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The legume Rhizosphere

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Summary

Examination of the root surfaces of Medicago tribuloides Desr. with phase contrast microscopy or electron microscopy using thin sections revealed the presence of a layer of material outside the root surface. In thin sections of KMnO4 fixed roots this layer was composed of a thin electron dense layer, an electron dense granular matrix of varying width and an enclosing electron dense membrane. After inoculation with an effective Rhizobium strain, rhizobia were found aggregated in a definite zone adjacent to the root surface when either living roots were examined by phase microscopy or thin sections by electron microscopy. This layer was also found in inoculated and uninoculated roots of Trifolium fragiferum and T. pratense. The bacteria were packed with inclusion granules and lay enclosed by a membrane layer adjacent to the granular matrix seen in uninoculated roots. The ultrastructural organisation of root hairs is essentially similar to that of other differentiated root cells. The replicated surface of the uninoculated root hair wall is largely amorphous with a few sculptured portions resembling a cuticle layer. The inoculated root hair wall often shows areas of exposed, open microfibrillar meshwork with rhizobia sitting on the microfibrils. The rhizobia resemble a flagellated, coccoid swarmer form of Rhizobium which is found in the barrel medic rhizosphere.

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References

  • Allen, E. K., and O. N. Allen: Biological aspects of symbiotic nitrogen fixation. In. Handbuch der Pflanzenphysiologie 8, 48–118 (1958). Berlin, Göttingen, Heidelberg: Springer.

    Google Scholar 

  • Allison, F. E.: Azotobacter inoculation of crops 1. Historical. Soil Sci. 64, 413–429 (1947).

    Google Scholar 

  • Beijerinck, M. W.: Die Bakterien der Papilionaceenknöllchen. Bot. Ztg. 46, 726–804 (1888).

    Google Scholar 

  • Belford, D. S., a. Myers, and R. D. Preston: Spatial and temporal variation of microfibrillar organisation in plant cell walls. Nature (Lond.) 181, 1251–1253 (1958).

    Google Scholar 

  • —, and R. D. Preston: The structure and growth of root hairs. J. exp. Bot. 12, 157–168 (1961).

    Google Scholar 

  • Bewley, W. F., and H. B. Hutchinson: On the changes through which the nodule organism (Ps. radicicola) passes under cultural conditions. J. Agricult. Sci. 10, 144–162 (1920).

    Google Scholar 

  • Bhaduri, S. N.: The influence of the numbers of Rhizobium supplied on the subsequent nodulation of the legume host plant. Ann. Bot. (Lond.) N.S. 15, 209–217 (1951).

    Google Scholar 

  • Bissett, K. A., and C. M. F. Hale: The production of swarmers in Rhizobium spp. J. gen. Microbiol. 5, 592–595 (1951).

    PubMed  Google Scholar 

  • Burginn-Wolff, A.: Untersuchungen über die Infektion von Wurzeln durch Knöllchenbakterien. Ber. schweiz. bot. Ges. 59, 75–111 (1959).

    Google Scholar 

  • Cormack, R. G. H.: Development of root hairs in angiosperms. Bot. Rev. 28, 446–464 (1962).

    Google Scholar 

  • Cullinmore, D. R., and M. Woodbine: A rhizosphere effect of the pea root on soil algae. Nature (Lond.) 198, 304–305 (1963).

    Google Scholar 

  • Dart, P. J., and F. V. Mercer: Development of the bacteroid in the root nodule of barrel medic (Medicago tribuloides Desr.) and subterraneum clover (Trifolium subterraneum L.). Arch. Mikrobiol. 46, 382–401 (1963).

    Google Scholar 

  • —, and J. S. Pate: Nodulation studies in legumes. III Aust. J. biol. Sci. 12, 427–444 (1959).

    Google Scholar 

  • Dart, P. J., J. S. Pate, and R. B. Donnelly: unpublished observations.

  • Dawes, C. J., and E. Bowler: Light and electron microscope studies of the cell wall structure of the root hairs of Raphanus sativus. Amer. J. Bot. 46, 561–565 (1959).

    Google Scholar 

  • Doudoroff, M., and R. Y. Stanier: Role of Poly-ß-hydroxybutyric acid in the assimilation of organic carbon by bacteria. Nature (Lond.) 183, 1440–1442 (1959).

    Google Scholar 

  • Fåhreus, G.: The infection of clover root hairs by nodule bacteria, studied by a simple glass slide technique. J. gen. Microbiol. 16, 374–381 (1957).

    PubMed  Google Scholar 

  • Fred, E. B., I. L. Baldwin, and E. McCoy: Root nodule bacteria and leguminous plants. Univ. Wisconsin Studies in Sci. 5, Madison, Wisc. (1932).

  • Frey-Wyssling, A.: Growth of plant cell walls. Symp. Soc. exp. Biol. 6, 320–328 (1952).

    Google Scholar 

  • —, and K. Muhlethaler: Über den Feinbau der Zellwand von Wurzelhaaren. Mikroskopie 4, 257–266 (1949).

    Google Scholar 

  • Hely, F. W., F. J. Bergersen, and J. Brockwell: Microbial antagonism in the rhizosphere as a factor in the failure of inoculation of subterraneum clover. Aust. J. biol. Sci. 8, 24–44 (1957).

    Google Scholar 

  • Houwink, A. L.: A macromolecular mono-layer in the cell wall of Spirillum spec. Biochim. biophys. Acta (Amst.) 10, 360–366 (1953).

    Article  Google Scholar 

  • —, and W. van Iterson: Electron microscopical observation on bacterial cytology. II. A study on flagellation. Biochim. biophys. Acta (Amst.) 5, 10–44 (1950).

    Article  Google Scholar 

  • —, and P. A. Roelofsen: Fibrillar architecture of growing plant cell walls. Acta Bot. Neérl. 3, 385–395 (1954).

    Google Scholar 

  • Jenny, H., and K. Grossenbacher: Root soil boundaries as seen in the electron microscope. Soil. Sci. Soc. Amer. Proc. 27, 273–277 (1963).

    Google Scholar 

  • Jensen, H. L.: Nitrogen fixation and cellulose decomposition by soil microorganisms. 1. Proc. Linn. Soc. N.S.W. 65, 543–546 (1940).

    Google Scholar 

  • —: Bacterial treatment of non-leguminous seeds as an agricultural practice. Aust. J. Sci. 4, 117–120 (1942).

    Google Scholar 

  • Katzelson, H., J. W. Rouatt, and T. N. B. Payne: The liberation of amino acids and reducing compounds by plant roots. Plant and Soil 7, 35–48 (1955).

    Google Scholar 

  • Kawamatu, S.: Electron microscope observations on the root hair cell of Azolla imbricata Nakai. Cytologia 28, 12–20 (1963).

    Google Scholar 

  • Kefford, N. P., J. Brockwell, and J. A. Zwar: The symbiotic synthesis of auxin by legumes and nodule bacteria and its role in nodule development. Aust. J. biol. Sci. 13, 456–467 (1960).

    Google Scholar 

  • Krasilnikov, N. A.: Soil microorganisms and higher plants. Acad. Sci. U.S.S.R. Moscow. English edition — National Science Foundation (1959).

  • Kuprevich, V. F.: Extracellular enzymes of roots of higher plants. Report Acad. Sci. U.S.S.R. 18, 953–956 (1949) — quoted in Krasilnikov, N. A.: Soil microorganisms and higher plants, p. 276

    Google Scholar 

  • Leifson, E., and L. W. Erdman: Flagellar characteristics of Rhizobium species. Antonie van Leeuwenhoek J. Microbiol. Serol. 24, 97–110 (1958).

    Google Scholar 

  • —, and I. Palen: Variations and spontaneous mutations in the genus Listeria in respect to flagellation and motility. J. Bact. 70, 233–240 (1955).

    PubMed  Google Scholar 

  • Ljunggren, H., and G. Fåhreus: Effect of Rhizobium polysaccharide on the formation of polygalacturonase in lucerne and clover. Nature (Lond.) 184, 1578–1579 (1959).

    Google Scholar 

  • ——: The role of polygalacturonase in root-hair invasion by nodule bacteria. J. gen. Microbiol. 26, 521–528 (1961).

    PubMed  Google Scholar 

  • Lundegardh, H., and G. Stenlid: On the exudation of nucleotides and flavanone from living roots. Ark. Bot. (Stockh.) 31A, 1–27 (1944).

    Google Scholar 

  • Mercer, E., and M. S. C. Birbeck: Electron microscopy. A handbook for biologists. Blackwell Scientific Publications. Oxford 1961.

    Google Scholar 

  • Mollenhauer, H. H., W. G. Whaley, and J. H. Leech: A function of the Golgi apparatus in outer root cap cells. J. Ultrastr. Res. 5, 193–200 (1961).

    Google Scholar 

  • ——: An observation on the functioning of the Golgi apparatus. J. Cell Biol. 17, 222–225 (1963).

    Article  PubMed  Google Scholar 

  • Murray, R. G. E.: On the cell wall structure of Spirillum serpens. Canad. J. Microbiol. 9, 381–392 (1963).

    Google Scholar 

  • —, and A. Birch-Andersen: Specialised structure in the region of the flagella tuft Spirillum serpens. Canad. J. Microbiol. 9, 393–402 (1963).

    Google Scholar 

  • Nutman, P. S.: Some observations on root-hair infection by nodule bacteria. J. exp Bot. 10, 250–263 (1959).

    Google Scholar 

  • —: The relation between root hair infection by Rhizobium and nodulation in Trifolium and Vicia. Proc. roy. Soc. B 156, 122–137 (1962).

    Google Scholar 

  • Nutman, P. S.: Factors influencing the balance of mutual advantage in legume symbiosis. In Symp. Soc. gen. Microbiol. 13, 51–71 (1963).

  • Purchase, H. F.: Restriction of infection threads in nodulation of clover and lucerne. Aust. J. biol. Sci. 11, 155–161 (1958).

    Google Scholar 

  • —, and P. S. Nutman: Studies on the physiology of nodule formation. IV. The influence of bacterial numbers in the rhizosphere on nodule initiation. Ann. Bot. (Lond.). N.S. 21, 439–454 (1957).

    Google Scholar 

  • Roberts, E. A.: The epidermal cells of roots. Bot. Gaz. 62, 488–506 (1916).

    Article  Google Scholar 

  • Roelofsen, P. A.: The plant cell-wall. Encyclopedia of Plant. Anatomy 3, (4). Berlin-Nikolassee: Gebrüder Borntraeger 1959.

    Google Scholar 

  • Rovira, A. D.: Plant root excretions in relation to the rhizosphere effect. 1. The nature of root exudate from oats and peas. Plant and Soil 7, 178–194 (1956).

    Google Scholar 

  • —: Root excretions in relation to the rihzosphere effect. IV. Influence of plant species, age of plant, light, temperature, and calcium nutrition on exudation. Plant and Soil 11, 53–64 (1959).

    Google Scholar 

  • —: Plant root exudates in relation to the rhizosphere microflora. Soils and Fertilisers 25, 167–172 (1962).

    Google Scholar 

  • —, and J. R. Harris: Plant root excretions in relation to the rhizosphere effect. V. Exudation of B-group vitamins. Plant and Soil 14, 199–214 (1961).

    Google Scholar 

  • Salton, M. R. J., and R. C. Williams: Electron microscopy of the cell walls of Bacillus megaterium and Rhodospirillum rubrum. Biochim. biophys. Acta. (Amst.) 14, 455–458 (1954).

    Article  Google Scholar 

  • Schaede, R.: Die Knöllchen der adventiven Wasserwurzeln von Neotunia oleracea und ihre Bakteriensymbiose. Planta (Berl.) 31, 1–21 (1940).

    Google Scholar 

  • Schlegel, H. G., u. G. Gottschalk: Poly-ß-hydroxybuttersäure, ihre Verbreitung, Funktion und Biosynthese. Angew. Chem. 74, 342 (1962).

    Google Scholar 

  • Schroth, M. N., and W. C. Snyder: Effect of host exudates on chlamydospore germination of the bean root rot fungus, Fusarium solani F. phaseoli. Phytopathology 51, 389–393 (1961).

    Google Scholar 

  • Scott, F. M.: Internal suberisation of tissues. Bot. Gaz. 111, 378–394 (1950).

    Article  Google Scholar 

  • —: Root hair zone of soil-grown roots. Nature (Lond.) 199, 1009–1010 (1963).

    Google Scholar 

  • —, B. G. Bystrom, and E. Bowler: Root hairs, cuticle and pits. Science 140, 63–64 (1963).

    Google Scholar 

  • —, K. C. Hamner, E. Baker, and E. Bowler: Electron microscope studies of cell wall growth in the onion root. Amer. J. Bot. 43, 313–324 (1956).

    Google Scholar 

  • ————: Electron microscope studies of the epidermis of Allium cepa. Amer. J. Bot. 45, 449–461 (1958).

    Google Scholar 

  • Starr, M. P., and R. C. Williams: Helical fine structure of flagella of a motile diphtheroid. J. Bact. 63, 701–706 (1952).

    PubMed  Google Scholar 

  • Thornton, H. G., and N. Gangulee: The life cycle of the nodule organism Bacillus radicicola (Beij) in soil, its relation to infection of the host plant. Proc. Roy. Soc. B 99, 427–451 (1926).

    Google Scholar 

  • Vincent, J. M., B. Humphrey, and R. J. North: Some features of the fine structure and chemical composition of Rhizobium trifolii. J. gen. Microbiol. 29, 551–555 (1962).

    PubMed  Google Scholar 

  • Weibull, C.: Movement. In: The Bacteria, Vol. 1, p. 153–205, Ed. I. C. Gunsalus and R. Y. Stanier. London: Academic Press 1960.

    Google Scholar 

  • Williams, M. A., and G. B. Chapman: Electron microscopy of flagellation in species of Spirillum. J. Bact. 81, 195–203 (1961).

    PubMed  Google Scholar 

  • Wilson, P. W.: The biochemistry of symbiotic nitrogen fixation. Madison, Wis.: Univ. Wis. Press 1940.

    Google Scholar 

Download references

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Dart, P.J., Mercer, F.V. The legume Rhizosphere. Archiv. Mikrobiol. 47, 344–378 (1964). https://doi.org/10.1007/BF00406359

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