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Intercellular communication inAzolla roots: I. Ultrastructure of plasmodesmata

Summary

A model is proposed for the structure of the plasmodesmata ofAzolla root primordia, based on micrographs obtained by a combination of fixation in glutaraldehyde/p-formaldehyde/tannic acid/ferric chloride, digestion of cell walls and the use of stereo pairs. Unlike the model for plasmodesmatal structure proposed byRobards (1971), the desmotubule is depicted as a virtually closed cylindrical bilayer providing little or no open pathway for transport. In this respect it is similar to the model ofLópez-Sáez et al. (1966). An analysis of the molecular packing of types of lipids found in endoplasmic reticulum (of which the desmotubule is an extension) indicates that the model is geometrically feasible. Details cannot be discerned with accuracy, but material, possibly particulate, occupies much of the space between desmotubule and plasma membrane, the cytoplasmic lumen being reduced to inter-particle spaces of cross-sectional area comparable to that of the bore in a gap junction connexon. Implications for intercellular transport are discussed.

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References

  • Brighigna, L., 1974: The ultrastructure of plasmodesmata in sucking scale inTillandsia. Caryologia27, 369–377.

    Google Scholar 

  • Burgess, J., 1971: Observations on structure and differentiation in plasmodesmata. Protoplasma73, 83–95.

    Google Scholar 

  • Burton, P. R., Hinkley, R. E., Pierson, G. B., 1975: Tannic acidstained microtubules with 12, 13 and 15 protofilaments. J. Cell Biol.65, 227–233.

    Google Scholar 

  • Carde, J. P., 1974: Le tissu de transfert (= cellules de Strasburger) dans les aiguilles du pin maritime (Pinuspinaster Ait) II caractères cytochimiques et infrastructuraux de la paroi et des plasmodesmes. J. Microscopie20, 51–72.

    Google Scholar 

  • Carnie, S. L., Israelachvili, J. N., Pailthorpe, B. A., 1979: Lipid packing and transbilayer asymmetries of mixed lipid vesicles. Biochim. biophys. Acta554, 340–357.

    Google Scholar 

  • Crispeels, M. J., 1980: The endoplasmic reticulum. In: The Biochemistry of Plants, Vol. 1 (Stumpf, P. K., Conn, E. E., eds.), pp. 389–410. New York: Academic Press.

    Google Scholar 

  • Donaldson, R. P., Beevers, H., 1977: Lipid composition of organelles from germinating castor bean endosperm. Plant Physiol.59, 259–263.

    Google Scholar 

  • Evert, R. F., Eschrich, W., Heyser, W., 1977: Distribution and structure of plasmodesmata in mesophyll and bundle-sheath cells ofZea mays L. Planta136, 77–89.

    Google Scholar 

  • Futaesaku, Y., Mizuhira, V., Nakamura, H., 1972: A new fixation method using tannic acid for electron microscopy and some observations of biological specimens. Proc. Int. Congr. Histochem. Cytochem.4, 155–165.

    Google Scholar 

  • Flagg-Newton, J., Simpson, L., Loewenstein, W. R., 1979: Permeability of the cell-to-cell membrane channels in mammalian cell junction. Science205, 404–407.

    Google Scholar 

  • Gruen, D. R. W., 1980: A statistical mechanical model of the lipid bilayer above its phase transition. Biochim. biophys. Acta595, 161–183.

    Google Scholar 

  • -Wolfe, J., 1982: Lateral tensions and pressures in lipid monolayers and membranes. Biochim. biophys. Acta (in press).

  • Gunning, B. E. S., Hughes, J. E., Hardham, A. R., 1978: Formative and proliferative divisions, cell differentiation and developmental changes in the meristem ofAzolla roots. Planta143, 121–144.

    Google Scholar 

  • —,Robards, A. W., 1976: Plasmodesmata and symplastic transport. In: Transport and Transfer Processes in Plants (Wardlaw, I. E., Passioura, J., eds.), pp. 15–41. New York: Academic Press.

    Google Scholar 

  • —,Steer, M. W., 1975: Ultrastructure and the biology of plant cells, pp. 312. London: E. Arnold.

    Google Scholar 

  • Hawes, C. R., Juniper, B. E., Horne, J. C., 1981: Low and high voltage electron microscopy of mitosis and cytokinesis in maize roots. Planta152, 397–407.

    Google Scholar 

  • Hepler, P. K., 1982: Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma111, 121–133.

    Google Scholar 

  • Israelachvili, J. N., 1978: The packing of lipids and proteins in membranes. In: Light Transducing Membranes (Deamer, D., ed.), p. 91. New York: Academic Press.

    Google Scholar 

  • —,Mitchell, D. J., Ninham, B. W., 1977: Theory of self-assembly of lipid bilayers and vesicles. Biochim. biophys. Acta470, 185–201.

    Google Scholar 

  • Juniper, B. E., Lawton, J. R., 1979: The effect of caffeine, different fixation regimes and low temperature on microtubules in the cells of higher plants. Planta145, 411–416.

    Google Scholar 

  • La Fountain, J. R., Zobel, C. R., Thomas, H. R., Calbreath, C., 1977: Fixation and staining of f-actin and microfilaments using tannic acid. J. Ultrastruct. Res.88, 78–86.

    Google Scholar 

  • Loewenstein, W. R., Kanno, Y., Socolar, J., 1978: The cell-to-cell channel. Fed. Proc.37, 2645–2650.

    Google Scholar 

  • —,Rose, B., 1978: Calcium in (junctional) intercellular communication and a thought on its behaviour in intracellular communication. Ann. N.Y. Acad. Sci.307, 285–307.

    Google Scholar 

  • Löpez-Sáez, J. F., Giménez-Martín, G., Risueño, M. C., 1966: Fine structure of the plasmodesm. Protoplasma61, 81–84.

    Google Scholar 

  • Mitchell, D. J., Ninham, B. W., 1981: Micelles, vesicles and microemulsions. J. Chem. Soc., Faraday Trans. 2,77, 601–629.

    Google Scholar 

  • Nehls, R., Schaffner, G., 1976: Specific negative staining of proteinsin situ with iron tannin. Cytobiol.13, 285–290.

    Google Scholar 

  • Olesen, P., 1975: Plasmodesmata between mesophyll and bundle sheath cells in relation to the exchange of C4-acids. Planta123, 199–202.

    Google Scholar 

  • —, 1978: Structure of chloroplast membranes as revealed by natural and experimental fixation with tannic acid: particles in and on a thylakoid membrane. Biochem. Physiol. Pflanzen172, 319–342.

    Google Scholar 

  • —, 1979: The neck constriction in plasmodesmata: evidence for a peripheral sphincter-like structure revealed by fixation with tannic acid. Planta144, 349–358.

    Google Scholar 

  • —, 1980: A model of a possible sphincter associated with plasmodesmatal neck regions. Europ. J. Cell Biol.22, 250.

    Google Scholar 

  • Overall, R. L., Gunning, B. E. S., 1982: Intercellular communication inAzolla roots II. Electrical coupling. Protoplasma111, 151–160.

    Google Scholar 

  • - - 1982: Intercellular communication in the filamentous green algaOedogonium: electrical coupling and ultrastructure of plasmodesmata. In preparation.

  • Pierson, G. B., Burton, P. R., Himes, R. H., 1979: Wall substructure of microtubules polymerisedin vitro from tubulin of crayfish nerve cord and fixed with tannic acid. J. Cell Sci.39, 89–99.

    Google Scholar 

  • Reiss-Husson, F., Luzzati, V., 1964: The structure of the micellar solution of some amphiphilic compounds in pure water as determined by absolute small angle X-ray scattering techniques. J. phys. Chem.68, 3504–3511.

    Google Scholar 

  • Reynolds, E. S., 1963: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol.17, 208–212.

    Google Scholar 

  • Robards, A. W., 1968: A new interpretation of plasmodesmatal ultrastructure. Planta82, 200–210.

    Google Scholar 

  • —, 1971: The ultrastructure of plasmodesmata. Protoplasma72, 315–323.

    Google Scholar 

  • —, 1976: Plasmodesmata in higher plants. In: Intercellular communication in plants: Studies on plasmodesmata (Gunning, B. E. S., Robards, A. W., eds.), pp. 15–53. Berlin-Heidelberg-New York: Springer.

    Google Scholar 

  • Seagull, R. W., Heath, I. B., 1979: The effects of tannic acid on thein vivo preservation of microfilaments. European J. Cell Biol.20, 184–188.

    Google Scholar 

  • Semenova, G. A., Tageeva, S. V., 1972: Ultrastructural organization of intercellular connections between the plasmodesms of plant cells. Doklady Akad. Nauk SSSR202, 1427–1428.

    Google Scholar 

  • Simonescu, N., Simonescu, M., 1976: Galloylglucoses of low molecular weight as mordants in electron microscopy. J. Cell Biol.70, 608–621.

    Google Scholar 

  • Simpson, I., Rose, B., Loewenstein, W. R., 1977: Size limit of molecules permeating the junctional membrane channels. Science195, 294–296.

    Google Scholar 

  • Spurr, A. R., 1969: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res.26, 31–43.

    Google Scholar 

  • Singer, S. J., Nicholson, G. L., 1972: The fluid mosaic model of the structure of cell membranes. Science175, 720–731.

    Google Scholar 

  • Tanford, C., 1973: The hydrophobic effect, pp. 200. New York: Wiley.

    Google Scholar 

  • Tardieu, A., Luzzati, V., Reman, F. C., 1973: Structure and polymorphism of the hydrocarbon chains of lipids: a study of lecithin-water phases. J. mol. Biol.75, 711–733.

    Google Scholar 

  • Tilney, L. G., Bryan, J., Bush, D. J., Fujiwara, K., Mooseker, M. S., Murphy, D. B., Snyder, D. J., 1973: Microtubules: evidence for 13 protofilaments. J. Cell Biol.59, 267–275.

    Google Scholar 

  • Vian, B., Rougier, M., 1974: Ultrastructure des plasmodesmes après cryoultramicrotomie. J. Microscopie20, 307–312.

    Google Scholar 

  • Wick, S. M., Seagull, R. W., Osborn, M., Weber, K., Gunning, B. E. S., 1981: Immunofluorescence microscopy of organized microtubule arrays in structurally stabilized meristematic plant cells. J. Cell Biol.89, 685–690.

    Google Scholar 

  • Wochok, Z. S., Clayton, D., 1976: Ultrastructure of unique plasmodesmata inSelaginella wildenowii. Planta132, 313–315.

    Google Scholar 

  • Wolfe, J., Steponkus, P. L., 1981: The stress-strain relation of the plasma membrane of isolated plant protoplasts. Biochim. biophys. Acta643, 663–668.

    Google Scholar 

  • Wooding, F. B. P., 1968: Fine structure of callus phloem inPinus pinea. Planta83, 99–110.

    Google Scholar 

  • Zee, S.-Y., 1969: The fine structure of differentiating sieve elements ofVicia faba. Aust. J. Bot.17, 441–456.

    Google Scholar 

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Overall, R.L., Wolfe, J. & Gunning, B.E.S. Intercellular communication inAzolla roots: I. Ultrastructure of plasmodesmata. Protoplasma 111, 134–150 (1982). https://doi.org/10.1007/BF01282071

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  • DOI: https://doi.org/10.1007/BF01282071

Keywords

  • Azolla
  • plasmodesmata
  • desmotubule
  • membrane
  • intercellular communication