Abstract
Biological dinitrogen fixation by legume-rhizobia symbiosis is very important both from the economic and from the ecological point of view. Theoretically, the reduction of the N2-molecule to ammonia requires at least 16 ATP and 1.5 mg C per mg N fixed (Nfix). These values are difficult to determine in situ as this necessitates the determination of that part of root respiration which drives N2-fixation. New approaches to such determinations and the results obtained are described. The values vary, depending on the plant species studied, the developmental stage of the plants and the genetic variability of macro- (and micro-?) symbionts. The values range between 1.5 and 4 mg C/mg Nfix. In some species (e.g.Vicia faba L. cv. Fribo), the apparent CO2 assimilation is enhanced in order to meet this high energy need. In others (e.g.Pisum sativum L. cv. Grapis), root growth is restricted. Physiological criteria are discussed which allow an early diagnosis of the energetic efficiency of various combinations of macro-and microsymbionts as a basis for a selection in plant breeding.
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References
Allam, F., Vom Energieverbrauch der Knöllchenbakterien bei der Bindung des Luftstickstoffs. Z. Pfl-Ernähr. Düng. Bodenk.,Abt. A 20 (1931) 270–301.
Arp, D. J., Hydrogen cycling in symbiotic bacteria, in: Biological Nitrogen Fixation, pp. 432–460. Eds G. Stacey, R. H. Burris and H. J. Evans. Chapman and Hall, London-New York 1992.
Atkins, C. A., Efficiencies and inefficiencies in the legume/Rhizobium symbiosis — A review. Pl. Soil82 (1984) 273–284.
Atkins, C. A., Herridge, D. F., and Plate, J. S., The economy of carbon and nitrogen in nitrogen fixing annual legumes, in: Isotopes in Biological Dinitrogen Fixation, pp. 211–242. IAEA/Vienna 1978.
Bergersen, F. J., Biochemistry of symbiotic nitrogen fixation in legumes. A. Rev. Pl. Physiol.22 (1971) 121–140.
Betlenfalvay, G. I., Abu-Shakra, S. S., and Phillips, D. A., Interdependence of nitrogen nutrition and photosynthesis inPisum sativum L. I. Effect of combined nitrogen on symbiotic nitrogen fixation and photosynthesis. Pl. Physiol.62 (1978) 127–130.
Bethlenfalvay, G. I., and Phillips, D. A., Effect of light intensity on efficiency of carbon dioxide and nitrogen reduction inPisum sativum L. Pl. Physiol.60 (1977) 868–871.
Bond, G., Symbiosis of leguminous plants and nodule bateria. I. Observations on respiration and on the extent of utilization of host carbohydrates by the nodule bacteria. Ann. Bot.5 (1941) 313–337.
Bothe, H., Yates, M. G., and Cannon, F. C., Physiology, biochemistry and genetics of dinitrogen fixation, in: Encyclopedia of Plant Physiology, 15A, pp. 241–285. Springer Verlag, Berlin-Heidelberg-New York-Toronto 1983.
Burns, R. C., and Hardy, R. W. F., Nitrogen Fixation in Bacteria and Higher Plants, p. 189. Springer Verlag, Berlin-Heidelberg-New York-Toronto 1975.
Christiansen-Weniger, F., Der Energiebedarf der Stickstoffbindung durch die Knöllchenbakterien im Vergleich zu anderen Stickstoffbindungsmöglichkeiten und erste Versuche zur Ermittlung desselben. Zentbl. Bakt. 2 Abt.58 (1923) 41–66.
Daesch, G., and Mortenson, L. E., Sucrose catabolism in Clostridium pasteurianum and its relation to N2 fixation. J. Bact.96c (1967) 346–351.
De Visser, R., Brouwer, K. S., and Posthumus, F., Alternative Path Mediated ATP Synthesis in Roots ofPisum sativum upon Nitrogen Supply. Pl. Physiol.80 (1986) 295–300.
Dixon, R. O. D., Nitrogenase-hydrogenase interrelationships in rhizobia. Biochimie60 (1978) 233–236.
Evans, H. J., and Burris, R. H., Highlights in biological nitrogen fixation during the last 50 years, in: Biological Nitrogen Fixation, pp. 1–42. Eds G. Stacey, R. H. Burris and H. J. Evans, Chapman and Hall, London-New York 1992.
Hayas, B., Der Einfluß verschiedener Rhizobiumstämme auf die Luftstickstoffbindung einer syrischen und einer DDR-Erbsensorte (Pisum sativum L.). Diss. Uni. Halle-Wittenberg 1988.
Hill, S., The apparent ATP requirement for nitrogen fixation in growing Klebsiella pneumonia. J. gen. Microbiol.95 (1976) 297–312.
Imam, S., and Eady, R. R., Nitrogenase of Klebsiella pneumoniae: reductant-independent ATP hydrolysis and the effect of pH on the efficiency of coupling of ATP hydrolysis to substrate reduction. FEBS Lett.110 (1980) 35–38.
Knowles, R., Brouzes, R., and O'Toole, P., Kinetics of nitrogen fixation and acetylene reduction, and effects of oxygen and of acetylene on these processes, in a soil system. Bull. Ecol. Res. Comm. Stockh.17 (1973) 255–262.
Lambers, H., Cyanid-resistant respiration: a non-phosphorylating electron transport pathway acting as an energy overflow. Physiologia Pl.55 (1982) 478–485.
Mahon, J. D., Respiration and the energy requirement for nitrogen fixation in nodulated pea roots. Pl. Physiol.60 (1977) 812–821.
McCree, K. J., and Silsbury, J. H., Growth and maintenance requirements of subterraneum clover. Crop Sci.18 (1978) 13–18.
Merbach, W., Untersuchungen über Stickstoffumsatz und symbiontische N2-Fixerung bei Körnerleguminosen. Diss. B. Uni. Halle-Wittenberg 1982.
Minchin, F. R., and Pate, J. S., The carbon balance of a legume and the functional economy of its root nodules. J. expl Bot.24 (1973) 259–271.
Müntz, K., Symbiotic nitrogen fixation of legumes: discovered 100 years ago — what do we know at present? Biol. Zentbl.106 (1987) 547–567.
Nelson, L. M., and Salminen, O. S., Uptake hydrogenase activity and ATP formation in Rhizobium leguminosarum bacteroids. J. Bact.151 (1985) 989–995.
Pate, J. S., and Herridge, D. F., Partitioning and utilization of net photosynthate in a nodulated annual legume. J. expl Bot.29 (1978) 401–412.
Phillips, D. A., Efficiency of symbiotic nitrogen fixation in legumes. A. Rev. Pl. Physiol.31 (1980) 29–49.
Schilling, G., Genetic specificity of nitrogen nutrition in leguminous plants. Pl. Soil72 (1983) 321–334.
Schulze, J., Untersuchungen zur Kohlenstoffbilanz bei Leguminosen und Nichtleguminosen unter besonderer Berücksichtigung der organischen Wurzelausscheidungen. Diss. Uni. Halle-Wittenberg 1993.
Truelsen, T. A. R., and Wyndaele, R., Recycling efficiency in hydrogenase uptake positive strains of Rhizobium leguminosarum. Physiologia Pl.62 (1984) 45–50.
Vance, C. P., and Heichel, G. H., Carbon in N2-fixation: limitation or exquisite adaptation. A. Rev. Pl. Physiol. Pl. Molec. Biol.42 (1991) 373–392.
Warembourg, F. R., Montagne, D., and Bardin, R., The simultaneous use of14CO2 and15N2 labelling techniques to study the carbon and nitrogen economy of legumes grown under natural conditions. Physiologia Pl.56 (1982) 46–55.
Warembourg, F. R., and Roumet, C., Why and how to estimate the cost of symbiotic N2-fixation? A progressive approach based on the use of14C and15N isotopes. Pl. Soil115 (1989) 167–177.
Watt, G. D., Bulen, W. A., Burns, A., and Hadfield, K. L., Stoichiometry ATP/2 e− values, and energy requirements for reaction catalysis by nitrogenase from Azotobacter vinelandii. Biochemistry14 (1975) 4266–4272.
Yates, M. G., The enzymology of molybdenum-dependent nitrogen fixation, in: Biological Nitrogen Fixation, pp. 685–735. Eds G. Stacey, R. H. Burris and H. J. Evans. Chapman and Hall, London-New York 1992.
Zumft, W. G., The biochemistry of dinitrogen fixation, in: Biology of Inorganic Nitrogen and Sulfur, pp. 116–135. Eds H. Bothe and A. Trebst. Springer Verlag, Berlin-Heidelberg-New York 1981.
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Schulze, J., Adgo, E. & Schilling, G. The influence of N2-fixation on the carbon balance of leguminous plants. Experientia 50, 906–912 (1994). https://doi.org/10.1007/BF01923477
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DOI: https://doi.org/10.1007/BF01923477