, Volume 182, Issue 4, pp 617–625 | Cite as

Respiratory capacity, nitrogenase activity and structural changes ofFrankia, in symbiosis withAlnus incana, in response to prolonged darkness

  • Per-Åke Vikman
  • Per-Olof Lundquist
  • Kerstin Huss-Danell


Plants ofAlnus incana (L.) Moench in symbiosis with a local source ofFrankia were exposed to prolonged darkness under controlled climate conditions.Frankia vesicle clusters were prepared from the root nodules, and the condition ofFrankia was measured as respiratory capacity by supplying the preparation with saturating amounts of four different substrates. During darkness, nitrogenase (EC activity decreased in intact plants and in the vesicle-cluster preparations. The respiratory capacity ofFrankia also decreased. After 4 d in darkness most respiration was lost, though all nitrogenase activity was already lost after 3 d. When the dark treatment was ended after 2 d and normal light/dark conditions restored, nitrogenase activity immediately started to recover. The respiratory capacity continued to decrease and no recovery was observed until the third day after the end of the dark treatment. Whole-plant nitrogenase activity slowly increased at a rate similar to the rate of increase observed in untreated plants. Transmission electron micrographs of the root nodules showed that the cytoplasm of infected host cells and the cells ofFrankia were structurally degraded in response to dark treatment, while young vesicles were frequent during recovery. Growth and differentiation ofFrankia cells were apparently important for recovery of the enzyme activities studied.

Key words

Alnus Darkness and nitrogenase activity Frankia Nitrogenase Respiration Root nodule structure 



acetylene-reduction activity


transmission electron microscopy


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  1. Boller, T., Wiemken, A. (1986) Dynamics of vacuolar compartmentation. Annu. Rev. Plant Physiol.37, 137–164CrossRefGoogle Scholar
  2. Cohen, H.P., Sarath, G., Lee, K., Wagner, F.W. (1986) Soybean root nodule ultrastructure during dark-induced stress and recovery. Protoplasma132, 69–75CrossRefGoogle Scholar
  3. Dixon, R.O.D., Wheeler, C.T. (1986) Nitrogen fixation in plants. Blackie, GlasgowGoogle Scholar
  4. Fontaine, M.S., Lancelle, S.A., Torrey, J.G. (1984) Initiation and ontogeny of vesicles in culturedFrankia strain HFPAr13. J. Bacteriol.160, 921–927PubMedGoogle Scholar
  5. Greitner, C.S., Winner, W.E. (1989) Effects of O3 on alder photosynthesis and symbiosis withFrankia. New Phytol.111, 647–656Google Scholar
  6. Hill, S. (1988) How is nitrogenase regulated by oxygen? FEMS Microbiol. Rev.54, 111–130Google Scholar
  7. Huss-Danell, K. (1978) Nitrogenase activity measurements in intact plants ofAlnus incana. Physiol. Plant.43, 372–376Google Scholar
  8. Huss-Danell, K., Bergman, B. (1990) Nitrogenase inFrankia ofAlnus incana root nodules: immunolocalization of the Fe- and MoFe-proteins during vesicle differentiation. New Phytol.116, in pressGoogle Scholar
  9. Huss-Danell, K., Hahlin, A-S. (1988) Nitrogenase activity decay and energy supply inFrankia after addition of ammonium to the host plantAlnus incana. Physiol. Plant.74, 745–751Google Scholar
  10. Huss-Danell, K., Sellstedt, A. (1983) Nitrogenase activity in response to restricted shoot growth inAlnus incana. Can. J. Bot.61, 2949–2955Google Scholar
  11. Huss-Danell, K., Sellstedt, A. (1985) Nitrogenase activity in response to darkening and defoliation ofAlnus incana. J. Exp. Bot.36, 1352–1358Google Scholar
  12. Huss-Danell, K., Sellstedt, A., Flower-Ellis, A., Sjöström, M. (1982) Ammonium effects on function and structure of nitrogen-fixing root nodules ofAlnus incana (L.) Moench. Planta 156, 332–340Google Scholar
  13. Huss-Danell, K., Winship, L.J., Hahlin, A.S. (1987) Loss and recovery of nitrogenase inAlnus incana nodules exposed to low oxygen and low temperature. Physiol. Plant.70, 355–360Google Scholar
  14. Lalonde, M., Knowles, R. (1975) Ultrastructure of theAlnus crispa var. mollis Fern. root nodule endohyte. Can. J. Microbiol.21, 1058–1080PubMedGoogle Scholar
  15. Newcomb, W., Wood, S.M. (1987) Morphogenesis and fine structure ofFrankia (Actinomycetales): The microsymbiont of nitrogen-fixing actinorhizal root nodules. Int. Rev. Cytol.109, 1–88PubMedGoogle Scholar
  16. Palade, G.E. (1952) A study of fixation for electron microscopy. J. Exp. Med.95, 285–298CrossRefPubMedGoogle Scholar
  17. Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol.17, 208–212CrossRefPubMedGoogle Scholar
  18. Roponen, I. (1970) The effect of darkness on the leghemoglobin content and amino acid levels in the root nodules of pea plants. Physiol. Plant.23, 452–460Google Scholar
  19. Sarath, G., Pfeiffer, N.E., Sodhi, C.S., Wagner, F.W. (1986) Bacteroids are stable during dark-induced senescence of soybean root nodules. Plant Physiol.82, 346–350Google Scholar
  20. Sellstedt, A., Huss-Danell, K. (1984) Growth, nitrogen fixation and relative efficiency of nitrogenase inAlnus incana grown in different cultivation systems. Plant Soil78, 147–158CrossRefGoogle Scholar
  21. Sellstedt, A., Huss-Danell, K., Ahlqvist, A-S. (1986) Nitrogen fixation and biomass production in symbioses betweenAlnus incana andFrankia strains with different hydrogen metabolism. Physiol. Plant.66, 99–107Google Scholar
  22. Sundström, K.R., Huss-Danell, K. (1987) Effects of water stress on nitrogenase activity inAlnus incana.Physiol. Plant.70, 342–348Google Scholar
  23. Vance, C.P., Johnson, L.E.B., Halvorsen, A.M., Heichel, G.H., Barnes, D.K. (1980) Histological and ultrastructural observations ofMedicago sativa root nodule senescence after foliage removal. Can. J. Bot.58, 295–309Google Scholar
  24. Vikman, P.-Å., Huss-Danell, K. (1987) Capacity for hexose respiration in symbioticFrankia fromAlnus incana. Physiol. Plant. 70, 349–354Google Scholar
  25. Wheeler, C.T. (1971) The causation of the diurnal changes in nitrogen fixation in the nodules ofAlnus glutinosa. New Phytol. 70, 487–495Google Scholar
  26. Wheeler, C.T., Bowes, B.G. (1974) Effects of light and darkness on nitrogen fixation by root nodules ofAlnus glutinosa in relation to their cytology. Z. Pflanzenphysiol.71, 71–75Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • Per-Åke Vikman
    • 1
  • Per-Olof Lundquist
    • 1
  • Kerstin Huss-Danell
    • 1
  1. 1.Department of Plant PhysiologyUniversity of UmeåUmeåSweden

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