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An epitope of rice threonine- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins

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Abstract

A monoclonal antibody, LM1, has been derived that has a high affinity for an epitope of hydroxyproline-rich glycoproteins (HRGPs). In suspension-cultured rice (Oryza sativa L.) cells the epitope is carried by three major proteins with different biochemical properties. The most abundant is the 95-kDa extracellular rice extensin, a threonine- and hydroxyproline-rich glycoprotein (THRGP) occurring in the cell wall and secreted into the medium. This THRGP can be selectively oxidatively cross-linked in the presence of hydrogen peroxide and an endogenous peroxidase with the result that it does not enter a protein gel. A second polypeptide with the LM1 epitope (180 kDa), also occurring in the suspension-cultured cells and medium, is not oxidatively cross-linked. Three further polypeptides (52, 65 and 110 kDa) with the characteristics of hydrophobic proteins of the plasma-membrane also carry the LM1 epitope as determined by immuno-blotting of detergent/aqueous partitions of a plasma-membrane preparation and immuno-fluorescence studies with rice protoplasts. At the rice root apex the LM1 epitope is carried by four glycoproteins and is developmentally regulated. The major locations of the epitope are at the surface of cells associated with the developing protoxylem and metaxylem in the stele, the longitudinal radial walls of epidermal cells and a sheath-like structure at the surface of the root apex.

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Abbreviations

AGP:

arabinogalactan protein

ELISA:

enzyme-linked immunosorbent assay

HRGP:

hydroxyproline-rich glycoprotein

THRGP:

threonine- and hydroxyproline-rich glycoprotein

References

  • Akashi, T., Shibaoka, H. (1991) Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY2 cells. J. Cell Sci. 98, 169–174

    Google Scholar 

  • Akashi, T., Kawasaki, S., Shibaoka, H. (1990) Stabilisation of cortical microtubules by the cell wall in cultured tobacco cells. Planta 182, 363–369

    Google Scholar 

  • Baginski, E.S., Foa, P.P., Zak, B. (1967) Determination of phosphate: study of labile organic phosphate interference. Clin. Chim. Acta 15, 155–158

    Google Scholar 

  • Bazin, H. (1982) Production of rat monoclonal antibodies with the LOU rat non-secreting IR983F myeloma cell line. Prot. Biol. Fluids 29, 615–618

    Google Scholar 

  • Bordier, A.L. (1981) Phase separation of integral membrane proteins in Triton-X-114 solution. J. Biol. Chem. 256, 1604–1607

    Google Scholar 

  • Bradley, D.J., Kjellbom, P., Lamb C.J. (1992) Elicitor- and wound-inducible oxidative cross-linking of a proline-rich plant cell wall protein. Cell 70, 21–30

    Google Scholar 

  • Brownleader, M.D., Dey, P.M. (1993) Purification of extensin from the cell walls of tomato (hybrid of Lycopersicon esculentum and L. peruvianum) cells in suspension culture. Planta 191, 457–469

    Google Scholar 

  • Brownleader, M.D, Golden, K.D., Dey, P.M. (1993) An inhibitor of extensin peroxidase in cultured tomato cells. Phytochemistry 33, 755–758

    Google Scholar 

  • Caelles, C., Delseny, M., Puigdomenech, P. (1992) The hydroxyproline-rich glycoprotein from Oryza sativa. Plant Mol. Biol. 18, 617–619

    Google Scholar 

  • Carpita, N.C., Gibeaut, D.M. (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3, 1–30

    Google Scholar 

  • Chen, Z., Silva, H., Klessig, D.F. (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262, 1883–1886

    CAS  PubMed  Google Scholar 

  • Cooper, J.B., Varner, J.E. (1983) Insolubilisation of hydroxyprolinerich cell wall glycoprotein in aerated carrot root slices. Biochim. Biophys. Res. Commun. 112, 161–167

    Google Scholar 

  • Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356

    Google Scholar 

  • Epstein, L., Lamport, D.T.A. (1984) An intramolecular linkage involving isodityrosine in extensin. Phytochemistry 23, 1241–1246

    Google Scholar 

  • Everdeen, D.S, Kiefer, S., Willard, J.J., Muldoon, E.P., Dey, P.M., Li, X-B., Lamport, D.T.A. (1988) Enzymic cross-linkage of monomeric extensin precursors in vitro. Plant Physiol. 87, 616–621

    Google Scholar 

  • Fritz, S.E., Hood, K.R., Hood, E.E. (1991) Localisation of soluble and insoluble fractions of hydroxyproline-rich glycoproteins during maize kernel development. J. Cell Sci. 98, 545–550

    Google Scholar 

  • Fry, S.C. (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu. Rev. Plant Physiol. 37, 165–186

    Google Scholar 

  • Gallagher, S.R., Leonard, R.T. (1982) Effect of vanadate, molybdate and azide on membrane-associated ATPase and soluble phosphatase activities of corn roots. Plant Physiol. 77, 196–201

    Google Scholar 

  • Hammond-Kosack, K.E., Atkinson H.J., Bowles D.J. (1989) Systemic accumulation of novel proteins in the apoplast of potato plants following root invasion by the cyst-nematode Globodera rostochiensis. Mol. Plant. Pathol. 35, 495–506

    Google Scholar 

  • Herman, E.M., Lamb, C.J. (1992) Arabinogalactan-rich glycoproteins are localised on the cell surface and in intra-vacuolar multivesicular bodies. Plant Physiol. 98, 264–272

    Google Scholar 

  • Hood, E.E., Shen, Q.X., Varner, J.E. (1988) A developmentally regulated hydroxyproline-rich glycoprotein in maize pericarp cell walls. Plant Physiol. 87, 138–142

    Google Scholar 

  • Kakimoto, T., Shibaoka, H. (1986) Calcium-sensitivity of cortical microtubules in the green alga Mougeotia. Plant Cell Physiol. 27, 91–101

    Google Scholar 

  • Kieliszewski, M.J., Lamport, D.T.A. (1987) Purification and partial characterisation of a hydroxyproline-rich glycoprotein from Zea mays. Plant Physiol. 85, 823–827

    Google Scholar 

  • Kieliszewski, M.J., Lamport, D.T.A. (1994) Extensin: repetitive motifs, functional sites, post-translational codes and phylogeny. Plant J. 5, 157–172

    Google Scholar 

  • Kieliszewski, M.J., Leykam J.F., Lamport, D.T.A. (1990) Structure of the threonine-rich extensin from Zea mays. Plant Physiol. 92, 316–326

    Google Scholar 

  • Knox, J.P., Linstead, P.J., King, J., Cooper, C., Roberts, K. (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181, 512–521

    Google Scholar 

  • Knox, J.P., Linstead, P.J., Peart, J., Cooper, C., Roberts, K. (1991) Developmentally-regulated epitopes of cell surface arabinogalactan-proteins and their relation to root tissue pattern formation. Plant J. 1, 317–326

    Google Scholar 

  • Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

    PubMed  Google Scholar 

  • Larsson, C. (1985) Plasma membranes. Modern methods of plant analysis (N.S.) 1, 85–104

    Google Scholar 

  • Leach, J.E., Cantrell, M.A., Sequeira, L. (1982) A hydroxyprolinerich bacterial agglutinin from potato: extraction, purification and characterisation. Plant Physiol. 92, 327–333

    Google Scholar 

  • Liddell, J.E., Cryer, A. (1991) A practical guide to monoclonal antibodies. John Wiley and Sons

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275

    CAS  PubMed  Google Scholar 

  • Ludevid, M.D., Ruiz-Avila, L., Valles, M.P., Stiefel, V., Torrent, M., Tome, J.M., Puigdomenech, P. (1990) Expression of genes for cell-wall proteins in dividing and wounded tissues of Zea mays. Planta 180, 524–529

    Google Scholar 

  • Malamy, J., Carr, J.P., Klessig, D.F., Raskin, I. (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002–1004

    Google Scholar 

  • Mellon, J.E., Helgeson, J.P. (1982) Interaction of a hydroxyprolinerich glycoprotein from tobacco callus with potential pathogens. Plant Physiol. 70, 401–405

    Google Scholar 

  • Metraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Schmidt, E., Blum, W., Inveradi, B. (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004–1006

    Google Scholar 

  • Murphy, J.M., Hood, E.E. (1993) Molecular basis for extensin size heterogeneity in two maize varieties. Plant Mol. Biol. 21, 885–893

    Google Scholar 

  • Oparka, K.J., Prior, D.A.M., Crawford, J.W. (1994) Behaviour of plasma membrane and plasmodesmata during plasmolysis of onion epidermal cells. Plant Cell Environ. 17, 163–171

    Google Scholar 

  • Pont-Lezica, R.F., McNally, J.G., Pickard, B.G. (1993) Wall-tomembrane linkers in onion epidermis: some hypotheses. Plant Cell Environ. 16, 111–123

    Google Scholar 

  • Rasmussen, J.B., Hammerschmidt, R., Zook, M.N. (1991) Systemic induction of salicylic acid accumulation in cucumber after innoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97, 1342–1347

    Google Scholar 

  • Shedletsky, E., Shmuel, M., Trainin, T., Kalman, S., Delmer, D. (1992) Cell wall structure in cells adapted to growth on the cellulose-synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol. 100, 120–130

    Google Scholar 

  • Showalter, A.M. (1993) Structure and function of plant cell wall proteins. Plant Cell 5, 9–23

    Article  CAS  PubMed  Google Scholar 

  • Smallwood, M., Beven, A., Donovan, N., Neill, S.J., Peart, J., Roberts, K., Knox, J. P. (1994) Localization of cell wall proteins in relation to the developmental anatomy of the carrot root apex. Plant J. 5, 237–246

    Google Scholar 

  • Stafstrom. J.P., Staehelin, L.A. (1986) Cross-linking patterns in saltextractable extensin from carrot cell walls. Plant Physiol. 81, 234–241

    Google Scholar 

  • Sutherland, M.W. (1991) The generation of oxygen radicals during host plant responses to infection. Physiol. Mol. Plant Pathol. 39, 79–94

    Google Scholar 

  • Towbin, H., Staehlin, T., Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4354

    Google Scholar 

  • Waffenschmidt, S., Woessner, J.P., Beer, K., Goodenough, U.W. (1993) Isodityrosine cross-linking mediates insolubilisation of walls in Chlamydomonas. Plant Cell 5, 809–820

    Google Scholar 

  • van Holst, G.J., Varner, J.E. (1984) Reinforced polyproline II conformation in a hydroxyproline-rich cell-wall glycoprotein from carrot root. Plant Physiol. 74, 247–251

    Google Scholar 

  • Yalpani, N., Silverman, P., Wilson, T.M.A., Kleier, D.A., Raskin, I. (1991) Salicylic acid as a systemic signal and an inducer of pathogenesis-related proteins. Plant Cell 3, 809–818

    Google Scholar 

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Authors and Affiliations

  1. Centre for Plant Biochemistry and Biotechnology, University of Leeds, LS2 9JT, Leeds, UK

    Margaret Smallwood, Helen Martin & J. Paul Knox

Authors
  1. Margaret Smallwood
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  2. Helen Martin
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  3. J. Paul Knox
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Additional information

This work was supported by The Leverhulme Trust. We also acknowledge support from The Royal Society and thank Prof. L.A. Staehelin for the carrot extensin, N. Stacey for the rice cell culture and Dr. J. Keen for protein sequencing.

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Smallwood, M., Martin, H. & Knox, J.P. An epitope of rice threonine- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins. Planta 196, 510–522 (1995). https://doi.org/10.1007/BF00203651

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  • DOI: https://doi.org/10.1007/BF00203651

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