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Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices

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Summary

Arabinogalactan protein and wall-associated kinase (WAK) are suspected to be regulatory players at the interface between cytoplasm and cell wall. Both WAK(s) and arabinogalactan shown likely to represent arabinogalactan protein(s) have been visualized there with computational optical-sectioning microscopy. The arabinogalactan occurs in a polyhedral array at the external face of the cell membrane. WAK, and other proteins as yet unidentified, appear to fasten the membrane to the wall at vertices of the array. Evidence is presented that the array bears an important part of the mechanical stress experienced by the membrane, and it is speculated that the architectural organization of arabinogalactan protein, WAK, and other components of the array is critical for coordination of endomembrane activities, growth, and differentiation. The array has been named the plasmalemmal reticulum.

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Abbreviations

AGP:

arabinogalactan protein

(β-D-Glc)3 :

β-D-glucosyl Yariv phenylglycoside

(β-D-Man)3 :

β-D-mannosyl Yariv phenylglycoside

SDS-AGE:

sodium dodecyl sulfate-agarose gel electrophoresis

SDS-PAGE:

sodium dodecyl sulfate-polyacrylamide gel electrophoresis

WAK:

wall-associated kinase

References

  • Arioli T, Peng LC, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279: 717–720

    Google Scholar 

  • Balestrini R, Hahn MG, Faccio A, Mendgen K, Bonfante P (1996) Differential localization of carbohydrate epitopes in plant cell walls in the presence and absence of arbuscular mycorrhizal fungi. Plant Physiol 111: 203–213

    Google Scholar 

  • Batiza AF, Rayment I, Kung C (1999) Channel gate! Tension, leak and disclosure. Struct Fold Des 7: R99-R103

    Google Scholar 

  • Blaustein MP, Arnon A, Hamlyn JM, Juhaszova M (1999) How ouabain works: key role of the plasmerosome in the regulation of cell responsiveness. Biophys J 76: A393

    Google Scholar 

  • Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Mol Biol 49: 281–309

    Google Scholar 

  • Conchello J-A (1998) Super-resolution and convergence properties of the expectation-maximization algorithm for maximum-likelihood deconvolution of incoherent images. J Optic Soc Am A 15: 2609–2619

    Google Scholar 

  • —, McNally JG (1996) Fast regularization technique for expectation maximization algorithm for computational optical sectioning microscopy. In: Cogswell CJ, Kino GS, Wilson T (eds) Three-dimensional microscopy: image acquisition and processing. SPIE-International Society for Optical Engineering, Bellingham, Wash, pp 199–208 (Proceedings of SPIE, vol 2655)

    Google Scholar 

  • Diekmann W, Herkt B, Low PS, Nurnberger T, Scheel D, Terschuren C, Robinson DG (1994) Visualization of elicitor-binding loci at the plant cell surface. Planta 195: 126–137

    Google Scholar 

  • Ding JP, Pickard BG (1993a) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J 3: 83–110

    Google Scholar 

  • — — (1993b) Modulation of mechanosensitive calcium channels by temperature. Plant J 3: 713–720

    Google Scholar 

  • Du H, Simpson RJ, Moritz RL, Clarke AE, Bacic A (1994) Isolation of the protein backbone of an arabinogalactan protein from the styles ofNicotiana alata and characterization of a corresponding cDNA. Plant Cell 6: 1643–1653

    Google Scholar 

  • — —, Clarke AE, Bacic A (1996) Molecular characterization of a stigma-specific gene encoding an arabinogalactan protein (AGP) fromNicotiana alata. Plant J 9: 313–323

    Google Scholar 

  • Edwards KL, Pickard BG (1987) Detection and transduction of physical stimuli in plants. In: Wagner E, Greppin H, Millet B (eds) The cell surface and signal transduction. Springer, New York Berlin Heidelberg, pp 45–66

    Google Scholar 

  • Faik A, Labouré AM, Gulino D, Mandaron P, Falconet D (1998) A plant surface protein sharing structural properties with animal integrins. Eur J Biochem 253: 552–559

    Google Scholar 

  • Faro C, Ramalho-Santos M, Vieira M, Mendes A, Simões I, Andrade R, Verissimo P, Lin X-L, Tang J, Pires E (1999) Cloning and characterization of cDNA encoding Cardosin A, an RGD-containing plant aspartic protease. J Biol Chem 274: 28724–28729

    Google Scholar 

  • Fetrow JS, Skolnick J (1998) Method for prediction of protein function from sequence using the sequence-to-structure-to-function paradigm with application to glutaredoxins/thioredoxins and T1 ribonucleases. J Mol Biol 281: 949–968

    Google Scholar 

  • Freshour G, Clay RP, Fuller MS, Albersheim P, Darvill AG, Hahn MG (1996) Developmental and tissue-specific structural alterations of the cell-wall polysaccharides ofArabidopsis thaliana roots. Plant Physiol 110: 1413–1429

    Google Scholar 

  • Gens JS, Reuzeau C, Doolittle KW, McNally JG, Pickard BG (1996) Covisualization by computational optical-sectioning microscopy of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194: 215–230

    Google Scholar 

  • Giddings TH Jr, Staehelin LA (1991) Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 85–89

    Google Scholar 

  • Guharay F, Sachs F (1984) Mechanotransducer ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol 352: 685–701

    Google Scholar 

  • Gunning BES, Steer MW (1996) Plant cell biology: structure and function. Jones and Bartlett, Sudbury, Mass

    Google Scholar 

  • Harlow E, Lane D (1988) Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 90–91

    Google Scholar 

  • He Z-H, Fujiki M, Kohorn BD (1996) A cell wall-associated receptor-like protein kinase. J Biol Chem 271: 19789–19793

    Google Scholar 

  • —, He D, Kohorn BD (1998) Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J 14: 55–63

    Google Scholar 

  • —, Cheeseman I, He DZ, Kohorn BD (1999) A cluster of five cell wall-associated receptor kinase genes, Wak1–5, are expressed in specific organs of Arabidopsis. Plant Mol Biol 39: 1189–1196

    Google Scholar 

  • Hepler PK, Palevitz BA, Lancelle SA, McCauley MM, Lichtscheidl I (1990) Cortical endoplasmic reticulum in plants. J Cell Sci 96: 355–373

    Google Scholar 

  • Hillis DM (1994) Homology in molecular biology. In: Hall BK (ed) Homology: the hierarchical basis of comparative biology. Academic Press, San Diego, pp 339–368

    Google Scholar 

  • Hirai N, Sonobe S, Hayashi T (1998) In situ synthesis of beta-glucan microfibrils on tobacco plasma membrane sheets. Proc Natl Acad Sci USA 95: 15102–15106

    Google Scholar 

  • Johnson-Flanagan AM, Singh J (1986) Membrane deletion during plasmolysis in hardened and non-hardened plant cells. Plant Cell Environ 4: 299–305

    Google Scholar 

  • Kiba A, Sugimoto M, Toyoda K, Ichinose Y, Yamada T, Shiraishi T (1998) Interaction between cell wall and plasma membrane via RGD motif is implicated in plant defense responses. Plant Cell Physiol 39: 1245–1249

    Google Scholar 

  • Kjellbom P, Larsson C (1984) Preparation and polypeptide composition of chlorophyll-free plasma membranes from leaves of light-grown spinach and barley. Physiol Plant 62: 501–509

    Google Scholar 

  • —, Snogerup L, Stöhr C, Reuzeau C, McCabe PF, Pennell RI (1997) Oxidative cross-linking of plasma membrane arabinogalactan proteins. Plant J 12: 1189–1196

    Google Scholar 

  • Knebel W, Quader H, Schnepf E (1990) Mobile and immobile endoplasmic reticulum in onion bulb epidermis cells: short- and long-term observations with a confocal laser scanning microscope. Eur J Cell Biol 52: 328–340

    Google Scholar 

  • Knox JP (1995) Developmentally regulated proteoglycans and glycoproteins of the plant cell surface. FASEB J 9: 1004–1012

    Google Scholar 

  • Kohorn BD, Lane S, Smith TA (1992) An Arabidopsis serine/threonine kinase homologue with an epidermal growth factor repeat selected in yeast for its specificity for a thylakoid membrane protein. Proc Natl Acad Sci USA 89: 10989–10992

    Google Scholar 

  • —, He Z-H, Fujiki M (1996) Elusin: a receptor-like kinase with an EGF domain in the cell wall. In: Shewry PR, Halford NG, Hooley R (eds) Protein phosphorylation in plants. Clarendon, Oxford, pp 297–304

    Google Scholar 

  • Kreuger M, van Holst G-J (1993) Arabinogalactan proteins are essential in somatic embryogenesis ofDaucus carota L. Planta 189: 243–248

    Google Scholar 

  • — —, (1995) Arabinogalactan-protein epitopes in somatic embryogenesis ofDaucus carota L. Planta 197: 135–141

    Google Scholar 

  • — —, (1996) Arabinogalactan proteins and plant differentiation. Plant Mol Biol 30: 1077–1086

    Google Scholar 

  • Labouré AM, Faik A, Mandaron P, Falconet D (1999) RGD-dependent growth of maize calluses and immunodetection of an integrin-like protein. FEBS Lett 442: 123–128

    Google Scholar 

  • Martinac B, Adler J, Kung C (1990) Mechanosensitive ion channels ofEschericia coli activated by amphipaths. Nature 348: 261–263

    Google Scholar 

  • Mau S-L, Chen C-G, Pu Z-Y, Moritz RL, Simpson RJ, Bacic A, Clarke AE (1995) Molecular cloning of cDNAs encoding the protein backbones of arabinogalactan-proteins from the filtrate of suspension-cultured cells ofPyrus communis andNicotiana alata. Plant J 8: 269–281

    Google Scholar 

  • McCabe PF, Valentine TA, Forsberg LS, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9: 2225–2241

    Google Scholar 

  • Nagpal P, Quatrano RS (1999) Isolation and characterization of a cDNA clone fromArabidopsis thaliana with partial sequence similarity to integrins. Gene 230: 33–40

    Google Scholar 

  • Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174: 195–291

    Google Scholar 

  • Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytol 126: 571–591

    Google Scholar 

  • —, Prior DAM, Crawford JW (1994) Behavior of plasma-membrane, cortical ER and plasmodesmata during plasmolysis of onion epidermal cells. Plant Cell Environ 17: 163–171

    Google Scholar 

  • Pickard BG (1994) Contemplating the plasmalemmal control center model. Protoplasma 182: 1–9

    Google Scholar 

  • —, Ding JP (1993) The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control center? Aust J Plant Physiol 20: 439–459

    Google Scholar 

  • Pont-Lezica RF, McNally JG, Pickard BG (1993) Wall-to-membrane linkers in onion epidermis: some hypotheses. Plant Cell Environ 16: 111–123

    Google Scholar 

  • Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, Hahn MG (1994) Generation of monoclonal antibodies against plant cell-wall polysaccharides 1: characterization of a monoclonal antibody to a terminal α-(1 → 2)-linked fucosyl-containing epitope. Plant Physiol 104: 699–710

    Google Scholar 

  • Reuzeau C, Doolittle KW, McNally JG, Pickard BG (1997a) Covisualization in living onion cells of putative integrin, spectrin, actin, intermediate filaments and other proteins at the cell membrane and in an endomembrane sheath. Protoplasma 199: 173–197

    Google Scholar 

  • —, McNally JG, Pickard BG (1997b) The endomembrane sheath: a key structure for understanding the plant cell? Protoplasma 200: 1–9

    Google Scholar 

  • Roy S, Jauh GY, Hepler PK, Lord EM (1998) Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta 204: 450–458

    Google Scholar 

  • —, Holdaway-Clarke TL, Hackett GR, Kunkel JG, Lord EM, Hepler PK (1999) Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. Plant J 19: 379–386

    Google Scholar 

  • Sachs F (1997) Mechanical transduction by ion channels: how forces reach the channel. Soc Gen Physiol Ser 52: 209–218

    Google Scholar 

  • Saier MH Jr (1999) A proposed system for the classification of transmembrane transport proteins in living organisms. In: Van Winkle LJ (ed) Biomembrane transport. Academic Press, San Diego, pp 265–276

    Google Scholar 

  • Šamaj J, Baluska F, Bobak M, Volkmann D (1999a) Extracellular matrix surface network of embryogenic units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep 18: 369–374

    Google Scholar 

  • —, Ensikat HJ, Baluska F, Knox JP, Barthlott W, Volkmann D (1999b) Immunogold localization of plant surface arabinogalactan-proteins using glycerol liquid substitution and scanning electron microscopy. J Microsc Oxford 193 Part 2: 150–157

    Google Scholar 

  • Schultz C, Gilson P, Oxley D, Joelian Y, Bacic A (1998) GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci 3: 426–431

    Google Scholar 

  • Steffan W, Kovác P, Albersheim P, Darvill AG, Hahn MG (1995) Characterization of a monoclonal antibody that recognizes an arabinosylated (1 → 6)-β-D-galactan epitope in plant complex carbohydrates. Carbohydr Res 275: 295–307

    Google Scholar 

  • Stöhr C, Snogerup L, Pennell RI, Kjellbom P (1996) An agarose gel electrophoresis method for the separation of arabinogalactan proteins. Plant J 10: 943–948

    Google Scholar 

  • Strugger S (1935) Prakticum der Zell- und Gewebephysiologie der Pflanze. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Svetek J, Yadav MP, Nothnagel EA (1999) Presence of a glycosylphosphatidylinositol lipid anchor on rose arabinogalactan proteins. J Biol Chem 274: 14724–14733

    Google Scholar 

  • Toonen MAJ, Schmidt EDL, van Kammen A, de Vries SC (1997) Promotive and inhibitory effects of diverse arabinogalactan proteins onDaucus carota L. somatic embryogenesis. Planta 203: 188–195

    Google Scholar 

  • Watanabe Y, Ohno T, Okada Y (1982) Virus multiplication in tobacco protoplasts inoculated with tobacco mosaic virus RNA encapsulated in large unilamellar vesicle liposomes. Virology 120: 478–480

    Google Scholar 

  • Zimmermann S, Nurnberger T, Frachisse JM, Wirtz W, Guern J, Hedrich R, Scheel D (1997) Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94: 2751–2755

    Google Scholar 

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Authors and Affiliations

  1. The Gladys Levis Allen Laboratory of Plant Sensory Physiology, Biology Department, Washington University, St. Louis, Missouri

    J. Scott Gens, Masaaki Fujiki & Barbara G. Pickard

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  1. J. Scott Gens
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  2. Masaaki Fujiki
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  3. Barbara G. Pickard
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Correspondence to Barbara G. Pickard.

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Scott Gens, J., Fujiki, M. & Pickard, B.G. Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212, 115–134 (2000). https://doi.org/10.1007/BF01279353

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