Identification of the endophypte of Dryas and Rubus (Rosaceae)

  • J. H. Becking
Part of the Developments in Plant and Soil Sciences book series (DPSS, volume 12)


Root nodules of Dryas drummondii are of the coralloid type (Alnus type). The endophyte is present in the middle cortical cells of the root-nodule tissue. Transmission electron micrographs revealed an actinorhizal endophyte with septate hyphae and non-septate spherical or ovoid vesicles. Vesicles always possess at the base a septum; septa formation in the endophyte is always associated with the presence of mesosomes. Branching of the endophyte is not necessarily correlated with septum formation. Hyphal structures are more prominent in the apical part of the root nodule and vesicles are more numerous in a broad zone below this. In the middle and towards the base of the root nodule the endophytic structures appear in a stage of disintegration. Vesicles appear in a broad region near the periphery of the host cell and regularly show no strict orientation towards the host-cell wall. In the center of the host cells only hyphae occur. In the intercellular spaces between the host cells the Frankia endophyte produces spore-like structures although the outline of the sporangia is often faint.

The coralloid root of Rubus ellipticus shows characteristically a basal rootlet initiated below the dichotomous branching of the nodular lobes, but extending beyond the root nodule. The endophyte is only present in the outer cortex of the root nodule in a 1–2 cell wide layer. This endophytic layer is bounded, internally as well as externally, with a 4–5 cell wide layer of tannin-filled host cells. The implications of this situation are discussed. Tannin-filled cells occur regularly in Rubus species and their arrangement has been used for taxonomic purposes within the genus. The Rubus endophyte is a Frankia species with septate hyphae and distinctly septate spherical vesicles. The ultrastructure of the vesicles of the Rubus endophyte is very similar to that of the Alnus endophyte.

Key words

Cytology of root nodules Dryas drummondii Frankia Geographic distribution Nitrogen fixation Rubus ellipticus Ultrastructure of endophyte 


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  1. 1.
    Allen E K, Allen O N and Klebesadel L J 1963 An insight into symbiotic nitrogen-fixing plant associations in Alaska. Science in Alaska, Proc. 14th Alaskan Sci. Conf., Anchorage, Alaska, pp 54–63.Google Scholar
  2. 2.
    Becking J H 1977 Dinitrogen-fixing associations in higher plants other than Legumes. In A Treatise on Dinitrogen Fixation, Section III: Biology. Eds. R W F Hardy and W S Silver, John Wiley & Sons, New York, 185–275.Google Scholar
  3. 3.
    Becking J H 1979 Nitrogen fixation by Rubus ellipticus J E Smith. Plant and Soil 53, 541–545.Google Scholar
  4. 4.
    Becking J H, De Boer, W E and Houwink A L 1964 Electron microscopy of the endophyte of Alnus glutinosa. Antonie van Leeuwenhoek, J. Microbiol. Serol. 30, 343–376.Google Scholar
  5. 5.
    Bond G 1976 The results of the IBP survey of root-nodule formation in non-leguminous angiosperms. In Symbiotic Nitrogen Fixation in Plants. Ed. P S Nutman, Int. Biol. Programme, vol. 7, Cambridge Univ. Press, pp 443–474.Google Scholar
  6. 6.
    Bond G 1976 Observations on the root nodules of Purshia tridentate. Proc. R. Soc. Lond. B, 193, 127–135.CrossRefGoogle Scholar
  7. 7.
    Bond G and Becking J H 1982 Root nodules in the genus Colletia. New Phytol. 90, 57–65.CrossRefGoogle Scholar
  8. 8.
    Chaudhary A H, Khokhar, S N, Zafar, Y and Hafèez, F 1981 Actinomycetous root nodules in Angiosperms of Pakistan. Plant and Soil 60, 341–348.CrossRefGoogle Scholar
  9. 9.
    Edwards M R and Gordon M A 1962 Membrane systems of Actinomyces bovin, In Electron Microscopy. Ed. S S Breese Jr., 5th Int. Congr. Electron Microscopy, Academic Press, New York, p. UU-3.Google Scholar
  10. 10.
    Edwards M R and Stevens, R W 1963 Fine structure of Listeria monocytogenes. J. Bacteriol. 86, 414–428.PubMedGoogle Scholar
  11. 11.
    Fitz-James P C 1960 Participation of the cytoplasmic membrane in the growth and spore formation of Bacilli. J. Biophys. Biochem. Cytol. 8, 507–528.PubMedCrossRefGoogle Scholar
  12. 12.
    Fritsch F E 1887 Anatomische systematische Studien über die Gattung Rubus. Sitz.-Ber. Wiener Akad. 95, 28 pp and 2 Plates.Google Scholar
  13. 13.
    Gardner I C 1976 Ultrastructural studies of non-leguminous root nodules. In Symbiotic Nitrogen Fixation in Plants. Ed. P S Nutman. Int. Biol. Programme, vol 7, Cambridge Univ. Press, pp 485–495.Google Scholar
  14. 14.
    Gardner I C and Gatner E M S 1973 The formation of vesicles in the developmental cycle of the nodular endophyte of Hippophaé rhamnoides L. Arch. Mikrobiol. 89, 233–240.CrossRefGoogle Scholar
  15. 15.
    Gerlach D 1969 Botanische Mikrotechnik. Verlag Georg Thieme, Stuttgart, 298 p.Google Scholar
  16. 16.
    Heisey R M, Delwiche C C, Virginia R A, Wrona, A F and Bryan, B A 1980 A new nitrogen-fixing non-legume: Chanzaebatia foliose (Rosaceae). Am. J. Bot. 67, 429–431.CrossRefGoogle Scholar
  17. 17.
    Hutchinson J 1964 The Genera of Flowering Plants (Angiospermae), vol.1, Dicotyledones. Clarendon Press, Oxford, 516 p.Google Scholar
  18. 18.
    Lalonde M 1978 Confirmation of the infectivity of a free-living actinomycete isolated from Comptonia peregrina (L.) Coult. root nodules by immunological and ultrastructural studies. Can J. Bot. 56, 2621–2635.CrossRefGoogle Scholar
  19. 19.
    Lalonde M 1979 Immunological and ultrastructural demonstration of nodulation of the European Alnus glutinosa (L.) Gaertn. host plant by an actinomycetal isolate from the North American Comptonia peregrine (L.) Coult. root nodule. Bot. Gaz. (Chicago) 140 (Suppl.), S35–43.CrossRefGoogle Scholar
  20. 20.
    Lalonde M, Knowles R and Devoe I W 1976 Absence of `void area’ in freeze-etched vesicles of the Alnus crispa var. mollis Fern. root nodule endophyte. Arch. Microbiol. 107, 263–267.CrossRefGoogle Scholar
  21. 21.
    Lawrence D B, Schoenike R E, Quispel A and Bond G 1967 The role of Dryas drummondii in vegetation development following ice recession at Glacier Bay, Alaska, with special reference to its nitrogen fixation by root nodules. J. Ecol. 55, 793–813.CrossRefGoogle Scholar
  22. 22.
    Löhnis M P 1930 Investigations upon the ineffectiveness of root-nodules on leguminosae. Zentr. Bakteriol. Parasitenkd. II Abt. 80, 342–368.Google Scholar
  23. 23.
    Metcalfe C R and Chalk, L 1950 Anatomy of the Dicotyledons, vol. 1, Clarendon Press, Oxford, 724 p.Google Scholar
  24. 24.
    Metcalfe C R and Chalk L 1983 Anatomy of the Dicotyledons, vol. 2, 2nd Ed., Wood structure and Conclusion of the General Introduction. Clarendon Press, Oxford, 297 p.Google Scholar
  25. 25.
    Newcomb W 1981 Fine structure of the root nodules of Dryas drummondii Richards (Rosaceae). Can. J. Bot. 59, 2500–2514.CrossRefGoogle Scholar
  26. 26.
    Righetti T L and Munns D N 1980 Nodulation and nitrogen fixation in Cliffrose (Cowania mexicana var. stansburiana (Torr.) Jeps.). Plant Physiol. 65, 411–412.PubMedCrossRefGoogle Scholar
  27. 27.
    Schulze-Menz G K 1964 Rosales. In A. Engler’s Syllabus der Pflanzenfamilien, 12th ed. Ed. H Melchior, Gebr. Borntraeger, Berlin, 193–242.Google Scholar
  28. 28.
    Solereder H 1899 Systematische Anatomie der Dicotylendonen. Verlag Ferd. Enke, Stuttgart, 984 pp.Google Scholar
  29. 29.
    Strand R and Laetsch W M 1977 Cell and endophyte structure of the nitrogen-fixing root nodules of Ceanothus integerrimus H. and A, I. Fine structure of the nodule and its endosymbiont. Protoplasma 93, 165–178.CrossRefGoogle Scholar
  30. 30.
    Strand R and Laetsch W M 1977 Cell and endophyte structure of the nitrogen-fixing root nodules of Ceanothus integerrirnus H. and A. II. Progress of the endophyte into young cells of the growing nodule. Protoplasma 93, 179–190.CrossRefGoogle Scholar
  31. 31.
    Tjepkema J D and Cartica R J 1982 Diffusion limitation of oxygen uptake and nitrogenase activity in the root nodules of Parasponia rigida. Plant Physiol. 69, 728–733.PubMedCrossRefGoogle Scholar
  32. 32.
    Willis J C 1973 A Dictionary of the Flowering Plants and Ferns, 8th ed. (Revised by H K Airy Shaw), Cambridge Univ. Press, Cambridge, 1245 p.Google Scholar

Copyright information

© Martinus Nijhoff/Dr W. Junk Publishers, The Hague 1984

Authors and Affiliations

  • J. H. Becking
    • 1
  1. 1.Research Institute ITALWageningenThe Netherlands

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