Skip to main content
SpringerLink
Log in

Substructure of freeze-substituted plasmodesmata

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The substructure of plasmodesmata in freeze-substituted tissues of developing leaves of the tobacco plant (Nicotiana tabacum L. var. Maryland Mammoth) was studied by high resolution electron microscopy and computer image enhancement techniques. Both the desmotubule wall and the inner leaflet of the plasmodesmatal plasma membrane are composed of regularly spaced electron-dense particles approximately 3 nm in diameter, presumably proteinaceous and embedded in lipid. The central rod of the desmotubule is also particulate. In plasmodesmata with central cavities, spoke-like extensions are present between the desmotubule and the plasma membrane in the central cavity region. The space between the desmotubule and the plasma membrane appears to be the major pathway for intercellular transport through plasmodesmata. This pathway may be tortuous and its dimensions could be regulated by interactions between desmotubule and plasma membrane particles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ER:

endoplasmic reticulum

PJF:

propane jet freezing

HPF:

high pressure freezing

CRT:

cathode ray tube

IP3 :

inositoltrisphosphate

References

  • Baron-Epel O, Hernandez D, Jiang LW, Meiners S, Schindler M (1988) Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Gell Biol 106: 715–721

    Google Scholar 

  • Burgess J (1971) Observations on structure and differentiation in plasmodesmata. Protoplasma 73: 83–95

    Google Scholar 

  • Calvert HE, Pence MK, Peters GA (1986) Ultrastructural ontogeny of leaf cavity trichomes inAzolla implies a functional role in metabolite exchange. Protoplasma 129: 10–27

    Google Scholar 

  • Ding B, Parthasarathy MV, Niklas K, Turgeon R (1988) A morphometric analysis of the phloem unloading pathway in developing tobacco leaves. Planta 176: 307–318

    Google Scholar 

  • —, Turgeon R, Parthasarathy MV (1991 a) Plasmodesmatal substructure in cryofixed developing tobacco leaf tissue. In: Bonnemain JL, Delrot S, Dainty J, Lucas WJ (eds) Recent advances in phloem transport and assimilate compartmentation. Quest Editions, Nantes, pp 317–323

    Google Scholar 

  • — — — (1991 b) Routine cryofixation of plant tissues by propane jet freezing for freeze substitution. J Electron Microsc Techn 19: 107–117

    Google Scholar 

  • — — — (1991 c) Microfilament organization and distribution in freeze substituted tobacco plant tissues. Protoplasma 165: 96–105

    Google Scholar 

  • Erwee MG, Goodwin PB (1983) Characterization of theEgeria densa Planch, leaf symplast. Inhibition of the intercellular movement of fluorescent probes by group II ions. Planta 158: 320–328

    Google Scholar 

  • Evert RF, Eschrich W, Heyser W (1977) Distribution and structure of plasmodesmata in mesophyll cells ofZea mays L. Planta 136: 77–89

    Google Scholar 

  • Fujiwara K, Link RW (1982) The use of tannic acid in microtubule research. In: Wilson L (ed) Methods in cell biology. Academic Press, New York, pp 217–233

    Google Scholar 

  • Futaesaku Y, Mizuhira V, Nakamura H (1972) The new fixation method using tannic acid for electron microscopy and some observations of biological specimens. In: Proceedings of the IVth International Congress for Histochemistry and Cytochemistry, pp 155–166

  • Goodwin PB (1983) Molecular size limit for movement in the symplast of theElodea leaf. Planta 157: 124–130

    Google Scholar 

  • Gunning BES, Hughes JE (1976) Quantitative assessment of symplastic transport of pre-nectar into the trichomes ofAbutilon nectaries. Aust J Plant Physiol 3: 619–637

    Google Scholar 

  • —, Overall RL (1983) Plasmodesmata and cell-to-cell transport in plants. BioScience 33: 260–265

    Google Scholar 

  • , Robards AW (eds) (1976) Intercellular communication in plants: studies on plasmodesmata. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Hepler PK (1982) Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111: 121–133

    Google Scholar 

  • Lancelle SA, Cresti M, Hepler PK (1987) Ultrastructure of the cytoskeleton in freeze-substituted pollen tubes ofNicotiana alata. Protoplasma 140: 141–150

    Google Scholar 

  • Lopez-Saez JF, Gimenez-Martin G, Risueno MC (1966) Fine structure of the plasmodesm. Protoplasma 61: 81–84

    Google Scholar 

  • Markham R, Frey S, Hills GJ (1963) Methods for the enhancement of image detail and accentuation of structure in electron microscopy. Virology 20: 88–102

    Google Scholar 

  • Millonig G, Marinozzi V (1968) Fixation and embedding in electron microscopy. In: Barer R, Cosslett VE (eds) Advances in optical and electron microscopy, vol 2. Academic Press, New York, pp 251–341

    Google Scholar 

  • Mollenhauer HH, Morré DJ (1987) Some unusual staining properties of tannic acid in plants. Histochemistry 88: 17–22

    Google Scholar 

  • Olesen P (1979) The neck constriction in plasmodesmata evidence for a peripheral sphincter-like structure revealed by fixation with tannic acid. Planta 144: 349–358

    Google Scholar 

  • —, Robards AW (1990) The neck region of plasmodesmata: general architecture and some functional aspects. In: Robards AW, Jongsma H, Lucas WJ, Pitts J, Spray D (eds) Parallels in cell to cell junctions in plants and animals. Springer, Berlin Heidelberg New York Tokyo, pp 145–170

    Google Scholar 

  • Overall RL, Wolfe J, Gunning BES (1982) Intercellular communication inAzolla roots: I. Ultrastructure of plasmodesmata. Protoplasma 111: 134–150

    Google Scholar 

  • Paine PL, Moor LC, Horowitz SB (1975) Nuclear envelope permeability. Nature 254: 109–114

    Google Scholar 

  • Palevitz BA, Hepler PK (1985) Changes in dye coupling of stomatal cells ofAllium andCommelina demonstrated by microinjection of Lucifer Yellow. Planta 164: 473–479

    Google Scholar 

  • Robards AW (1968) A new interpretation of plasmodesmatal ultrastructure. Planta 82: 200–210

    Google Scholar 

  • — (1971) The ultrastructure of plasmodesmata. Protoplasma 72: 315–323

    Google Scholar 

  • — (1976) Plasmodesmata in higher plants. In: Gunning BES, Robards AW (eds) Intercellular communication in plants: studies on plasmodesmata. Springer, Berlin Heidelberg New York, pp 15–57

    Google Scholar 

  • —, Lucas WJ (1990) Plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 41: 369–419

    Google Scholar 

  • Scalet M, Crivellato E, Mallardi F (1989) Demonstration of phenolic compounds in plant tissues by an osmium-iodide postfixation procedure. Stain Technol 64: 273–280

    Google Scholar 

  • Seagull RW, Heath IB (1979) The effect of tannic acid on the in vivo preservation of microfilaments. Eur J Cell Biol 20: 184–188

    Google Scholar 

  • — — (1980) The differential effects of cytochalasin B on microfilament populations and cytoplasmic streaming. Protoplasma 103: 231–240

    Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31–43

    Google Scholar 

  • Terry BR, Robards AW (1987) Hydrodynamic radius alone governs the mobility of molecules through plasmodesmata. Planta 171: 145–157

    Google Scholar 

  • Thomson WW, Platt-Aloia WW (1985) The ultrastructure of the plasmodesmata of the salt glands ofTamarix aphylla as revealed by transmission electron microscopy and freeze fracture electron microscopy. Protoplasma 125: 13–23

    Google Scholar 

  • Tilney LG, Bryan J, Bush DJ, Fujiwara K, Mooseker MS, Murphy DB, Snyder DH (1973) Microtubules: evidence for 13 protofilaments. J Cell Biol 59: 267–275

    Google Scholar 

  • —, Cooke TJ, Connelly PS, Tilney MS (1991) The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J Cell Biol 122: 73–747

    Google Scholar 

  • Tiwari SC, Polito VS (1988) Organization of the cytoskeleton in pollen tubes ofPyrus communis: a study employing conventional and freeze-substitution electron microscopy, immunofluorescence, and rhodamine-phallaidin. Protoplasma 147: 100–112

    Google Scholar 

  • —, Wick SM, Williamson RE, Gunning BES (1984) Cytoskeleton and integration of cellular function in cells of higher plants. J Cell Biol 99: 63s-69s

    Google Scholar 

  • Tucker EB (1988) Inositol bisphosphate and inositol triphosphate inhibit cell-to-cell passage of carboxyfluorescein in staminal hairs ofSetcreasea purpurea. Planta 174: 358–363

    Google Scholar 

  • — (1990) Calcium-loaded 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid blocks cell-to-cell diffusion of carboxyfluorescein in staminal hairs ofSetcreasea purpurea. Planta 82: 34–38

    Google Scholar 

  • Turgeon R (1984) Termination of nutrient import and development of vein loading capacity of albino tobacco leaves. Plant Physiol 76: 45–48

    Google Scholar 

  • — (1987) Phloem unloading in tobacco sink leaves: insensitivity to anoxia indicates a symplastic pathway. Planta 171: 73–81

    Google Scholar 

  • Willison JHM (1976) Plasmodesmata: a freeze fracture view. Can J Bot 54: 2842–2847

    Google Scholar 

  • Yahalom A, Warmbrodt RD, Laird DW, Traub O, Revel JP, Willecke K, Epel BL (1991) Maize mesocotyl plasmodesmata proteins crossreact with connexin gap junction protein antibodies. Plant Cell 3: 407–417

    Google Scholar 

  • Zee SY (1969) The fine structure of differentiating sieve elements ofVicia faba. Aust J Bot 17: 441–456

    Google Scholar 

Download references

Author information

Author notes

  1. B. Ding

    Present address: Department of Botany, University of California, Davis, California, USA

Authors and Affiliations

  1. Section of Plant Biology, Division of Biological Sciences, Cornell University, 14853, Ithaca, NY, USA

    B. Ding, R. Turgeon & M. V. Parthasarathy

Authors
  1. B. Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Turgeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. V. Parthasarathy
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ding, B., Turgeon, R. & Parthasarathy, M.V. Substructure of freeze-substituted plasmodesmata. Protoplasma 169, 28–41 (1992). https://doi.org/10.1007/BF01343367

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01343367

Keywords

Search

Navigation