, Volume 198, Issue 1, pp 110–117 | Cite as

Generation of rhythmic and arrhythmic behaviour of Crassulacean acid metabolism in Kalanchoë daigremontiana under continuous light by varying the irradiance or temperature: Measurements in vivo and model simulations

  • Thorsten E. E. Grams
  • Friedrich Beck
  • Ulrich LüttgeEmail author


Leaves of Kalanchoë daigremontiana Hamet et Perr. at a photon flux density (PFD) above 220 μmol·m−2s−1 (400–700 nm) or at leaf temperatures above 27.0 °C showed a rapid loss of rhythmicity, and a more or less pronounced damping-out of the endogenous circadian rhythm of CO2 exchange under continuous illumination. This rhythm was reinitiated after reduction of the PFD by 90–120 μmol·m−2·s−1 or reduction of leaf temperature by 3.5–11.0 °C under otherwise unchanged external conditions. The reduction in the magnitude of the external control parameter of the Crassulacean acid metabolism (CAM) rhythm (i.e. PFD or leaf temperature) set the phase of the new rhythm. The maxima of CO2 uptake occurred about 5, 28, 51, 75 h after the reduction. Simulations with a CAM model under comparable conditions showed a similar behaviour. The influence of temperature on the endogenous CAM rhythm observed in K. daigremontiana in vivo could be simulated by incorporating into the model temperature-dependent switch modes for passive efflux of malate from the vacuole to the cytoplasm. Thus, the model indicates that tonoplast function plays an important role in regulation of the endogenous CAM rhythm in K. daigremontiana.

Key words

Circadian rhythm Crassulacean acid metabolism Kalanchoe Model simulations Phase setting Tonoplast 



Crassulacean acid metabolism


photosynthetically active radiation


photon flux density


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  1. Anderson CM, Wilkins MB (1989a) Period and phase control by temperature in the circadian rhythm of carbon dioxide fixation in illuminated leaves of Bryophyllum fedtschenkoi. Planta 177: 456–469Google Scholar
  2. Anderson CM, Wilkins MB (1989b) Phase resetting of the circadian rhythm of carbon dioxide assimilation in Bryophyllum leaves in relation to their malate content following brief exposure to high and low temperatures, darkness and 5% carbon dioxide. Planta 180: 61–73Google Scholar
  3. Buchanan-Bollig IC (1984) Circadian rhythms in Kalanchoë: effects of the irradiance and temperature on gas exchange and carbon metabolism. Planta 160: 264–271Google Scholar
  4. Buchanan-Bollig IC, Smith JAC (1984) Circadian rhythms in Crassulacean acid metabolism: phase relationships between gas exchange, leaf water relations and malate metabolism in Kalanchoë daigremontiana. Planta 161: 314–319Google Scholar
  5. Carter PJ, Nimmo HG, Fewson CA, Wilkins MB (1991) Circadian rhythms in the activity of a plant protein kinase. EMBO J 10: 2063–2068Google Scholar
  6. Friemert V, Heininger D, Kluge M, Ziegler H (1988) Temperature effects on malic-acid efflux from the vacuoles and on the carboxylation pathways in Crassulacean acid metabolism plants. Planta 174: 453–461Google Scholar
  7. Hohorst HJ (1970) L-(-)-Malat. Bestimmung mit Malatdehydrogenase und NAD. In: Bergmeyer HU (ed) Methoden der enzymatischen Analyse. Verlag Chemie, Weinheim, pp. 1544–1548Google Scholar
  8. Iwasaki I, Arata H, Kijima H, Nishimura M (1992) Two types of channels involved in the malate ion transport across the tonoplast of a Crassulacean acid metabolism plant. Plant Physiol 98: 1494–1497Google Scholar
  9. Kliemchen A, Schomburg M, Galla H-J, Lüttge U, Kluge M (1993) Phenotypic changes in the fluidity of the tonoplast membrane of crassulacean-acid-metabolism plants in response to temperature and salinity stress. Planta 189: 403–409Google Scholar
  10. Kluge M, Ting IP (1978) Crassulacean acid metabolism: analysis of an ecological adaptation. Springer, Berlin Heidelberg New YorkGoogle Scholar
  11. Kluge M, Kliemchen A, Galla H-J (1991) Temperature effects on Crassulacean acid metabolism: EPR spectroscopic studies on the thermotropic phase behaviour of the tonoplast membranes of Kalanchoë daigremontiana. Bot Acta 104: 355–360Google Scholar
  12. Kusumi K, Arata H, Iwasaki I, Nishimura M (1994) Regulation of PEP-carboxylase by biological clock in a CAM plant. Plant Cell Physiol 35: 233–242Google Scholar
  13. Lange OL, Beyschlag W, Meyer A, Tenhunen JD (1984) Determination of photosynthetic capacity of lichens in the field —a method for measurements of light response curves at saturating CO2 concentration. Flora 175: 283–293Google Scholar
  14. Lüttge U (1987) Carbon dioxide and water demand: Crassulacean acid metabolism (CAM), a versatile ecological adaptation exemplifying the need for integration in ecophysiological work. New Phytol 106: 593–626Google Scholar
  15. Lüttge U, Ball E (1978) Free running oscillations of transpiration and CO2 exchange in CAM plants without a concomitant rhythm of malate levels. Z Pflanzenphysiol 90: 96–77Google Scholar
  16. Lüttge U, Beck F (1992) Endogenous rhythms and chaos in crassulacean acid metabolism. Planta 188: 28–38Google Scholar
  17. Lüttge U, Smith JAC (1984) Mechanism of passive malic-acid efflux from the vacuole of the CAM plant Kalanchoë daigremontiana. J Membr Biol 81: 149–158Google Scholar
  18. Lüttge U, Stimmel K-H, Smith JAC, Griffiths H (1986) Comparative ecophysiology of CAM and C3 bromeliads. II. Field measurements of gas exchange of bromeliads in the humid tropics. Plant Cell Environ 9: 377–383Google Scholar
  19. Nimmo GA, Wilkins MB, Fewson CA, Nimmo HG (1987) Persistent circadian rhythm in the phosphorylation state of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi leaves and its sensitivity to inhibition by malate. Planta 170: 408–415Google Scholar
  20. Nuernbergk EL (1961) Endogener Rhythmus und CO2-Stoffwechsel bei Pflanzen mit diurnalem Säurerhythmus. Planta 56: 28–70Google Scholar
  21. Nungesser D, Kluge M, Tolle H, Oppelt W (1984) A dynamic computer model of the metabolic and regulatory processes in Crassulacean acid metabolism. Planta 162: 204–214Google Scholar
  22. Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29: 379–414Google Scholar
  23. Ratajczak R, Kemna I, Lüttge U (1994) Characteristics, partial purification and reconstitution of the vacuolar malate transporter of the CAM plant Kalanchoë daigremontiana Hamet et Perrier de la Bâthie. Planta 195: 226–236Google Scholar
  24. Wilkins MB (1959) An endogenous rhythm in the rate of carbon dioxide output of Bryophyllum I. Some preliminary experiments. J Exp Bot 10: 377–390Google Scholar
  25. Wilkins MB (1960) An endogenous rhythm in the rate of carbon dioxide output of Bryophyllum II. The effects of light and darkness on the phase and period of the rhythm. J Exp Bot 11: 269–288Google Scholar
  26. Wilkins MB (1962) An endogenous rhythm in the rate of carbon dioxide output of Bryophyllum III. The effects of temperature changes on the phase and period of the rhythm. Proc R Soc London B 156: 220–241Google Scholar
  27. Wilkins MB (1983) The circadian rhythm of carbon-dioxide metabolism in Bryophyllum: the mechanism of phase-shift induction by thermal stimuli. Planta 157: 471–480Google Scholar
  28. Wilkins MB (1984) A rapid circadian rhythm of carbon dioxide metabolism in Bryophyllum fedtschenkoi. Planta 161: 381–384Google Scholar
  29. Wilkins MB, Thomas SL (1993) The damping and reinitiation of the circadian rhythm of CO2 output in Bryophyllum leaves in relation to their malate content. J Exp Bot 44: 901–906Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Thorsten E. E. Grams
    • 1
  • Friedrich Beck
    • 2
  • Ulrich Lüttge
    • 1
    Email author
  1. 1.Institut für BotanikTechnische Hochschule DarmstadtDarmstadtGermany
  2. 2.Institut für KernphysikTechnische Hochschule DarmstadtDarmstadtGermany

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