Alternative Carbohydrate Reserves Used in the Daily Cycle of Crassulacean Acid Metabolism

  • C. C. Black
  • J.-Q. Chen
  • R. L. Doong
  • M. N. Angelov
  • S. J. S. Sung
Part of the Ecological Studies book series (ECOLSTUD, volume 114)


Each day a massive interlocked biochemical cycle occurs in the green tissues of crassulacean acid metabolism plants. The function of this interlocked cycle, in its simplest context, is to furnish most of the CO2 for CAM plant photosynthesis. In addition, this diel (24 h) cycle produces the primary identifying marks of a CAM tissue through two ancillary cycles. One cycle involves a nocturnal acidification and its loss the next day, while the second concerns the depletion of a carbohydrate reserve at night and its replenishment the next day. Formally Benjamin Heyne (1815) is credited with writing, nearly two centuries ago, about the “acid as sorrel” taste of a succulent green plant at dawn and the “bland taste” caused by acidity loss later in the day. In fact, the exact origins of these observations are lost in antiquity, but certainly are referred to in Roman and Biblical writings. The circumstantial cause of the acidity was postulated to be an organic acid about a century ago and the bland taste later was associated with starch; but these ideas were not plainly coupled together in theory nor quantitatively studied until the late 1940s. Then, with the discovery of major portions of intermediary metabolism and the advent of additional quantitative biochemical procedures, the nature of the daily reciprocal relation between the acid and the bland taste was recognized and measured quantitatively. The acid taste is caused principally by malic acid, while the bland taste is caused by deacidification plus the reciprocal synthesis of a bland tasting carbohydrate, e.g. a polysaccharide such as starch.


Malic Acid Daily Cycle Malic Enzyme Crassulacean Acid Metabolism Acid Invertase 
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  1. Ball E, Hann J, Kluge M, Lee HSJ, Lüttge U, Orthen B, Popp M, Schmitt A, Ting IP (1991) Ecophysiological comportment of the tropical CAM-tree Clusia in the field. II. Modes of photosynthesis in trees and seedlings. New Phytol 117: 483–491CrossRefGoogle Scholar
  2. Bennet-Clark TA (1933) The role of organic acids in plant metabolism. Part I, II and III. New Phytol 32:37–71, 128–161, 197–230CrossRefGoogle Scholar
  3. Black CC (1973) Photosynthetic carbon fixation in relation to net CO2 uptake. Annu Rev Plant Physiol 24: 253–286CrossRefGoogle Scholar
  4. Black CC (1976) Fractionation of stable carbon isotopes during crassulacean acid metabolism and the presentation of a unified concept of diurnal CO2 metabolism in CAM plants. In: Benedict CR (ed) The fractionation of stable carbon isotopes by plants. Southern Section American Society of Plant Physiologists, Rockville, pp 51–73Google Scholar
  5. Black CC, Carnal NW, Kenyon WH (1982) Compartmentation and the regulation of CAM. In: IP Ting, M Gibbs (eds) Crassulacean acid metabolism. American Society of Plant Physiologists, Rockville, pp 51–68Google Scholar
  6. Borland AM, Griffiths H (1989) The regulation of citric acid accumulation and carbon recycling during CAM in Ananas comosus. J Exp Bot 210: 53–60CrossRefGoogle Scholar
  7. Borland AM, Griffiths H (1992) Properties of phosphoenolpyruvate carboxylase and carbohydrate accumulation in the C3-CAM intermediate Sedum telephium L. grown under different light and watering regimes. J Exp Bot 43: 353–361CrossRefGoogle Scholar
  8. Brunnhöfer H, Schaub H, Egle K (1968) Die Beziehungen zwischen den Veränderungen der Malat- und Stärkekonzentrationen und dem CO2- und O2-Gaswechsel bei Bryophyllum daigremontianum. Z Pflanzenphysiol 60: 12–18Google Scholar
  9. Carnal NW, Black CC (1983) Phosphofructokinase activities in photosynthetic organisms: the occurrence of pyrophosphate dependent 6-phosphofructokinase in plants and algae. Plant Physiol 71: 150–155PubMedCrossRefGoogle Scholar
  10. Carnal NW, Black CC (1989) Soluble sugars as the carbohydrate reserve for CAM in pineapple leaves. Implications for the role of pyrophosphate: 6-phosphofructokinase in glycolysis. Plant Physiol 90: 91–100PubMedCrossRefGoogle Scholar
  11. Chang NK, Vines HM, Black CC (1981) Nitrate assimilation and crassulacean acid metabolism in leaves of Kalanchoe fedtschenkoi variety marginata. Plant Physiol 68: 464–468PubMedCrossRefGoogle Scholar
  12. Chen JQ (1992) Biochemical properties and physiological roles of plant invertases. PhD Dissertation, University of Georgia, Athens, pp 258Google Scholar
  13. Chen JQ, Black CC (1992) Biochemical and immunological properties of alkaline invertase isolated from sprouting soybean hypocotyls. Arch Biochem Biophys 295: 61–69PubMedCrossRefGoogle Scholar
  14. Crews CE, William SL, Vines HM, Black CC (1976) Changes in the metabolism and physiology of crassulacean acid metabolism plants grown in controlled environments. In: Burris RH, Black CC (eds) CO2 Metabolism and plant productivity. University Park Press, Baltimore, pp 235–250Google Scholar
  15. Dittrich P (1976) Nicotinamide adenine dinucleotide-specific “malic” enzyme in Kalanchoë daigremontiana and other plants exhibiting crassulacean acid metabolism. Plant Physiol 57: 310–314PubMedCrossRefGoogle Scholar
  16. Dittrich P, Campbell WH, Black CC (1973) Phosphoenolpyruvate carboxykinase in plants exhibiting crassulacean acid metabolism. Plant Physiol 52: 357–361PubMedCrossRefGoogle Scholar
  17. Edwards G, Walker D (1983) C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis. Blackwell, OxfordGoogle Scholar
  18. Franco AC, Ball E, Lüttge U (1991) The influence of nitrogen, light and water stress on CO2 exchange and organic acid accumulation in the tropical C3-CAM tree, Clusia minor. J Exp Bot 42: 597–603CrossRefGoogle Scholar
  19. Griffiths H, Ong BL, Avadhani PN, Goh CJ (1989) Recycling of respiratory CO2 during crassulacean acid metabolism: alleviation of photoinhibition in Pyrrosia piloselloides. Planta 179: 115–122CrossRefGoogle Scholar
  20. Haag-Kerwer A, Franco AC, Lüttge U (1992) The effect of temperature and light on gas exchange and acid accumulation in the C3-CAM plant Clusia minor L. J Exp Bot 43:345–352CrossRefGoogle Scholar
  21. Heyne B (1815) On the deoxidation of the leaves of Cotyledon calycina. Trans Linn Soc Lond 213: 815–816Google Scholar
  22. Holtum JAM, Osmond CB (1981) The gluconeogenic metabolism of pyruvate during deacidification in plants with crassulacean acid metabolism. Aust J Plant Physiol 8: 31–44CrossRefGoogle Scholar
  23. Kenyon WH, Holaday AS, Black CC (1981) Diurnal changes in metabolite levels and crassulacean acid metabolism in Kalanchoë daigremontiana leaves. Plant Physiol 68: 1002–1007PubMedCrossRefGoogle Scholar
  24. Kenyon WH, Severson RF, Black CC (1985) Maintenance carbon cycle in crassulacean acid metabolism plant leaves. Plant Physiol 77: 183–189PubMedCrossRefGoogle Scholar
  25. Kluge M, Osmond CB (1971) Pyruvate, Pi dikinase in crassulacean acid metabolism. Naturwissenschaften 58: 414–415CrossRefGoogle Scholar
  26. Kluge M, Ting IP (1978) Crassulacean acid metabolism: analysis of an ecological adaptation. Springer, Berlin Heidelberg New YorkCrossRefGoogle Scholar
  27. Lüttge U, Smith JAC, Marigo G, Osmond CB (1981) Energetics of malate accumulation in the vacuoles of Kalanchoë tubiflora cells. FEBS Lett 126: 81–84CrossRefGoogle Scholar
  28. Master RWP (1959) Organic acid and carbohydrate metabolism in Nopalea cochinellifera. Experientia 15: 30–31PubMedCrossRefGoogle Scholar
  29. Medina E, Olivares E, Diaz M (1986) Water stress and light intensity effects on growth and nocturnal acid accumulation in a terrestrial CAM bromeliad (Bromelia humilis Jacq.) under natural conditions. Oecologia 70: 441–446CrossRefGoogle Scholar
  30. Paul MJ, Loos K, Stitt M, Ziegler P (1993) Starch-degrading enzymes during the induction of CAM in Mesembryanthemum crystallinum. Plant Cell Environ 16: 531–538CrossRefGoogle Scholar
  31. Popp M, Kramer D, Lee H, Diaz M, Ziegler H, Lüttge U (1987) Crassulacean acid metabolism in tropical dicotyledonous trees of the genus Clusia. Trees 1: 238–247CrossRefGoogle Scholar
  32. Pucher GW, Vickery HB, Abrahams MD, Leavenworth CS (1949) Studies on the metabolism of crassulacean plants: diurnal variation of organic acids and starch in excised leaves of Bryophyllum calycinum. Plant Physiol 25: 610–620CrossRefGoogle Scholar
  33. Sideris CP, Young HY, Chun HHQ (1948) Diurnal changes and growth rates as associated with ascorbic acid, titratable acidity, carbohydrate and nitrogenous fractions in the leaves of Ananas comosus (L.) Merr. Plant Physiol 23: 38–69PubMedCrossRefGoogle Scholar
  34. Sugiyama T, Laetsch WM (1975) Occurrence of pyruvate orthophosphate dikinase in the succulent plant, Kalanchoë daigremontiana Hamet et Perr. Plant Physiol 56: 605–607PubMedCrossRefGoogle Scholar
  35. Sung SJS, Xu DP, Galloway CM, Black CC (1988) A reassessment of glycolysis and gluconeogenesis in higher plants. Physiol Plant 72: 650–654CrossRefGoogle Scholar
  36. Sutton BG (1975a) The path of carbon in CAM plants at night. Aust J Plant Physiol 2: 377–387Google Scholar
  37. Sutton BG (1975b) Glycolysis in CAM plants. Aust J Plant Physiol 2: 389–402CrossRefGoogle Scholar
  38. Thomas M (1947) Plant Physiology, 3rd edn. J & A Churchill, LondonGoogle Scholar
  39. Thomas M (1949) Physiological studies on acid metabolism in green plants. I. CO2 fixation and CO2 liberation in crassulacean acid metabolism. New Phytol 48: 390–420CrossRefGoogle Scholar
  40. Ting IP, Gibbs M (eds) (1982) Crassulacean acid metabolism. American Society of Plant Physiologists, RockvilleGoogle Scholar
  41. Verbücheln O, Steup M (1984) Carbon metabolism and malate formation in the CAM plant Aloë arborescens. In: Sybesma C (ed) Advances in photosynthesis research, vol 3. Martinus Nijhoff, The Hague, pp 421–424Google Scholar
  42. Vickery HB (1954) The effect of abnormally prolonged alternating periods of light and darkness upon the composition of Bryophyllum calycinum leaves. Plant Physiol 29: 520–526PubMedCrossRefGoogle Scholar
  43. Whiting BH, van de Venter HA, Small JGC (1979) Crassulacean acid metabolism in jointed cactus (Opuntia aurantiaca) Lindley. Agroplantae 11: 41–43Google Scholar
  44. Winter K (1985) Crassulacean acid metabolism. In: Barber J, Baker NR (eds) Photosynthetic mechanisms and the environment. Elsevier, Amsterdam, pp 329–387Google Scholar
  45. Wolf J (1937) Beiträge zur Kenntnis des Säurestoffwechsels sukkulenter Crassulaceen. II. Mitteilung. Untersuchungen über Beziehungen zwischen Sedoheptose und Äpfelsäure. Planta 26: 516–522CrossRefGoogle Scholar
  46. Wood WML (1952) Organic acid metabolism of Sedum praealtum. J Exp Bot 3: 336–355CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • C. C. Black
    • 1
  • J.-Q. Chen
    • 1
  • R. L. Doong
    • 1
  • M. N. Angelov
    • 1
  • S. J. S. Sung
    • 1
  1. 1.Department of Biochemistry, Life Sciences BuildingThe University of GeorgiaAthensUSA

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