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Crassulacean acid metabolism photosynthesis: `working the night shift'

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Abstract

Crassulacean acid metabolism (CAM) can be traced from Roman times through persons who noted a morning acid taste of some common house plants. From India in 1815, Benjamin-Heyne described a `daily acid taste cycle' with some succulent garden plants. Recent work has shown that the nocturnally formed acid is decarboxylated during the day to become the CO2 for photosynthesis. Thus, CAM photosynthesis extends over a 24-hour day using several daily interlocking cycles. To understand CAM photosynthesis, several landmark discoveries were made at the following times: daily reciprocal acid and carbohydrate cycles were found during 1870 to 1887; their precise identification, as malic acid and starch, and accurate quantification occurred from 1940 to 1954; diffusive gas resistance methods were introduced in the early 1960s that led to understanding the powerful stomatal control of daily gas exchanges; C4 photosynthesis in two different types of cells was discovered from 1965 to ∼1974 and the resultant information was used to elucidate the day and night portions of CAM photosynthesis in one cell; and exceptionally high internal green tissue CO2 levels, 0.2 to 2.5%, upon the daytime decarboxylation of malic acid, were discovered in 1979. These discoveries then were combined with related information from C3 and C4 photosynthesis, carbon biochemistry, cellular anatomy, and ecological physiology. Therefore by ∼1980, CAM photosynthesis finally was rigorously outlined. In a nutshell, 24-hour CAM occurs by phosphoenol pyruvate (PEP) carboxylase fixing CO2(HCO3 ) over the night to form malic acid that is stored in plant cell vacuoles. While stomata are tightly closed the following day, malic acid is decarboxylated releasing CO2 for C3 photosynthesis via ribulose bisphosphate carboxylase oxygenase (Rubisco). The CO2 acceptor, PEP, is formed via glycolysis at night from starch or other stored carbohydrates and after decarboxylation the three carbons are restored each day. In mid to late afternoon the stomata can open and mostly C3 photosynthesis occurs until darkness. CAM photo-synthesis can be both inducible and constitutive and is known in 33 families with an estimated 15 to 20 000 species. CAM plants express the most plastic and tenacious photosynthesis known in that they can switch photosynthesis pathways and they can live and conduct photosynthesis for years even in the virtual absence of external H2O and CO2, i.e., CAM tenaciously protects its photosynthesis from both H2O and CO2 stresses.

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References

  • Bender MM (1968) Mass spectrometric studies of carbon 13 variations in corn and other grasses. Radiocarbon 10: 468–472

    Google Scholar 

  • Bender MM, Rouhani I, Vines HM and Black CC (1973) 13C/12C ratio changes in Crassulacean acid metabolism plants. Plant Physiol 52: 427–430

    PubMed  CAS  Google Scholar 

  • Bennet-Clark TA (1933a) The role of organic acids in plant metabolism. Part I. New Phytol 32: 37–71

    Article  CAS  Google Scholar 

  • Bennet-Clark TA (1933b) The role of the organic acids in plant metabolism. Part II. New Phytol 32: 128–161

    Article  CAS  Google Scholar 

  • Bennet-Clark TA (1949) Organic acids of plants. Ann Rev Biochem 18: 639–654

    Article  CAS  Google Scholar 

  • Black CC (1973) Photosynthetic carbon fixation in relation to net CO2 uptake. Annu Rev Plant Physiol 24: 253–286

    Article  CAS  Google Scholar 

  • Black CC, Chen TM and Brown RH (1969) Biochemical basis for plant competition. Weed Sci 17: 338–344

    CAS  Google Scholar 

  • Black CC, Mustardy L, Sung SS, Kormanik PP, Xu DP and Paz N (1987) Regulation and roles for alternative pathways of hexose metabolism in plants. Physiol Plant 69: 387–394

    Article  CAS  Google Scholar 

  • Black CC, Loboda T, Chen JQ and Sung SJS (1995) Can sucrose cleavage enzymes serve as markers for sink strength and is sucrose a signal molecule during plant sink development. In: Pontis HG, Salerno GL and Echevevria E (eds) Proceedings of First International Symposium on Sucrose Metabolism, pp 49–64. American Society of Plant Physiologists, Rockville, Maryland

    Google Scholar 

  • Bradbeer JW, Ranson SL and Stiller M (1958) Malate synthesis in Crassulacean leaves. I. The distribution of 14C in malate of leaves exposed in 14CO2 in the dark. Plant Physiol 33: 66–70

    PubMed  CAS  Google Scholar 

  • Burris RH and Black CC (eds) (1976) CO2 Metabolism and Plant Productivity. University Park Press, Baltimore, Maryland, 431pp

    Google Scholar 

  • Carnal NW and Black CC (1979) Pyrophosphate-dependent phosphofructokinase, A new glycolytic enzyme in pineapple leaves. Biochem Biophys Res Comm 86: 20–26

    Article  PubMed  CAS  Google Scholar 

  • Carnal NW and Black CC (1983) Phosphofructokinase activities in photosynthetic organisms: the occurrence of pyrophosphatedependent 6–phosphofructokinase in plants and algae. Plant Physiol 71: 150–155

    PubMed  CAS  Google Scholar 

  • Chang NK, Vines HM and Black CC (1981) Nitrate assimilation and Crassulacean acid metabolism in Kalanchoe fedtschenkoi marginate leaves. Plant Physiol 68: 464–468

    PubMed  CAS  Google Scholar 

  • Cockburn W, Ting IP and Sternberg LO (1979) Relationships between stomatal behavior and internal carbon dioxide concentration in Crassulacean acid metabolism plants. Plant Physiol 63: 1029–1032

    PubMed  CAS  Google Scholar 

  • Darwin C (1877) Communication to Gardner's Chronicle, 29 Dec. Collected Papers of Charles Darwin. Plant photo on the cover page of Science (#4291) (1979). Book Review Vol 196 (#4291), pp 784–785

    Google Scholar 

  • DeSaussure T (1804) Recherches chimiques sur la vegetation, p 25. Nyon, Paris

    Google Scholar 

  • Dittrich P (1975) Nicotinamide adenine dinucleotide specific ‘malic’ enzyme in Kalanchoe daigremontiana and other plants exhibiting Crassulacean acid metabolism. Plant Physiol 57: 310–314

    Google Scholar 

  • Dittrich P, Campbell WH and Black CC Jr. (1973) Phosphoenolpyruvate carboxykinase in plants exhibiting Crassulacean acid metabolism. Plant Physiol 52: 357–361

    PubMed  CAS  Google Scholar 

  • Ekern PC (1965) Evapotranspiration of pineapple in Hawaii. Plant Physiol 40: 736–739

    PubMed  CAS  Google Scholar 

  • Freitag H and Stichler W (2002) Bienertia cycloptera Bunge ex Boiss, Chenopodiaceae, another C4 plant without Kranz tissues. Plant Biol 4: 121–132

    Google Scholar 

  • Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature, and stomatal resistance. Meded Landbouwhogesch Wageningen 59: 1–68

    Google Scholar 

  • Gregory FG, Spear I and Thimann KV (1954) The interrelation between CO2 metabolism and photoperiodism in Kalanchoe. Plant Physiol 29: 220–229

    PubMed  CAS  Google Scholar 

  • Grew N (1682) An Idea of a Philosophical History of Plants, 2nd ed. Royal Society, London, 24 pp

    Google Scholar 

  • Hartsock TL and Nobel PS (1976) Watering converts a CAM plant to daytime CO2 uptake. Nature 262: 574–576

    Article  CAS  Google Scholar 

  • Hatch MD (2002) C4 Photosynthesis, discovery and resolution. Photosynth Res 73: 251–256

    Article  PubMed  CAS  Google Scholar 

  • Hatch MD, Osmond CB and Slatyer RO (eds) (1970) Photosynthesis and Photorespiration, Wiley-Interscience New York, 558 pp

    Google Scholar 

  • Heyne B (1815) On the deoxidation of the leaves of Cotyledon calycina. Trans Linn Soc London 11 pII: 213–215

    Google Scholar 

  • Joshi MC, Boyer JS and Kramer PJ (1965) Growth, carbon dioxide exchange, transpiration and transpiration ratio of pineapple. Bot Gaz 126: 174–179

    Article  CAS  Google Scholar 

  • Kamen MD (1963) Primary Processes in Photosynthesis. Academic Press, New York, 183 pp

    Google Scholar 

  • Kenyon WH, Kringstad R and Black CC (1978) Diurnal changes in the malic acid content of vacuoles isolated from leaves of the Crassulacean acid metabolism plant, Sedum telephium. FEBS Lett 94: 281–283

    Article  CAS  Google Scholar 

  • Kluge M and Osmond CB (1971) Pyruvate, Pi dikinase in Crassulacean acid metabolism. Naturwissenschaften 58: 414–415

    Article  CAS  Google Scholar 

  • Kluge M and Osmond CB (1972) Studies on phosphoenolpyruvate carboxylase and other enzymes of Crassulacean acid metabolism of Bryophyllum tubiflorum and Sedum praealtum. Z Pflanzenphysiol 66: 97–105

    Google Scholar 

  • Kluge M and Ting IP (1978) Crassulacean Acid Metabolism. Ecological Studies 30: 1–209. Springer-Verlag, Berlin

    Google Scholar 

  • Kraus G (1884) Ñeber dieWasservertheilungen der Pflanze. IV. Die Acidität des Zellsaftes. Abh Der Naturforsch Ges Halle 16: 141–205

    Google Scholar 

  • Link HF (1819) Zusatz (to translation of Heyne's paper). Jahrbücher der Gewächskunde von Sprengel, Sehrader und Link 1: 73–76

    Google Scholar 

  • Maxwell K, von Caemmerer S and Evans JR (1997) Is low internal conductance to CO2 diffusion a consequence of succulence in plants with Crassulacean acid metabolism? Aust J Plant Physiol 24: 777–786

    Article  CAS  Google Scholar 

  • Mayer A (1875) Ñber die Bedeutung der organischen Säuren in den Pflanzen. Landw Versuchsstat 18: 410–452

    Google Scholar 

  • Mayer A (1887) Die Sauerstoffausscheidung einiger dickblättriger Pflanzen bei Abwesenheit von Kohlensäure und die physiologische Bedeutung dieser Erscheinung. Landwirtschaftl Vers Stn 34: 127–143

    Google Scholar 

  • Moyse A (1955) Le metabolisme des acides organiques chez Bryophyllum (Crassulaceae). II. Les variations de l'acidité et la photosynthèse, en fonction de la tension d'oxygène. Physiol Plant 8: 478–492

    Article  CAS  Google Scholar 

  • Nimmo HG (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5: 75–80

    Article  PubMed  CAS  Google Scholar 

  • Nishida K (1963) Studies on the re-assimilation of respiratory CO2 in illuminated leaves. Plant Cell Physiol 3: 111–124

    Google Scholar 

  • Nobel PS, Bobich EG (2002) Initial net CO2 uptake responses and root growth for a CAM community placed in a closed environment. Ann Bot 90: 593–598

    Article  PubMed  CAS  Google Scholar 

  • Nuernbergk EL (1961) Endogener Rhythmus und CO2 Stoffwechsel bei Pflanzen mit diurnalem Säurerhythmus. Planta 56: 28–70

    Article  CAS  Google Scholar 

  • O'Leary MH and Osmond CB (1980) Diffusional contribution to carbon isotope fractionation during dark CO2 fixation in CAM plants. Plant Physiol 66: 931–934

    PubMed  Google Scholar 

  • Osmond CB (1976) CO2 assimilation and dissimilation in the light and dark in CAM plants. In: RH Burris and CC Black (eds) CO2 Metabolism and Plant Productivity, pp 217–233. University Park Press, Baltimore, Maryland

    Google Scholar 

  • Osmond CB (1978) Crassulacean acid metabolism - a curiosity in context. Annu Rev Plant Physiol 29: 379–414

    Article  CAS  Google Scholar 

  • Osmond CB, Allaway WG, Sutton BG, Troughton JH, Queiroz O, Lüttge U and Winter K (1973) Carbon isotope discrimination in photosynthesis of CAM plants. Nature 246: 41–42

    Article  CAS  Google Scholar 

  • Porter HK and Ranson SL (1980) Meirion Thomas. Biogr Mem R Soc XX: 547–568

    Google Scholar 

  • Pucher GW and Vickery HB (1942) On the identity of the so-called Crassulacean malic acid with isocitric acid. J Biol Chem 145: 525–532

    CAS  Google Scholar 

  • Pucher GW, Sherman CC and Vickery HB (1936) Colorimetric determination of citric acid. J Biol Chem 113: 235–245

    CAS  Google Scholar 

  • Pucher GW, Wakeman AJ and Vickery HB (1941) Organic acids in plant tissue. Modifications of analytical methods. Ind Eng Chem Anal Ed 13: 244–246

    Article  CAS  Google Scholar 

  • Pucher GW, Leavenworth CS, Ginter WD and Vickery HB (1947) Studies in the metabolism of crassulacean plants: the diurnal variation in organic acid and starch content of Bryophyllum calycinum. Plant Physiol 22: 360–376

    PubMed  CAS  Google Scholar 

  • Queiroz O (1967) Recherche d'un modèle enzymatique pour le déterminisme de la désacidification diurne chez les Crassulacées. CR Acad Sci 265: 1928–1931

    CAS  Google Scholar 

  • Ranson SL and Thomas M (1960) Crassulacean acid metabolism. Annu Rev Plant Physiol 11: 81–110

    Article  CAS  Google Scholar 

  • Reinfelder JR, Kraepiel AML and Morel FMM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996–999

    Article  PubMed  CAS  Google Scholar 

  • Rouhani I (1972) Pathways of carbon metabolism in spongy mesophyll cells isolated from Sedum telephium leaves and their relationship to Crassulacean acid metabolism plants. PhD thesis, University of Georgia, Athens

    Google Scholar 

  • Saltman P, Kunitake G, Spolter H and Stitt C (1956) The dark fixation of CO2 by succulent leaves: the first products. Plant Physiol 31: 464–468

    Article  PubMed  CAS  Google Scholar 

  • Smith BN and Epstein S (1971) Two categories of 13C/12C ratios for higher plants. Plant Physiol 47: 380–384

    PubMed  CAS  Google Scholar 

  • Smith JAC and Winter K (1996) Taxonomic distribution of Crassulacean acid metabolism. In: Winter K and Smith JAC (eds) Crassulacean Acid Metabolism, pp 427–436. Springer-Verlag, Berlin

    Google Scholar 

  • Smyth DA and Black CC (1984) Measurement of the pyrophosphate content of plant tissues. Plant Physiol 75: 862–864

    PubMed  CAS  Google Scholar 

  • Spalding MH, Stumpf DK, Ku MSB, Burris RH and Edwards GE (1979) Crassulacean acid metabolism and diurnal variations of internal CO2 and O2 concentrations in Sedum praealtum DC. Aust J Plant Physiol 6: 557–67

    CAS  Google Scholar 

  • Sugiyama T, Laetsch WM (1975) Occurrence of pyruvate orthophosphate dikinase in the succulent plant, Kalanchoe daigremontiana Hamet et Perr. Plant Physiol 56: 605–607

    PubMed  CAS  Google Scholar 

  • Thomas M and Beevers H (1949) Physiological studies on acid metabolism in green plants. II. Evidence of CO2 fixation in Bryophyllum and the study of diurnal variation of acidity in this genus. New Phytol 48: 421–447

    Article  CAS  Google Scholar 

  • Ting IP and Gibbs M (eds) (1982) Crassulacean Acid Metabolism. American Society of Plant Physiology, Rockville, Maryland, 308pp

    Google Scholar 

  • Ting IP and Hanscom Z (1977) Induction of acid metabolism in Portulacaria afra. Plant Physiol 59: 511–514

    PubMed  CAS  Google Scholar 

  • Vickery HB (1972) A chemist among plants. Annu Rev Plant Physiol 23: 1–28

    Article  CAS  Google Scholar 

  • Vickery HB, and Pucher GW (1940) Organic acids of plants. Ann Rev Biochem 9: 529–544

    Article  CAS  Google Scholar 

  • Voznesenskaya EV, Franceschi V, K iirats O, Freitag H and Edwards GE (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414: 543–546

    Article  PubMed  CAS  Google Scholar 

  • Walker DA (1956) Malate synthesis in a cell free extract from a Crassulacean plant. Nature 178: 593–594

    Article  CAS  Google Scholar 

  • Warren DM and Wilkins MB (1961) An endogenous rhythm in the rate of dark fixation of carbon dioxide in leaves of Bryophyllum fedtschenkoi. Nature 191: 686–688

    Article  CAS  Google Scholar 

  • Winter K and Smith JAC (eds) (1996) Crassulacean Acid Metabolism.Springer-Verlag, Heidelberg, 436 pp

    Google Scholar 

  • Winter K and von Willert DJ (1972) NaCl-induzierter crassulaceensäurestoffwechsel bei Mesembryanthemum crystallinum. Z Pflanzenphysiol 67: 166–170

    CAS  Google Scholar 

  • Winter K, Lüttge U, Winter E and Troughton JH (1978) Seasonal shift from C3 photo-synthesis to Crassulacean acid metabolism in Mesembryanthemum crystallinum in its native environment. Oecologia 34: 225–237

    Article  Google Scholar 

  • Wolf J (1937) Beiträge zur Kenntnis des Säurestoffwechsels Sukkulenter Crassulaceen. II. Untersuchungen über Beziehungen zwischen Sedoheptose und Äpfel-und Zitronensäure. Planta 29: 314–324

    Article  Google Scholar 

  • Wolf J (1938) Beiträge zur Kenntnis des Säurestoffwechsels Sukkulenter Crassulaceen. III. Stoffliche zusammenhänge zwischen gärfähigen Kohlenhydraten und Organischen Säuren. Planta 29: 314–324

    Article  Google Scholar 

  • Wolf J (1949) Beiträge zur Kenntnis des Säurestoffwechsels sukkulenter. Crassulaceen. VI. Mitt.: neuere Vorstellungen vom Chemismus des Säurestoffwechsels. Planta 37: 510–534

    Article  CAS  Google Scholar 

  • Wolf J (1960) Der diurnale Säurerhythmus. In: Ruhland W (ed) Encyclopedia of Plant Physiology, Vol 12, pp 809–889. Springer-Verlag, Berlin

    Google Scholar 

  • Wood HG and Werkmann CH (1938) The utilization of carbon dioxide by propionic acid bacteria. Biochem J 32: 1262–1271

    PubMed  CAS  Google Scholar 

Download references

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Black, C.C., Osmond, C.B. Crassulacean acid metabolism photosynthesis: `working the night shift'. Photosynthesis Research 76, 329–341 (2003). https://doi.org/10.1023/A:1024978220193

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