (PRPs) and the glycine-rich proteins (GRPs). discrete groups of cells in diverse floral tissues (Evans et The gene family encoding the PRPs of soybean show a al. 1988). The current implication of these observations is strikingly complex pattern of organ-specific and develop- that carbohydrate elaboration or modification on a com- mentally regulated expression (Hong et al. 1989; Datta et mon glycoprotein core results in the restricted expressions 558 P. Knox Fig. 1. The expression of a cell surface 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 . 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 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 The observation that these cell surface AGPs are modi- and that patterns of expression reflect aspects of plant cell fied in relation to cell position in the relatively unorgan- and lineage identity. There is very little information ized clumps of cultured cells (for example, JTM4 binds only available on the protein core of AGPs (Showalter and to certain cells at the surface of a clump of carrot callus, as Varner, 1989), although a recent report indicates Ala-Hyp shown in Fig. 1C) further suggests a fundamental role in repeats in a ryegrass AGP (Gleeson et al. 1989). In contrast plant cell organization for this class of glycoproteins to the extensins, current evidence indicates great vari- (Stacey et al. 1990) and suggests specific expression of this ation in the carbohydrate components of AGPs, with a set of glycoproteins in response to an unknown factor or diversity of saccharide linkage on the galactan backbone. factors. These may be the variant physical tension within It appears to be modifications or differences in this arabi- tissues or gradients of metabolites, such as hormones, that nogalactan component that the monoclonal antibodies may also be involved in the formation of tissue patterns. recognize. The precise function of these glycoproteins is unknown,

Plant cell surface 559 but the observed patterns of expression, their location at presence of pectin, and its esterification, are regulated in the plasma membrane and the known ability of AGPs to certain root apices in a manner that reflects the major react with Yariv antigens (Fincher et al. 1983) may tissue boundaries, suggests that this important polysac- indicate a role involving molecular recognition and cell- charide of the plant cell wall may also play some role in the cell interaction in relation to cell identity or position. more complex processes that comprise plant cell develop- An extracellular glycoprotein, rich in aspartic acid, ment. serine, threonine and possessing N-linked oligosaccharide chains, has been found in the conditioned medium of I thank Clive Lloyd and Keith Roberts for critical comments -supplied carrot cells and has been immunolocalized that have influenced the final form of this essay. 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 References before differentiation of the vascular tissues. BACIC, A., HARRIS, P. J. AND STONE, B. A. (1988). Structure and function A highly localized expression of a gene encoding a cell of plant cell wallB. In The Biochemistry of Plants (ed. P. K. Stumpf and wall HRGP in tobacco has been noted in mature pericycle E. E. Conn), vol. 14, pp. 297-371. Academic Press, San Diego. and endodermal cells in regions that will give rise to CASSAB, G. I. AND VARNER, J. E. (1987). Immunocytolocalization of extensin in developing soybean seed coats by immunogold-silver lateral root meristems (Keller and Lamb, 1989). This staining and by tissue printing on nitrocellulose paper. J. Cell Biol. expression is transient; not being expressed when the root 105, 2581-2588. has fully burst beyond the cortex and epidermis of the CASSAB, G. I., LIN, J.-J., LIN, L.-S. AND VARNER, J. E. (1988). Ethylene main root axis or in the main root meristem itself (Keller effect on extensin and peroxidase distribution in the Bubapical region and Lamb, 1989). This wall glycoprotein may also be of pea epicotyls. PI. Physiol. 88, 522-524. CASSAB, G. I. AND VARNER, J. E. (1988). Cell wall proteins A. Rev. PI. involved in a structural strengthening of the cell wall, Physiol. PI. molec. Biol. 38, 321-353. required as the lateral root penetrates the outer tissues of CLARKE, A. E., ANDERSON, R. L. AND STONE, B. A. (1979). Form and the main root. function of arabinogalactans and arabinogalactan proteins. Phytochemistry 18, 521-540. DATTA, K., SCHMIDT, A. AND MARCUS, A. (1989). Characterization of two soybean repetitive proline-rich proteins and a cognate cDNA from Future directions germinated ares The Plant Cell 1, 945-952. EDELMAN, G. M. (1986). Cell adhesion molecules in the regulation of animal form and tissue pattern. A. Rev. Cell Biol 2, 81-116. The phenomenology of these restricted ocurrences of plant EKBLOM, P., VESTWEBER, D. AND KEMLER, R. (1986). Cell-matrix cell surface molecules, or genes encoding such molecules, interactions and cell adhesion during development. A. Rev. Cell Biol. varies widely, although as yet, all precisely determined 2, 27-47. localizations respect or reflect tissue boundaries; for EVANS, P. T., HOLAWAY, B. L. AND MALMBERO, R. L. (1988). Biochemical example, no cell surface marker is expressed by a segment differentiation in the tobacco flower probed with monoclonal antibodies. Planta 178, 269-269. of a root or shoot when seen in transverse section. They FINCHKR, G. B., STONE, B. A. AND CLARKE, A. E. (1983). Arabinogalactan provide diverse markers for differing aspects of plant proteins: structure, biosynthesis, and function. A. Rev. PI. Physwl. 34, development and it is to be hoped that studies utilizing 47-70. specifically expressed genes and those currently more GALLAGHER, J. T. (1989). The extended family of proteoglycans: social residents of the pericellular zone. Curr. Opinion Cell Biol. 1, directed at the nature and occurrence of the final products 1201-1218 of gene action, will reach a common ground. Intriguing GLEESON, P. A., MCNAMARA, M., WETTENHALL, E. H., STONE, B. A. AND advances have been made, and further analysis of gene FINCHEH, G. B. (1989). Characterization of the hydroxyproline-rich families and the protein and carbohydrate components to protein core of an arabinogalactan-protein secreted from suspension determine the variation within and between tissues, and cultured Lolium multifhrum endosperm. Biochem. J. 264, 857-862. HONQ, J. C, NAGAO, R. T. AND KEY, J. L. (1989). Developmental^ even species, remains important, along with the precise regulated expression of soybean proline-rich cell wall protein genes. description of the expression of these molecules in terms of The Plant Cell 1, 937-943. cells comprising a maturing developmental system. HONG, J. C, NAGAO, R T. AND KEY, J. L. (1990). Characterization of a proline-rich cell wall protein gene family of soybean. A comparative The functions of these molecules remain uncertain and analysis. J. biol. Chem. 268, 2470-2475. although no mutants involving their deletion or modifi- HOOD, E E., SHEN, Q. X. AND VARNER, J. E. (1988). A developmental^ cation have emerged they would be of great use in this regulated, hydroxyproline-rich glycoprotein in maize pericarp cell walls PL Physiol. 87, 13S-142 regard. The role and nature of recognition events and any KELLER, B. AND LAMB, C. J. (1989). Specific expression of a novel cell interactions between these classes of cell surface proteins hydroxyproline-rich glycoprotein gene in lateral root initiation. Genes or with wall polysaccharides require elucidation. Many of Dev. 3, 1639-1646. these cell surface molecules have carbohydrate com- KELLER, B., TEMPLBTON, M. D. AND LAMB, C. J. (1989). Specific ponents and the arabinogalactan proteins have lectin-like localization of a plant cell wall glycine-rich protein in protoxylem cells of the vascular system. Proc. natn. Acad. Sci. U.S-A. 86, 1629-1533. capacities, that may indicate a function related to the KDJLISZEWSKI, M. AND LAMPORT, D. T. A. (1986). Cross-reactivities of deposition of wall polysaccharides (Pennell et al. 1989). polyclonal antibodies against extensin precursors determined via Knowledge of the chemical structure of the epitope recog- ELISA techniques. Phytochemistry 25, 673-677. nized by antibodies such as JIM4 will be of great interest. KTKI.IHZKWSKI, M. AND LAMPORT, D. T. A. (1987). Purification and partial characterization of a hydroxyproline-rich glycoprotein in a The potential for interaction of the carbohydrate struc- graminaceous moncot, Zea mays. PI. Physiol. 85, 823-827. tures, polysaccharides, glycoproteins and proteoglycans, KIELISZEWSKI, M., LEYKAM, J. F. AND LAMPORT, D. T. A (1990). Structure to be found at the plant cell surface is immense. Analysis of the threonine-rich extensin from Zea mays. PI. Physiol. 92, 316-326. indicates that chemical variation occurs among samples of KNOX, J. P., DAY, S. AND ROBERTS, K. (1989). A set of cell surface glycoproteins forms a marker of cell position, and not cell type, in the an AGP taken 'even from a single tear' of gum exuded from root menstem of Daucus carota L. Development 106, 47-56. the trunk of an Acacia (Clarke et al. 1979). The KNOX, J. P., LDMSTEAD, P. J., KING, J., COOPER, C. AND ROBERTS, K. molecular basis of plant development is such an uncharted (1990). Pectin esterification is spatially regulated both within cell territory that the function of cell wall components has walls and between developing tissues of root apices. Planta (in press). been more readily ascribed to structural or defensive LAMPORT, D. T. A. AND NORTHCOTB, D. H. (1960). Hydroxyproline in primary cell walls of higher plants. Nature 188, 665-666. needs. The recent indication (Knox et al. 1990), that the Li, X., KIELISZEWSKI, M. AND LAMPORT, D. T. A. (1990). A chenopod

560 P. Knox extensin lacka repetitive tetrahydroxyproline blocks. PL Phyaiol. 92, SCHERES, B., VAN DB WIEL, C., ZALENSKY, A., HORVATH, B., SPAINK, H., 327-333. VAN ECK, H., ZWABTKRUIS, F., WOLTERS, A.-M., GLOUDEMANS, T., VAN LUDEVID, M. D., RUIZ-AVILA, L., VALLES, M. P., STIBFBL, V., TORRENT, M., KAMMBN, A. AND BISSEUNO, T. (1990). The ENOD12 gene product is TORNE, J. M. AND PUIODOMENECH, P. (1990). Expression of genes for involved in the infection process during the pea-rhizobium cell wall proteins in dividing and wounded tissues of Zea mays L. interaction. Cell 60, 281-294. Planta 180, 524-529. SHOWALTER, A. M. AND VARNIH, J. E. (1989). Plant hydroxyproline-rich MBYBR, D. J., AFONSO, C. L. AND GALBRATTH, D. W. (1988). Isolation and glycoproteins. In The Biochemistry of Plants (ed. P. K. Stumpf and E. characterization of monoclonal antibodies directed against plant E. Conn), vol. 15, pp. 485-620. Academic Press, San Diego. plasma membrane and cell wall epitopes: identification of a STACEY, N. J., ROBERTS, K AND KNOX, J. P. (1990). Patterns of monoclonal antibody that recognizes extensin and analysis of the expression of the JIM4 arabinogalactan protein epitope in cell cultures process of epitope biosynthesis in plant tissues and cell cultures. roots. Planta 174, 321-332. associated glycoproteins related to the arabinogalactan proteins is STIEFEL, V., PEREZ-GRAU, L., ALBBRICIO, F., GIRALT, E., RUIZ-AVILA, L., unique to flowering plants. J. Cell Biol. 108, 1966-1977. LUDBVID, M. D. AND PUIODOMENECH, P (1988). Molecular of PENNELL, R. I. AND ROBERTS, K. (1989). Sexual development in pea is cDNAa encoding a putative cell wall protein from Zea mays and presaged by a change in arabinogalactan protein expression. Nature immunological identification of related peptides. PL molec. Biol. 11, 344, 647-649. 483-493. ROBERTS, K. (1989). The plant extracellular matrix. Curr. Opinion Cell VAN HOLST, G.-J. AND CLARKE, A. E. (1986). Organ specific Biol. 1, 1020-1027. arabinogalactan proteins of Lycopersicon peruvianium (Mill.) SATOH, S. AND FUJII, T. (1988). Purification of GP57, an auxin-regulated demonstrated by crossed electrophoresis. PL Physiol. 80, 786-789. extracellular glycoprotein of carrota, and its immunocytochemical VARNER, J. E. AND LIN, L.-S. (1989). Plant cell wall architecture. Cell 56, localization in dermal tissues. Planta 175, 364-373. 231-239.

Plant cell surface 561