Summary
Cell adhesion and communication is one of the most fascinating fields of modern biology. How do cells receive information from the environment and from neighboring cells? How does this information elicit morphogenesis, cell division and migration? The recent identification of the surface molecules involved in these events in animal systems is beginning to disclose that a continuum, extracellular matrix-plasma membrane-cytoskeleton, may be a common structure present in all eukaryotic cells. In this article we compare current knowledge on this complex structure in animal systems to the emerging data on plants. We point out the areas that need additional research to fully understand the role of the cell wall-cytoskeleton continuum in plants.
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Abbreviations
- ABP:
-
actin-binding protein
- AGP:
-
arabinogalactan proteins
- CTK:
-
cytoskeleton
- ECM:
-
extracellular matrix
- FN:
-
fibronectin
- hFN:
-
human fibronectin
- HRGP:
-
hydroxyproline-rich glycoproteins
- hVN:
-
human vitronectin
- PM:
-
plasma membrane
- SAM:
-
substrate adhesion molecule
- VN:
-
vitronectin
References
Adair WS, Mecham RP (1990) Organization and assembly of plant and animal extracellular matrix. Academic Press, San Diego
Aderem A (1992) Signal transduction and the actin cytoskeleton: the role of MARCKS and profilin. Trends Biochem Sci 17: 438–443
Akashi T, Shibakoa H (1991) Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells. J Cell Sci 98: 169–174
—, Kawasaki S, Shibakoa H (1990) Stabilization of cortical microtubules by the cell wall in cultured tobacco cells. Effects of extensin on the cold-stability of cortical microtubules. Planta 183: 363–369
Albelda SM, Buck CA (1990) Integrins and other cell adhesion molecules. FASEB J 4: 2868–2880
Axelos M, Bardet C, Lescure B (1993) AnArabidopsis cDNA encoding a 33-kilodalton laminin receptor homolog. Plant Physiol 103: 299–300
Bretscher A (1991) Microfilament structure and function in the cortical cytoskeleton. Annu Rev Cell Biol 7: 337–374
Carpita NC, Gibeaut DM (1993) Structural models of primary cell wall in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3: 1–30
Cassab GI, Varner JE (1988) Cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 39: 321–353
Cosgrove DJ (1993) How do plant cell walls extend? Plant Physiol 102: 1–6
—, Hendrich R (1991) Strech-activated chloride, potassium and calcium channels coexisting in plasma membrane of guard cells ofVicia faba. L. Planta 186: 143–153
de Ruijter N, Emmons AM (1993) Immunodetection of spectrin antigens in plant cells. Cell Biol Int 17: 169–182
Diamond MS, Springer TA (1994) The dynamic regulation of integrin adhesiveness. Curr Biol 4: 506–517
Ding J-P, Pickard BG (1993 a) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J 3: 83–110
— — (1993 b) Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J 3: 713–720
Drake G, Carr DJ, Anderson WP (1978) Plasmolysis, plasmodesmata and the electrical coupling of oat coleoptile cells. J Exp Bot 29: 1205–1214
Edelman GM (1993) A golden age for adhesion. Cell Adhes Commun 1: 1–7
Falke L, Edwards KL, Pickard BG, Misier S (1988) A strech-activated anion channel in cultured tobacco cells. FEBS Lett 237: 141–144
Faraday CD, Spanswick RM (1993) Evidence for a membrane skeleton in higher plants-a spektrin-like polypeptide co-isolates with rice root plasma membranes. FEBS Lett 318: 313–316
Gens JS, McNally JG, Pickard BG (1993 a) Resolution of binding sites for antibodies to integrin, vitronectin and fibronectin on onion epidermis protoplasts and depectinated cell walls. ASGSB Bull: 7: 42
—, Ding J-P, Pont-Lezica R, McNally JG, Pickard BG (1993 b) Exploring the basis of mechanosensitivity. In: Ho D, Prakashi H (eds), Past, present and future of plant biology. Washington University, St. Louis, pp 53–55
Heuser J (1981) Preparing biological samples for stereomicroscopy by the quick-freeze, deep-etched, rotatory-replication technique. Methods Cell Biol 22: 97–122
Hocquette S, Pont-Lezica R (1993) Involvement of vitronectin-like molecules in wall-to-membrane linkages in onion epidermis. In: Ho D, Prakashi H (eds) Past, present and future of plant biology. Washington University, St. Louis, pp 38–41
Hohl HR, Guggenbhul C, Baisinger S (1992) Antibodies against animal substrate adhesion molecules (SAM) inhibit adhesion ofPhytophtora megasperma f. sp. glycinea to the host cell wall. Phytopathol 82: 1118
Hynes RO (1992) Integrins: versatility, modulation and signaling in cell adhesion. Cell 69: 11–25
Ingber D (1991) Integrin as mechanochemical transducers. Curr Opin Cell Biol 3: 841–848
Kachar B, Parakkal M, Fex J (1990) Structural basis for mechanical transduction in the frog vestibular sensory apparatus. I. The otolithic membrane. Hearing Res 45: 179–190
Kagawa T, Kadota A, Wada M (1992) The junction between the plasma membrane and the cell wall in fern protonemal cells, as visualized after plasmolysis, and its dependence on arrays of cortical microtubules. Protoplasma 170: 186–190
Keller B (1993) Structural cell wall proteins. Plant Physiol 101: 1127–1130
Kiermayer O (1964) Untersuchungen über die Morphogenese und Zellwandbildung beiMicrasterias denticulata. Bréb. Protoplasma 59: 76–132
Knox JP (1992) Cell adhesion, cell separation and plant morphogenesis. Plant J 2: 137–141
—, Linstead PJ, 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
Lambert AM (1993) Microtubule-organizing centers in higher plants. Curr Opin Cell Biol 5: 116–122
Luna EJ, Hitt AL (1992) Cytoskeleton-plasma membrane interactions. Science 258: 955–964
Martinac B (1993) Mechanosensitive ion channels: biophysics and physiology. In: Jackson MB (ed) Thermodynamics of cell surface receptors. CRC Press, Boca Raton, pp 327–372
McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary cell wall. J Cell Sci 96: 323–334
McCurdy DW, Williamson RE (1991) Actin and actin-associated proteins. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 3–14
Morris CE (1990) Mechanosensitive ion channels. J Membr Biol 113: 93–107
Odani S, Takehiko K, Ono T (1987) Amino acid sequence of a soybean (Glycine max) seed polypeptide having a poly(L-aspartic acid) structure. J Biol Chem 262: 10502–10505
Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytol 126: 571–591
—, Prior DAM, Crawford JW (1994) Behaviour of plasma membrane, cortical ER and plasmodesmata during plasmolysis of onion epidermal cells. Plant Cell Environ 17: 163–171
Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108: 1967–1977
Pickard BG, Ding J-P (1993) The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control center? Austr J Plant Physiol 20: 439–459
Pont-Lezica RF, McNally JG, Pickard BG (1993 a) Wall-to-membrane linkers in onion epidermis: some hypotheses. Plant Cell Environ 16: 111–123
—, Bardet C, Lescure B, Axelos M (1993 b) Characterization of a cDNA clone fromArabidopsis highly homologous to a laminin-receptor. J Cell Biochem 17A: 21–22
Pumplin DW, Bloch RJ (1993) The membrane skeleton. Trends Cell Biol 3: 113–117
Rils B, Rattan SIS, Clark BFC, Merrick WC (1990) Eurkaryotic protein elongation factors. Trends Biochem Sci 15: 420–424
Roberts AW, Haigler CH (1989) Rise in chlorotetracycline fluorescence accompanies tracheary element differentiation in suspension cultures ofZinnia. Protoplasma 152: 37–45
Roberts K (1989) The plant extracellular matrix. Curr Opin Cell Biol 1: 1020–1027
— (1990) Structures at the plant surface. Curr Opin Cell Biol 2: 920–928
Ruoslahti E (1991) Integrins. J Clin Invest 87: 1–5
Sachs F (1988) Mechanical transduction in biological systems. CRC Crit Rev Biomed Eng 16: 141–169
Sanders LC, Eord EM (1989) Direct movement of latex particles in the gynoecia of three species of flowering plants. Science 243: 1606–1608
—, Wang C-S, Walling LL, Lord EM (1991) A homolog of the substrate adhesion molecule vitronectin occurs in four species of flowering plants. Plant Cell 3: 629–635
Sastry SK, Horwitz AF (1993) Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signalling. Curr Opin Cell Biol 5: 819–831
Schelenbaum P, Vantard M, Peter C, Fellous A, Lambert AM (1993) Co-assembly properties of higher plant microtubule-associated proteins with purified brain and plant tubulins. Plant J 3: 253–260
Schroeder JI, Hagiwara S (1990) Respetitive increases in cytosolic CA2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci USA 87: 9305–9309)
—, Hedrich R (1990) Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells. Trends Biochem Sci 14: 187–192
Sentenac H, Bonneaud N, Minet M, Lacroute F, Gaymard JM, Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256: 663–665
Shaw PJ, Fairbairn DJ, Lloyd CW (1991) Cytoplasmic and nuclear intermediate filaments antigens in higher plant cells. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 69–81
Shedletzky E, Shmuel M, Trinin T, Kaiman S, Delmer D (1992) Cell wall structure in cells adapted to growth on the cellulose-synthesis inhibitor 2,6-dichlorophezonitrile. Plant Physiol 100: 120–130
Shindler M, Meiners S, Cheresh DA (1989) RGD-dependent linkage between plant cell wall and plasma membrane: consequences for growth. J Cell Biol 5: 9–23
Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–23
Simmonds DH (1992) Plant cell wall removal: cause for microtubule instability and division abnormalities in protoplast cultures? Physiol Plant 85: 387–390
Springer TA (1990) The sensation and regulation of interactions with the extracellular environment: the cell biology of lymphocyte adhesion receptors. Annu Rev Cell Biol 6: 359–402
Staiger CJ, Schliwa M (1987) Actin localization and function in higher plants. Protoplasma 141: 1–12
Steer MW (1990) Role of actin in tip growth. In: Heath IB (ed) Tip growth in plants and fungal cells. Academic Press, San Diego, pp 119–145
Strasburger E, Noll F, Schenk H, Schimper AFW (1983) Lehrbuch der Botanik, 32th edn. G Fischer, Stuttgart
Talbot LD, Ray PM (1992) Molecular size and separability features of pea cell wall polysaccharides. Implication for models of primary wall structure. Plant Physiol 98: 357–368
Thuleau P, Graziana A, Ranjeva R, Schroeder JI (1993) Solubilized proteins from carrot (Daucus carota L.) membranes bind calcium channel blockers and form calcium-permeable ion channels. Proc Natl Acad Sci USA 90: 765–769
Varner JE, Lin L-S (1989) Plant cell architecture. Cell 56: 231–239
Wagner VT, Matthysse AG (1992) Involvement of a vitronectin-like protein in attachement ofAgrobacterium tumefaciens to carrot suspension culture cells. J Bacteriol 174: 5999–6003
—, Brian L, Quatrano RS (1992) Role of vitronectin-like molecule in embryo adhesion of the brown algaFucus. Proc Natl Acad Sci USA 89: 3644–3648
Wang CS, Walling LL, Gu YQ, Ware CF, Lord EM (1994) Two classes of proteins and messenger-RNAs inLilium longiflorum L. identified by human vitronectin probes. Plant Physiol 104: 711–717
Wang N, Nutler JP, Ingber DE (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124–1127
Wayne R, Staves MP, Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. J Cell Sci 101: 611–623
Woessner JF (1993) The extracellular matrix. FASEB J 7: 735–736
Wyatt SE, Carpita NC (1993) The plant cytoskeleton-cell-wall continuum. Trends Cell Biol 3: 413–417
Yang C, Xing L, Zhai Z (1992) Intermediate filaments in higher plant cells and their assembly in a cell-free system. Protoplasma 171: 44–54
Zhu J-K, Damaz B, Konowiz AK, Bressan RA, Hasegawa PM (1994) A higher plant extracellular vitronectin-like adhesion protein is related to the translational elongation factor-1α. Plant Cell 7: 393–404
—, Shi J, Singh U, Wyatt SE, Bressan RA, Hasegawa PM, Carpita NC (1993) Enrichment of vitronectin- and fibronectin-like proteins in NaCl-adapted plant cells and evidence for their involvement in plasma membrane-cell wall adhesion. Plant J 3: 637–646
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Dedicated to Professor Dr. Hartmut K. Lichtenthaler on the occasion of his 60th birthday
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Reuzeau, C., Pont-Lezica, R.F. Comparing plant and animal extracellular matrix-cytoskeleton connections — are they alike?. Protoplasma 186, 113–121 (1995). https://doi.org/10.1007/BF01281321
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DOI: https://doi.org/10.1007/BF01281321