Plant Biol (Stuttg) 2005; 7(2): 176-181
DOI: 10.1055/s-2005-837541
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Redundancy of Stomatal Control for the Circadian Photosynthetic Rhythm in Kalanchoë daigremontiana Hamet et Perrier

T. P. Wyka1 , H. M. Duarte2 , U. E. Lüttge2
  • 1Biology Department, General Botany Laboratory, Adam Mickiewicz University, ul. Umultowska 89, 61-614 Poland
  • 2Institut für Botanik, Fachbereich Biologie, Technische Universität-Darmstadt, Schnittspahnstraße 3 - 5, 64287 Darmstadt, Germany
Further Information

Publication History

Received: August 23, 2004

Accepted: January 12, 2005

Publication Date:
11 April 2005 (online)


In continuous light, the Crassulacean acid metabolism plant Kalanchoë daigremontiana Hamet et Perrier has a circadian rhythm of gas exchange with peaks occurring during the subjective night. The rhythm of gas exchange is coupled to a weak, reverse phased rhythm of quantum yield of photosystem II (ΦPSII). To test if the rhythm of ΦPSII persists in the absence of stomatal control, leaves were coated with a thin layer of translucent silicone grease which prevented CO2 and H2O exchange. In spite of this treatment, the rhythm of ΦPSII occurred with close to normal phase timing and with a much larger amplitude than in uncoated leaves. The mechanism underlying the ΦPSII rhythm in coated leaves can be explained by a circadian activity of phosphoenolpyruvate carboxylase (PEPC). At peaks of PEPC activity, the small amount of CO2 contained in the coated leaf could have become depleted, preventing the carboxylase activity of Rubisco and causing decreases in electron transport rates (observed as deep troughs of ΦPSII at 23-h in LL and at ca. 24-h intervals afterwards). Peaks of ΦPSII would be caused by a downregulation of PEPC leading to improved supply of CO2 to Rubisco. Substrate limitation of photochemistry at 23 h (trough of ΦPSII) was also suggested by the weak response of ETR in coated leaves to stepwise light enhancement. These results show that photosynthetic rhythmicity in K. daigremontiana is independent of stomatal regulation and may originate in the mesophyll.


  • 1 Bohn A., Hinderlich S., Hütt M. T., Kaiser F., Lüttge U.. Identification of rhythmic subsystems in the circadian cycle of Crassulacean acid metabolism under thermoperiodic perturbations.  Biological Chemistry. (2003);  384 721-728
  • 2 Booji-James I. S., Swegle M. W., Edelman M., Mattoo A. K.. Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm.  Plant Physiology. (2002);  130 2069-2075
  • 3 Buchannan-Bollig I. C., Smith J. A. C.. Circadian rhythms in crassulacean acid metabolism: phase relationships between gas exchange, leaf water relations and malate metabolism in Kalanchoë daigremontiana. .  Planta. (1984);  161 264-271
  • 4 Duarte H. M., Jakovljevic I., Kaiser F., Lüttge U.. Lateral diffusion of CO2 in leaves of the crassulacean acid metabolism plant Kalanchoë daigremontiana Hamet et Perrier.  Planta. (2004);  in press
  • 5 Edwards G. E., Dai Z., Cheng S. H., Ku M. S. B.. Factors affecting the induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum. . Winter, K. and Smith, J. A. C., eds. Crassulacean Acid Metabolism. Berlin, Heidelberg; Springer Verlag (1996): 119-134
  • 6 Genty B., Briantais J. M., Baker N. M.. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.  Biochimica et Biophysica Acta. (1989);  990 320-324
  • 7 Gorton H. L., Williams W. E., Binns M. E., Gemmel C. N., Leheny E. A., Shepherd A. C.. Circadian stomatal rhythms in epidermal peels from Vicia faba. .  Plant Physiology. (1989);  90 1329-1334
  • 8 Hennesey T. L., Field C. B.. Circadian rhythms in photosynthesis. Oscillations in carbon assimilation and stomatal conductance under constant conditions.  Plant Physiology. (1991);  96 831-836
  • 9 Hütt Th., Lüttge U.. Nonlinear dynamics as a tool for modeling in plant physiology.  Plant Biology. (2002);  4 281-297
  • 10 Kluge M., Fischer K.. Über Zusammenhänge zwischen dem CO2-Austauch und der Abgabe von Wasserdampf durch Bryophyllum daigremontianum Berg.  Planta. (1967);  77 212-223
  • 11 Kondo A., Kaikawa J., Funaguma T., Ueno O.. Clumping and dispersal of chloroplasts in succulent plants.  Planta. (2004);  219 500-506
  • 12 Kreps J. A., Kay S. A.. Coordination of plant metabolism and development by the circadian clock.  Plant Cell. (1997);  9 1235-1244
  • 13 Lüttge U.. Circadian rhythmicity: is the biological clock hardware or software?.  Progress in Botany. (2002);  64 277-319
  • 14 Lüttge U., Beck F.. Endogenous rhythms and chaos in crassulacean acid metabolism.  Planta. (1992);  188 28-38
  • 15 Martin C. E.. Putative causes and consequences of recycling CO2 via Crassulacean acid metabolism. Winter, K. and Smith, J. A. C., eds. Crassulacean Acid Metabolism. Berlin, Heidelberg; Springer Verlag (1996): 192-203
  • 16 Mawson B. T., Zaugg M. W.. Modulation of light-dependent stomatal opening in isolated epidermis following induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum L.  Plant Physiology. (1994);  144 240-246
  • 17 McClung C. R.. Circadian rhythms in plants: a millenial view.  Physiologia Plantarum. (2000);  109 359-371
  • 18 Möllering H.. L-Malate. Bestimmung mit Malat-Dehydrogenase und Glutamat-Oxalacetat-Transaminase. Bergmeyer, H. W., ed. Methoden der enzymatischen Analyse, Vol. 25. Weinheim; Verlag Chemie (1974): 1636-1639
  • 19 Nimmo G. A., Wilkins M. B., Fewson C. A., Nimmo H. G.. Persistent circadian rhythms in the phosphorylation carboxylase from Bryophyllum fedtschenkoi leaves and its sensitivity to inhibition by malate.  Planta. (1987);  170 408-415
  • 20 Nimmo H. G.. The regulation of phosphoenolpyruvate carboxylase in CAM plants.  Trends in Plant Science. (2000);  5 75-80
  • 21 Rascher U., Liebig M., Lüttge U.. Evaluation of instant light-response curves of chlorophyll fluoresence parameters obtained with a portable chlorophyll fluorometer on site in the field.  Plant, Cell and Environment. (2000);  23 1397-1405
  • 22 Rascher U., Hütt Th., Siebke K., Osmond B., Lüttge U.. Spatio-temporal variations of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 11801-11805
  • 23 Ritz D., Kluge M.. Circadian rhythmicity of CAM in continuous light: coincidences between gas exchange parameters, 14CO2 fixation patterns and PEP-carboxylase properties.  Journal of Plant Physiology. (1987);  131 285-296
  • 24 Ting I. P.. Crassulacean acid metabolism.  Annual Review in Plant Physiology. (1985);  36 595-622
  • 25 Wilkins M. B.. Circadian rhythms: their origin and control.  New Phytologist. (1992);  121 347-375
  • 26 Winter K.. Gradient in the degree of Crassulacean acid metabolism within leaves of Kalanchoë daigremontiana. .  Planta. (1987);  172 88-90
  • 27 Wyka T. P., Lüttge U. E.. Contribution of C3 carboxylation to the circadian rhythm of carbon dioxide uptake in a Crassulacean acid metabolism plant Kalanchoë daigremontiana. .  Journal of Experimental Botany. (2003);  54 1471-1479
  • 28 Wyka T. P., Bohn A., Duarte H. M., Kaiser F., Lüttge U.. Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalanchoë daigremontiana: testing the tonoplast as oscillator model.  Planta. (2004);  219 705-713

T. Wyka

Biology Department, General Botany Laboratory
Adam Mickiewicz University

ul. Umultowska 89

61-614 Poznań



Editor: R. Monson