Skip to main content
SpringerLink
Log in

Ultrastructure and functioning of the transport system of the leguminous root nodule

  • Published:
Planta Aims and scope Submit manuscript

Summary

The structure of the vascular tissues of nitrogen-fixing nodules of 27 genera of legumes and some non-legumes has been investigated by light microscopy. Pisum and Trifolium nodules have been examined by electron microscopy.

Attention is directed to the presence of a pericycle in the vascular bundles of the nodules. In 7 of the legumes the pericycle cells possess a wall labyrinth consisting of branched filiform protuberances. The ultrastructure of the pericycle cell cytoplasm is described: its most striking feature is its abundant rough endoplasmic reticulum. These cells surround the xylem and phloem of the bundles, and are in turn surrounded by a layer of endodermal cells with Casparian strips. The pericycle cells develop their wall labyrinth in the levels of the nodule at which the bacterial tissue becomes pigmented; in nodule senescence their cytoplasm is disrupted level with the breakdown of the bacterial tissue.

A pathway for symplastic lateral transfer of assimilates exists, from the sieve elements through the pericycle, endodermis and cortex to the bacterial tissue. The apoplast within the endodermis consists largely of the pericycle wall labyrinth and the xylem. The ultrastructure of the Casparian strip resembles that of roots.

Intact, detached nodules can be induced to bleed a fluid from their severed vascular tissue. This fluid is exceptionally rich in organic nitrogen, particularly amides, but does not appear to contain sugars. Comparison between its amino acid composition and that of other parts of the nodule suggests that an active uptake or secretion of nitrogenous compounds precedes export from the nodule. Special functions are suggested for the nodule endodermis and the pericycle cells in this export process.

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

  • Allen, E.K., K.F. Gregory, and O.N. Allen: Morphological development of nodules on Caragana arborescens Lam. Canad. J. Bot. 33, 139–147 (1955).

    Google Scholar 

  • Allen, O.N., and E.K. Allen: Morphogenesis of the leguminous root nodule. Brookhaven Symp. Biol. No 6, 209–234 (1954).

  • Arisz, W.H.: Significance of the symplasm theory for transport in the root. Protoplasma 46, 5–62 (1956).

    Google Scholar 

  • Bieberdorf, F.W.: The cytology and histology of the root nodules of some Leguminoasae. J. Amer. Soc. Agron. 30, 375–389 (1938).

    Google Scholar 

  • Bond, G.: Quantitative observations on the fixation and transfer of nitrogen in the soya bean, with especial reference to the mechanism of transfer of fixed nitrogen from bacillus to host. Ann. Bot. (Lond.) 50, 559–578 (1936).

    Google Scholar 

  • —: Some biological aspects of nitrogen fixation. Symp. Long Ashton, Bristol, p. 15–25. London: Academic Press 1968.

    Google Scholar 

  • Bond, L.: Origin and developmental morphology of root nodules of Pisum sativum. Bot. Gaz. 109, 411–434 (1948).

    Article  Google Scholar 

  • Bonnett, H.T.: The root endodermis: fine structure and function. J. Cell. Biol. 37, 199–205 (1968).

    Article  PubMed  Google Scholar 

  • Brenchley, W.E., and H.G. Thornton: The relation between the development, structure and functioning of the nodules on Vicia faba, as influenced by the presence or absence of boron in the nutrient solution. Proc. roy. Soc. B 98, 373–398 (1925).

    Google Scholar 

  • Crafts, A.S., and T.C. Broyer: Migration of salts and water into xylem of the roots of higher plants. Amer. J. Bot. 25, 529–535 (1938).

    Google Scholar 

  • Dangeard, P.A.: Recherches sur les tubercles radicaux des Légumineuses. Botaniste 16, 1–260 (1926).

    Google Scholar 

  • Diboll, A.G.: Fine structural development of the megagametophyte of Zea mays following fertilization. Amer. J. Bot. 55, 787–806 (1968).

    Google Scholar 

  • Dörr, I.: Fembau der Kontakte zwischen Cuscuta-Hyphen und den Siebröhren ihrer Wirtspflanzen. Vortr. Bot., N. F. 2, 24–26 (1968).

    Google Scholar 

  • Esau, K.: Minor veins in Beta leaves: structure related to function. Proc. Amer. phil. Soc. 111, 219–233 (1967).

    Google Scholar 

  • Eymé, J.: Nouvelles observations sur l'infrastructure de tissus nectarigènes floraux. Botaniste 50, 169–183 (1967).

    Google Scholar 

  • —, and C. Suire: Au sujet de l'infrastructure des cellules de la région placentaire de Mnium cuspidatum Hedw. (Mousse bryale acrocarpe). C. R. Acad. Sc. (Paris) 265. 1788–1791 (1967).

    Google Scholar 

  • Falk, H., u. P. Sitte: Untersuchungen am Caspary-Streifen. Proc. Eur. Reg. Conf. on Electron Microscopy, Delft 2, 1063–1066 (1960).

    Google Scholar 

  • ——: Zellfeinbau bei Plasmolyse I. Der Feinbau der Elodea-Blattzellen. Protoplasma (Wien) 57, 290–303 (1963).

    Google Scholar 

  • Feder, N., and T.P. O'Brien: Plant microtechnique: some principles and new methods. Amer. J. Bot. 55, 123–144 (1968).

    Google Scholar 

  • Figier, J.: Localisation infrastructurale de la phosphomonoestérase acide dans la stipule de Vicia faba L. au niveau du nectaire. Planta (Berl.) 83, 60–79 (1968).

    Google Scholar 

  • Frazer, H.L.: The occurrence of endodermis in leguminous root nodules and its effect upon nodule function. Proc. roy. Soc. Edinb. B 61, 328–343 (1942).

    Google Scholar 

  • Freere, R.H., and E.R. Weibel: Stereologic techniques in microscopy. J. roy. micr. Soc. 87, 25–34 (1967).

    PubMed  Google Scholar 

  • Gibson, A.H.: The carbohydrate requirements for symbiotic nitrogen fixation. A “whole plant” growth analysis approach. Aust. J. biol. Sci. 19, 499–515 (1966).

    Google Scholar 

  • Gunning, B.E.S., J.S. Pate, and L.G. Briarty: Specialized “Transfer Cells” in minor veins of leaves and their possible significance in phloem translocation. J. Cell Biol. 37, C 7–12 (1968).

    Article  Google Scholar 

  • Harris, J.O., E.K. Allen, and O.N. Allen: Morphological development of nodules on Sesbania grandiflora Poir., with reference to the origin of nodule rootlets. Amer. J. Bot. 36, 651–661 (1949).

    Google Scholar 

  • Helander, H.F.: Morphology of animal secretory gland cells. In: Sekretion und Exkretion, funktionelle und morphologische Organisation der Zelle. Bd. 2, 2–21. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • Jensen, W.A.: The ultrastructure and histochemistry of the synergids of cotton. Amer. J. Bot. 52, 238–256 (1965).

    Google Scholar 

  • Ledbetter, M.C.: The Casparian strip: a site of a functional tight junction in plant roots. J. Cell Biol. 35, 79A (1967).

    Google Scholar 

  • Lüttge, U.: Untersuchungen zur Physiologie der Carnivoren-Drüsen II. Über die Resorption verschiedener Substanzen. Planta (Berl.) 66, 331–344 (1965).

    Google Scholar 

  • —: Funktion und Struktur pflanzlicher Drüsen. Naturwissenschaften 53, 96–103 (1966).

    Google Scholar 

  • —, and G.G. Laties: Dual mechanisms of ion absorption in relation to long distance transport in plants. Plant Physiol. 41, 1531–1539 (1966).

    Google Scholar 

  • Maier, K.: Wandlabyrinthe im Sporophyten von Polytrichum. Planta (Berl.) 77, 108–126 (1967).

    Google Scholar 

  • Marquardt, H., O.M. Barth, and U.v. Rahden: Zytophotometrische und elektronenmikroskopische Beobachtungen über die Tapetumzellen in den Antheren von Paeonia tenuifolia. Protoplasma (Wien) 65, 407–421 (1968).

    Google Scholar 

  • Mollenhauer, H.H.: Plastic embedding mixtures for use in electron microscopy. Stain Technol. 39, 111–114 (1964).

    PubMed  Google Scholar 

  • Pate, J.S.: Nodulation studies in legumes I. The synchronization of host and symbiotic development in the field pea, Pisum arvense L. Aust. J. biol. Sci. 11, 366–381 (1958).

    Google Scholar 

  • —: Root-exudation studies on the exchange of C14-labelled organic substances between the roots and shoot of the nodulated legume. Plant and Soil (Den Haag) 17, 333–356 (1962).

    Google Scholar 

  • —: Physiological aspects of inorganic and intermediate nitrogen metabolism. Symp. Long Ashton. Bristol, p. 219–240. London: Academic Press 1968.

    Google Scholar 

  • Pluijm, J.E.: An electron microscopic investigation of the filiform apparatus in the embryo sac of Torenia fournieri. In: Pollen physiology and fertilization, p. 8–16. Amsterdam: North Holland Publ. Co. 1963.

    Google Scholar 

  • Renaudin, S.: Sur les glandes de Lathraea clandestina L. Bull. Soc. Bot. Fr. 113, 379–385 (1966).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Scala, J., D. Schwab, and E. Simmons: The fine structure of the digestive gland of Venus's flytrap. Amer. J. Bot. 55, 649–657 (1968).

    Google Scholar 

  • Schnepf, E.: Zur Feinstruktur der Drüsen von Drosophyllum lusitanicum. Planta (Berl.) 54, 641–674 (1960).

    Google Scholar 

  • —: Zur Cytologie und Physiologie pflanzlicher Drüsen I. Über den Fangschleim der Insektivoren. Flora (Jena) 153, 1–22 (1963).

    Google Scholar 

  • —: Zur Cytologie und Physiologie pflanzlicher Drüsen IV. Licht-und elektronenmikroskopische Untersuchungen an Septalnektarien. Protoplasma (Wien) 58, 137–171, (1964).

    Google Scholar 

  • —: Physiologie und Morphologie sekretorischer Pflanzenzellen. In: Sekretion und Exkretion, funktionelle und morphologische Organisation der Zelle, Bd. 2, 72–88. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • Schulz, R., and W.A. Jensen: Capsella embryogenesis: the synergids before and after fertilization. Amer. J. Bot. 55, 541–552 (1968).

    Google Scholar 

  • Shimony, C., and A. Fahn: Light- and electron-microscopical studies on the structure of salt glands of Tamarix aphylla L. J. Linn. Soc. (Bot.) 60, 283–287 (1968).

    Google Scholar 

  • Thomson, W.W., and L. Liu: Ultrastructural features of the salt gland of Tamarix aphylla L. Planta (Berl.) 73, 201–220 (1967).

    Google Scholar 

  • Thornton, H.G., and J.E. Rudorf: The abnormal structure induced in nodules of Lucerne (Medicago sativa L.) by the supply of sodium nitrate to the host plant. Proc. roy. Soc. B 120, 240–252 (1936).

    Google Scholar 

  • Vogel, A.: Zur Feinstruktur der Drüsen von Pinguicula. Beih. Z. schweiz. Forstverw. 30, 113–122 (1960).

    Google Scholar 

  • Wieringa, K.T., and J.A. Bakhuis: Chromatography as a means of selecting effective strains of Rhizobia. Plant and Soil (Den Haag) 8, 254–260 (1957).

    Google Scholar 

  • Wilson, J.K.: The loss of nodules from legume roots and its significance. J. Amer. Soc. Agron. 34, 460–464 (1942).

    Google Scholar 

  • Wooding, F.B.P., and D.H. Northcote: An anomalous wall thickening and its possible role in the uptake of stem-fed tritiated glucose by Pinus pinea. J. Ultrastruct. Res. 12, 463–472 (1965).

    PubMed  Google Scholar 

  • Wrischer, M.: Elektronenmikroskopische Beobachtungen an extrafloralen Nektarien von Vicia faba L. Acta bot. Croatica 21, 75–94 (1962).

    Google Scholar 

  • Wylie, R.B.: Relations between tissue organization and vein distribution in dicotyledon leaves. Amer. J. Bot. 26, 219–255 (1939).

    Google Scholar 

  • Ziegler, H.: Die Physiologie pflanzlicher Drüsen. Ber. dtsch. bot. Ges. 78, 466–477 (1965).

    Google Scholar 

  • —, u. U. Lüttge: Die Salzdrüsen von Limonium vulgare. I. Die Feinstruktur. Planta (Berl.) 70, 193–206 (1966).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Botany Department, Queen's University, Belfast, N. Ireland

    J. S. Pate, B. E. S. Gunning & L. G. Briarty

Authors
  1. J. S. Pate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. E. S. Gunning
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. G. Briarty
    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

Pate, J.S., Gunning, B.E.S. & Briarty, L.G. Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta 85, 11–34 (1969). https://doi.org/10.1007/BF00387658

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00387658

Keywords

Search

Navigation