Skip to main content
SpringerLink
Log in

Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular communication in higher plants

  • Published:
Planta Aims and scope Submit manuscript

Abstract

It is generally accepted that higher plants evolved from ancestral forms of the modern charophytes. For this reason, we chose the characean alga, Chara corallina Klein ex Willd., em. R.D.W. (C. australis R. Br.), to determine whether this transition species produces plasmodesmata in a manner analogous to higher plants. As with higher plants and unlike most green algae, Chara utilizes a phragmoplast for cell division; however, in contrast with the situation in both lower and higher vascular plants, the developing cell plate and newly formed cell wall were found to be completely free of plasmodesmata. Only when the daughter cells had separated completely were plasmodesmata formed across the division wall. Presumably, highly localized activity of wall-degrading (or loosening) enzymes inserted into the plasma membrane play a central role in this process. In general appearance characean plasmodesmata are similar to those of higher plants with the notable exception that they lack an appressed endoplasmic reticulum. Further secondary modifications in plasmodesmal structure were found to occur as a function of cell development, giving rise to highly branched plasmodesmata in mature cell walls. These findings are discussed in terms of the evolution of the mechanism for plasmodesmata formation in algae and higher plants.

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

References

  • Bisalputra, T. (1966) Electron microscopic study of the protoplasmic continuity in certain brown algae. Can. J. Bot. 44, 89–93

    Google Scholar 

  • Ding, B., Turgeon, R., Parthasarathy, M.V. (1992a) Substructure of freeze substituted plasmodesmata. Protoplasma 169, 28–41

    Google Scholar 

  • Ding, B., Haudenshield, J.S., Hull, R.J., Wolf, S., Beachy, R.N., Lucas, W.J. (1992b) Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4, 915–928

    Google Scholar 

  • Ding, B., Haudenshield, J.S., Willmitzer, L., Lucas, W.J. (1993) Correlation between arrested secondary plasmodesmal development and onset of accelerated leaf senescence in yeast acid invertase transgenic tobacco plants. Plant J., in press

  • Fisher, D.B., Wu, Y, Ku, M.S.B. (1992) Turnover of soluble proteins in the wheat sieve tube. Plant Physiol. 100, 1433–1441

    Google Scholar 

  • Franceschi, V.R., Lucas, W.J. (1980) Structure and possible function(s) of charasomes; complex plasmalemma-cell wall elaborations present in some characean species. Protoplasma 104, 253–271

    Google Scholar 

  • Franceschi, V.R., Lucas, W.J. (1982) The relationship of the charasome to chloride uptake in Chara corallina: physiological and histochemical investigations. Planta 154, 525–537

    Google Scholar 

  • Fraser, T.W, Gunning, B.E.S. (1969) The ultrastructure of plasmodesmata in the filamentous green alga, Bulbochaete hiloensis (Nordst.) Tiffany. Planta 88, 244–254

    Google Scholar 

  • Graham, L.E., Delwiche, C.F., Mishler, B.D. (1991) Phylogenetic connections between the ‘green algae’ and the ‘bryophytes’. Adv. Bryol. 4, 213–244

    Google Scholar 

  • Graham, L.E., Kaneko, Y. (1991) Subcellular structure of relevance to the origin of land plants (Embryophytes) from green algae. Crit. Rev. Plant Sci. 10, 323–342

    Google Scholar 

  • Gunning, B.E.S., Robards, A.W. (1976) Intercellular communication in plants: Studies on plasmodesmata. Springer-Verlag, Berlin, Heidelberg

    Google Scholar 

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

    Google Scholar 

  • Kikuyama, M., Hara, Y., Shimada, K., Yamamoto, K., Hiramoto, Y. (1992) Intercellular transport of macromolecules in Nitella. Plant Cell Physiol. 33, 413–417

    Google Scholar 

  • Kollmann, R., Glockmann, C. (1985) Studies on graft unions. I. Plasmodesmata between cells of plants belonging to different unrelated taxa. Protoplasma 124, 224–235

    Google Scholar 

  • Kollmann, R., Glockmann, C. (1991) Studies on graft unions. III. On the mechanism of secondary formation of plasmodesmata at the graft interface. Protoplasma 165, 71–85

    Google Scholar 

  • Kollmann, R., Yang, S., Glockmann, C. (1985) Studies on graft unions. II. Continuous and half plasmodesmata in different regions of the graft interface. Protoplasma 126, 19–29

    Google Scholar 

  • Kwiatkowska, M. (1988) Symplasmic isolation of Chara vulgaris antheridium and mechanisms regulating the process of spermatogenesis. Protoplasma 142, 137–146

    Google Scholar 

  • Kwiatkowska, M. (1991) Autoradiographic studies on the role of plasmodesmata in the transport of gibberellin. Planta 183, 294–299

    Google Scholar 

  • Kwiatkowska, M., Maszewski, J. (1976) Plasmodesmata between synchronously and asynchronously developing cells of the antheridial filaments of Chara vulgaris L. Protoplasma 87, 317–327

    Google Scholar 

  • Kwiatkowska, M., Maszewski, J. (1985) Changes in ultrastructure of plasmodesmata during spermatogenesis in Chara vulgaris L. Planta 166, 46–50

    Google Scholar 

  • Kwiatkowska, M., Maszewski, J. (1986) Changes in the occurrence and ultrastructure of plasmodesmata in antheridia of Chara vulgaris L. during different stages of spermatogenesis. Protoplasma 132, 179–188

    Google Scholar 

  • Lucas, W.J. (1975) Photosynthetic fixation of 14carbon by internodal cells of Chara corallina. J. Exp. Bot. 26, 331–346

    Google Scholar 

  • Lucas, W.J., Wolf, S. (1993) Plasmodesmata: the intercellular organelle of green plants. Trends Cell Biol., in press

  • Lucas, W.J., Ding, B., van der Schoot, C. (1993) Plasmodesmata & the supracellular nature of plants. New Phytol., in press

  • Oliveira, L., Bisalputra, T. (1973) Studies in the brown alga Ectocarpus in culture. I. General ultrastructure of the sporophytic vegetative cells. J. Submicrosc. Cytol. 5, 107–120

    Google Scholar 

  • Pickett-Heaps, J.D. (1967a) Ultrastructure and differentiation in Chara sp. I. Vegetative cells. Aust. J. Biol. Sci. 20, 539–551

    Google Scholar 

  • Pickett-Heaps, J.D. (1967b) Ultrastructure and differentiation in Chara sp. II. Mitosis. Aust. J. Biol. Sci. 20, 883–894

    Google Scholar 

  • Pickett-Heaps, J.D. (1968) Ultrastructure and differentiation in Chara (fibrosa). IV. Spermatogenesis. Aust. J. Biol. Sci. 21, 655–690

    Google Scholar 

  • Pickett-Heaps, J.D. (1975) Green algae: structure, reproduction and evolution in selected genera. Sinauer Associates, Inc., Sunderland, Massachusetts

    Google Scholar 

  • Porter K.R., Machado, R.D. (1960) Studies on the endoplasmic reticulum. IV. Its form and distribution during mitosis in cells of onion root tip. J. Biophys. Biochem. Cytol. 7, 167–180

    Google Scholar 

  • Robards, A.W, Lucas, W.J. (1990) Plasmodesmata. Annu. Rev. Plant Physiol. Plant Molec. Biol. 41, 369–419

    Google Scholar 

  • Schmitz, K., Kühn, R. (1982) Fine structure, distribution and frequency of plasmodesmata and pits in the cortex of Laminaria hyperborea and L. saccharina. Planta 154, 385–392

    Google Scholar 

  • Schmitz, K., Srivastava, L.M. (1974) Fine structure and development of sieve tubes in Laminaria groenlandica Rosenv. Cytobiologie 10, 66–87

    Google Scholar 

  • Schmitz, K., Srivastava, L.M. (1975) On the fine structure of sieve tubes and the physiology of assimilate transport in Alaria marginata. Can. J. Bot. 53, 861–876

    Google Scholar 

  • Spanswick, R.M., Costerton, J.W.F. (1967) Plasmodesmata in Nitella translucens: structure and electrical resistance. J. Cell Sci. 2, 451–464

    Google Scholar 

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

    Google Scholar 

  • Steinbiß, H.-H., Schmitz, K. (1973) CO2-Fixierung und Stofftransport in benthischen marinen Algen. V. Zur autoradiographischen Lokalisatian der Assimilattransportbahnen im Thallus von Laminaria hyperborea. Planta 112, 253–263

    Google Scholar 

  • Stewart, K.D., Mattox, K.R., Floyd, G.L. (1973) Milosis, cytokinesis, the dislribution of plasmodesmata, and other cytological characteristics in the Ulotrichales, Ulvales and Chaetophorales: Phylogenetic and taxonomic considerations. J. Phycol. 9, 128–141

    Google Scholar 

  • Tilney, L.G., Cooke, T.J, Connelly, P.S., Tilney, M.S. (1991) The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J. Cell Biol. 112, 739–747

    Google Scholar 

  • Turner, F.R. (1968) An ultrastructural study of plant spermatogenesis: Spermatogenesis in Nitella. J. Cell Biol. 37, 370–393

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Washington State University, 99164-4238, Pullman, WA, USA

    Vincent R. Franceschi

  2. Section of Plant Biology, Division of Biological Sciences, University of California, 95616, Davis, CA, USA

    Biao Ding & William J. Lucas

Authors
  1. Vincent R. Franceschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Biao Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William J. Lucas
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This work was supported in part by National Foundation grant No. DCB-9016756 (W.J.L.). We thank the Electron Microscopy Center of Washington State University and the Zoology Department, University of California, Davis, for the use of their microscopy facilities.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Franceschi, V.R., Ding, B. & Lucas, W.J. Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular communication in higher plants. Planta 192, 347–358 (1994). https://doi.org/10.1007/BF00198570

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00198570

Key words

Search

Navigation