Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism
Joseph A. M. Holtum A D , J. Andrew C. Smith B and H. Ekkehard Neuhaus CA School of Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.
B Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK.
C Universität Kaiserslautern, Pflanzenphysiologie, Erwin Schrödinger-Strasse, D-67653 Kaiserslautern, Germany.
D Corresponding author. Email: joseph.holtum@jcu.edu.au
E This paper originates from a presentation at the IVth International Congress on Crassulacean Acid Metabolism, Tahoe City, California, USA, July–August 2004
F This paper is dedicated to Professor Dr Erwin Latzko on the occasion of his 80th birthday.
Functional Plant Biology 32(5) 429-449 https://doi.org/10.1071/FP04189
Submitted: 17 October 2004 Accepted: 22 February 2005 Published: 27 May 2005
Abstract
The massive daily reciprocal transfer of carbon between acids and carbohydrates that is unique to crassulacean acid metabolism (CAM) involves extensive and regulated transport of metabolites between chloroplasts, vacuoles, the cytosol and mitochondria. In this review of the CAM pathways of carbon flow and intracellular transport, we highlight what is known and what has been postulated. For three of the four CAM pathway variants currently known (malic enzyme- or PEP carboxykinase-type decarboxylase, and starch- or soluble sugar-type carbohydrate storage), the mechanisms of intracellular transport are still hypothetical and have yet to be demonstrated experimentally. Even in malic enzyme starch-storing species such as Kalanchoë daigremontiana Hamet et Perr. and Mesembryanthemum crystallinum L., the best-described variants of plants with the second-most common mode of photosynthetic carbon metabolism known, no tonoplast or mitochondrial transporter has been functionally described at a molecular level.
Keywords: CAM, photosynthetic carbon metabolism, plant metabolite transport.
Acknowledgments
JAMH was supported by the JCU Special Studies Program. We thank K Winter for constructive comments that improved the quality of the manuscript.
André M,
Thomas DA,
von Willert DJ, Gerbaud A
(1979) Oxygen and carbon dioxide exchanges in crassulacean-acid-metabolism-plants. Planta 147, 141–144.
| Crossref | GoogleScholarGoogle Scholar |
Allen GJ, Sanders D
(1997) Vacuolar ion channels of higher plants. Advances in Botanical Research 25, 217–252.
Aoki N,
Ohnishi J, Kanai R
(1992) Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants — a comparative study. Plant and Cell Physiology 33, 805–809.
Aoki N,
Ohnishi J, Kanai R
(1994) Proton / pyruvate cotransport into mesophyll chloroplasts of C4 plants. Plant and Cell Physiology 35, 801–806.
Arron GP,
Spalding MH, Edwards GE
(1979) Isolation and oxidative properties of intact mitochondria from the leaves of Sedum praealtum a crassulacean acid metabolism plant. Plant Physiology 64, 182–186.
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 Phytologist 117, 483–491.
Barkla BJ,
Zingarelli L,
Blumwald E, Smith JAC
(1995) Tonoplast Na+ / H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiology 109, 549–556.
| PubMed |
Berkemeyer M,
Scheibe R, Ocheretina O
(1998) A novel, non-redox-regulated NAD-dependent malate dehydrogenase from chloroplasts of Arabidopsis thaliana L. Journal of Biological Chemistry 273, 27927–27933.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bettey M, Smith JAC
(1993) Dicarboxylate transport at the vacuolar membrane of the CAM plant Kalanchoë daigremontiana: sensitivity to protein-modifying and sulphydryl reagents. Biochimica et Biophysica Acta 1152, 270–279.
| PubMed |
Black, CC ,
Carnal, NW ,
and
Kenyon, WH (1982). Compartmentation and the regulation of CAM. In ‘Crassulacean acid metabolism’. pp. 51–68. (American Society of Plant Physiologists: Rockville, MD)
Black, CC ,
Chen, J-Q ,
Doong, RL ,
Angelov, MN ,
and
Sung, SJS (1996). Alternative carbohydrate reserves used in the daily cycle of crassulacean acid metabolism. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 31–45. (Springer-Verlag: Berlin)
Blasius B,
Neff R,
Beck F, Lüttge U
(1999) Oscillatory model of crassulacean acid metabolism with a dynamic hysteresis switch. Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 93–101.
| Crossref | GoogleScholarGoogle Scholar |
Bohn A,
Hinderlich S,
Hutt MT,
Kaiser F, Lüttge U
(2003) Identification of rhythmic subsystems in the circadian cycle of crassulacean acid metabolism under thermoperiodic perturbations. Biological Chemistry 384, 721–728.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Borland AM, Dodd AN
(2002) Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Functional Plant Biology 29, 707–716.
| Crossref | GoogleScholarGoogle Scholar |
Borland AM, Taybi T
(2004) Synchronization of metabolic processes in plants with crassulacean acid metabolism. Journal of Experimental Botany 55, 1255–1265.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Borland AM,
Griffiths H,
Maxwell C,
Broadmeadow MSJ,
Griffiths NM, Barnes JD
(1992) On the ecophysiology of the Clusiaceae in Trinidad: expression of CAM in Clusia minor during the transition from wet to dry season and characterisation of three endemic species. New Phytologist 122, 349–357.
Borland AM,
Griffiths H,
Broadmeadow MSJ,
Fordham MC, Maxwell C
(1993) Short-term changes in carbon-isotope discrimination in the C3–CAM intermediate Clusia minor L. growing in Trinidad. Oecologia 95, 444–453.
| Crossref | GoogleScholarGoogle Scholar |
Borland AM,
Griffiths H,
Broadmeadow MSJ,
Fordham MC, Maxwell C
(1994) Carbon-isotope composition of biochemical fractions and the regulation of carbon balance in leaves of the C3-crassulacean acid metabolism intermediate Clusia minor L. growing in Trinidad. Plant Physiology 106, 493–501.
| PubMed |
Borland AM,
Griffiths H,
Maxwell C,
Fordham MC, Broadmeadow MSJ
(1996) CAM induction in Clusia minor L. during the transition of wet to dry season in Trinidad: the role of organic acid speciation and decarboxylation. Plant, Cell and Environment 19, 655–664.
Borland AM,
Tésci LI,
Leegood RC, Walker RP
(1998) Inducibility of crassulacean acid metabolism (CAM) in Clusia species: physiological / biochemical characterisation and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM. Planta 205, 342–351.
| Crossref | GoogleScholarGoogle Scholar |
Borland AM,
Hartwell J,
Jenkins GI,
Wilkins MB, Nimmo HG
(1999) Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in crassulacean acid metabolism. Plant Physiology 121, 889–896.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bradbeer, JW ,
Cockburn, W ,
and
Ranson, SL (1975). The labelling of the carboxyl carbon atoms of malate in Kalanchoë crenata leaves. In ‘Environmental and biological control of photosynthesis’. pp. 265–372. (Dr W Junk: The Hague)
Bremberger C, Lüttge U
(1992) Dynamics of tonoplast proton pumps and other tonoplast proteins of Mesembryanthemum crystallinum during the induction of crassulacean acid metabolism. Planta 188, 575–580.
| Crossref | GoogleScholarGoogle Scholar |
Bremberger C,
Haschke H-P, Lüttge U
(1988) Separation and purification of the tonoplast ATPase and pyrophosphatase from plants with constitutive and inducible crassulacean acid metabolism. Planta 175, 465–470.
| Crossref | GoogleScholarGoogle Scholar |
Brownell PF, Crossland CJ
(1974) Growth responses to sodium by Bryophyllum tubiflorum under conditions inducing crassulacean-acid metabolism. Plant Physiology 54, 416–417.
Carter C,
Pan S,
Zouhar J,
Avila EL,
Girke T, Raikhel NV
(2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unpredicted proteins. The Plant Cell 16, 3285–3303.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Carter PJ,
Nimmo HG,
Fewson CA, Wilkins MB
(1991) Circadian rhythms in the activity of a plant protein kinase. EMBO Journal 10, 2063–2068.
| PubMed |
Cheffings CM,
Pantoja O,
Ashcroft FM, Smith JAC
(1997) Malate transport and vacuolar ion channels in CAM plants. Journal of Experimental Botany 48, 623–631.
Chen L-S, Nose A
(2000) Characteristics of adenosinetriphosphatase and inorganic pyrophosphatase in tonoplast isolated from three CAM species, Ananas comosus, Kalanchoë pinnata and Kalanchoë daigremontiana.
Plant Production Science 3, 24–31.
Christopher JT, Holtum JAM
(1996) Patterns of carbon partitioning in leaves of crassulacean acid metabolism species during deacidification. Plant Physiology 112, 393–399.
| PubMed |
Christopher JT, Holtum JAM
(1998) Carbohydrate partitioning in the leaves of Bromeliaceae performing C3 photosynthesis or crassulacean acid metabolism. Australian Journal of Plant Physiology 25, 371–376.
Cook RM,
Lindsay JG,
Wilkins MB, Nimmo HG
(1995) Decarboxylation of malate in the crassulacean acid metabolism plant Bryophyllum (Kalanchoë) fedtschenkoi. Role of NAD-malic enzyme. Plant Physiology 109, 1301–1307.
| PubMed |
Crayn DM,
Winter K, Smith JAC
(2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences USA 101, 3703–3708.
| Crossref | GoogleScholarGoogle Scholar |
Cushman JC
(1993) Molecular cloning and expression of chloroplast NADP-malate dehydrogenase during crassulacean acid metabolism induced by salt stress. Photosynthesis Research 35, 15–27.
Cushman JC
(2001) Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environments. Plant Physiology 127, 1439–1448.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cushman, JC ,
and
Bohnert, HJ (1996). Transcriptional activation of CAM genes during development and environmental stress. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 135–158. (Springer-Verlag: Berlin)
Cushman JC, Bohnert HJ
(1997) Molecular genetics of crassulacean acid metabolism. Plant Physiology 113, 667–676.
| PubMed |
Cushman JC, Bohnert HJ
(1999) Crassulacean acid metabolism: molecular genetics. Annual Review of Plant Physiology and Plant Molecular Biology 50, 305–332.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cushman, JC ,
and
Bohnert, HJ (2002). Induction of crassulacean acid metabolism by salinity — molecular aspects. In ‘Salinity: environment — plants — molecules’. pp. 361–393. (Kluwer Academic Publishers: Dordrecht)
Cushman JC, Borland AM
(2002) Induction of crassulacean acid metabolism by water limitation. Plant, Cell and Environment 25, 295–310.
| Crossref | GoogleScholarGoogle Scholar |
Davies JM,
Poole RJ, Sanders D
(1993) The computed free energy change of hydrolysis of inorganic pyrophosphate and ATP: apparent significance for inorganic pyrophosphate-driven reactions of intermediary metabolism. Biochimica et Biophysica Acta 1141, 29–36.
Day DA
(1980) Malate decarboxylation by Kalanchoë daigremontiana mitochondria and its role in crassulacean acid metabolism. Plant Physiology 65, 675–679.
Deleens E, Garnier-Dardart J
(1977) Carbon isotope composition of biochemical fractions isolated from leaves of Bryophyllum daigremontianum Berger, a plant with crassulacean acid metabolism: some physiological aspects related to CO2 dark fixation. Planta 135, 241–248.
| Crossref | GoogleScholarGoogle Scholar |
Deleens E,
Garnier-Dardart J, Queiroz O
(1979) Carbon isotope composition of intermediates of the starch-malate sequence and level of the crassulacean acid metabolism in leaves of Kalanchoe blossfeldiana Tom Thumb. Planta 146, 441–449.
| Crossref | GoogleScholarGoogle Scholar |
Demmig B, Winter K
(1983) Photosynthetic characteristics of chloroplasts isolated from Mesembryanthemum crystallinum a halophilic plant capable of crassulacean acid metabolism. Planta 159, 66–76.
| Crossref | GoogleScholarGoogle Scholar |
Dittrich P
(1976) Nicotinamide adenine dinucleotide-specific ‘malic’ enzyme in Kalanchoe daigremontiana and other plants exhibiting crassulacean acid metabolism. Plant Physiology 57, 310–314.
Dittrich P,
Campbell WH, Black CC
(1973) Phosphoenolpyruvate carboxykinase in plants exhibiting crassulacean acid metabolism. Plant Physiology 52, 357–361.
Dodd AN,
Borland AM,
Haslam RP,
Griffiths H, Maxwell K
(2002) Crassulacean acid metabolism: plastic, fantastic. Journal of Experimental Botany 53, 569–580.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dodd AN,
Griffiths H,
Taybi T,
Cushman JC, Borland AM
(2003) Integrating diel starch metabolism with the circadian and environmental regulation of crassulacean acid metabolism in Mesembryanthemum crystallinum.
Planta 216, 789–797.
| PubMed |
Eicks M,
Maurino V,
Knappe S,
Flügge U-I, Fischer K
(2002) The plastidic pentose phosphate transporter represents an important link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiology 128, 512–522.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Emmerlich V,
Linka N,
Reinhold T,
Hurth MA,
Traub M,
Martinoia E, Neuhaus HE
(2003) The plant homolog to the human sodium / dicarboxylic cotransporter is the vacuolar malate carrier. Proceedings of the National Academy of Sciences USA 100, 11122–11126.
| Crossref | GoogleScholarGoogle Scholar |
Epimashko S,
Meckel T,
Fischer-Schliebs E,
Lüttge U, Thiel G
(2004) Two functionally different vacuoles for static and dynamic purposes in one plant mesophyll leaf cell. The Plant Journal 37, 294–300.
| PubMed |
Flügge I-U,
Stitt M, Heldt HW
(1985) Light-driven uptake of pyruvate into mesophyll chloroplasts from maize. FEBS Letters 183, 335–339.
| Crossref | GoogleScholarGoogle Scholar |
Flügge U-I,
Häusler RE,
Ludewig F, Fischer K
(2003) Functional genomics of phosphate antiport systems in plastids. Physiologia Plantarum 118, 475–482.
| Crossref | GoogleScholarGoogle Scholar |
Franco AC,
Ball E, Lüttge U
(1990) Patterns of gas exchange and organic acid oscillations in tropical trees of the genus Clusia.
Oecologia 85, 108–114.
| Crossref | GoogleScholarGoogle Scholar |
Franco AC,
Ball E, Lüttge U
(1992) Differential effects of drought and light levels on accumulation of citric and malic acids during CAM in Clusia.
Plant, Cell and Environment 15, 821–829.
Giegé P,
Heazlewood JL,
Roessner-Tunali U,
Millar AH,
Fernie AR,
Leaver CJ, Sweetlove LJ
(2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. The Plant Cell 15, 2140–2151.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Golldack D, Dietz KJ
(2001) Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiology 125, 1643–1654.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Griffiths H,
Ong BL,
Avadhani PN, Goh CJ
(1989) Recycling of respiratory CO2 during crassulacean acid metabolism: alleviation of photoinhibition. Planta 179, 115–122.
| Crossref | GoogleScholarGoogle Scholar |
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. Journal of Experimental Botany 43, 345–352.
Haag-Kerwer A,
Grams TEE,
Olivares E,
Ball E,
Arndt S,
Popp M,
Medina E, Lüttge U
(1996) Comparative measurements of gas-exchange, acid accumulation and chlorophyll a fluorescence of different species of Clusia showing C3 photosynthesis, or crassulacean acid metabolism, at the same field site in Venezuela. New Phytologist 134, 215–226.
Hafke JB,
Neff R,
Hütt MT,
Lüttge U, Thiel G
(2001) Day-to-night variations of cytoplasmic pH in a crassulacean acid metabolism plant. Protoplasma 216, 164–170.
| PubMed |
Hafke JB,
Hafke Y,
Smith JAC,
Lüttge U, Thiele G
(2003) Vacuolar malate uptake is mediated by an anion-selective inward rectifier. The Plant Journal 35, 116–128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hatch MD,
Dröscher L,
Flügge U-I, Heldt HW
(1984) A specific translocator for oxaloacetate transport in chloroplasts. FEBS Letters 178, 15–19.
| Crossref | GoogleScholarGoogle Scholar |
Häusler, RE ,
Holtum, JAM ,
and
Latzko, E (1987). CO2, not HCO3
–, is the inorganic carbon substrate of NADP malic enzyme from maize and wheat germ. In ‘Progress in photosynthesis research: III’. pp. 527–530. (Martinus Nijhoff: The Hague)
Häusler RE,
Baur B,
Scharte J,
Teichmann T,
Eicks M,
Fischer KL,
Flügge U-I,
Schubert S,
Weber A, Fischer K
(2000) Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum.
The Plant Journal 24, 285–296.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heineke D,
Kruse A,
Flügge IU,
Frommer WB,
Riesmeier JW,
Willmitzer L, Heldt HW
(1994a) Effect of antisense repression on the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 193, 174–180.
| Crossref | GoogleScholarGoogle Scholar |
Heineke D,
Wildenberger K,
Sonnewald U,
Wilmitzer L, Heldt HW
(1994b) Accumulation of hexoses in leaf vacuoles: studies with transgenic potato plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm. Planta 194, 29–33.
| Crossref | GoogleScholarGoogle Scholar |
Herppich M,
Herppich WB, von Willert DJ
(1995) Diurnal rhythm in citric acid content preceded the onset of night-time malic acid accumulation during metabolic changes in C3 to CAM in salt-stressed plants of Mesembryanthemum crystallinum.
Journal of Plant Physiology 147, 38–42.
Hobbie EA, Werner RA
(2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytologist 161, 371–385.
| Crossref | GoogleScholarGoogle Scholar |
Holtum JAM, Osmond CB
(1981) The gluconeogenic metabolism of pyruvate during deacidification in plants with crassulacean acid metabolism. Australian Journal of Plant Physiology 8, 31–44.
Holtum JAM, Winter K
(1982) Activity of enzymes of carbon metabolism during the induction of crassulacean acid metabolism in Mesembryanthemum crystallinum.
Planta 155, 8–16.
| Crossref | GoogleScholarGoogle Scholar |
Holtum, JAM ,
and
Osmond, CB (1995). The revolution in carbon partitioning and source-sink interactions in plants from the perspective of CAM. In ‘Carbon-partitioning and source-sink interactions in plants’. pp. 1–12. (American Society of Plant Physiologists: Rockville, MD)
Holtum JAM,
Aranda J,
Virgo A,
Gehrig HH, Winter K
(2004) δ13C Values and crassulacean acid metabolism in Clusia species from Panama. Trees — Structure and Function 18, 658–668.
| Crossref | GoogleScholarGoogle Scholar |
Hurth MA,
Suh SJ,
Kretzschmar T,
Geis T,
Bregante M,
Gambale F,
Martinoia E, Neuhaus HE
(2005) Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. Plant Physiology 137, 901–910.
| Crossref |
PubMed |
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 Physiology 98, 1494–1497.
Kalt W,
Osmond CB, Siedow JN
(1990) Malate metabolism in the dark after carbon-13-labeled carbon dioxide fixation in the crassulacean plant Kalanchoe tubiflora.
Plant Physiology 94, 826–832.
Kelly GJ, Latzko E
(1977) Chloroplast phosphofructokinase. I. Proof of phosphofructokinase activity in chloroplasts. Plant Physiology 60, 290–294.
Kenyon WH,
Severson RF, Black CC
(1985) Maintenance carbon cycle in crassulacean acid metabolism leaves. Plant Physiology 77, 183–189.
Klink R,
Haschke H-P,
Kramer D, Lüttge U
(1990) Membrane particles, proteins and ATPase activity of tonoplast vesicles of Mesembryanthemum crystallinum in the C3 and CAM state. Botanica Acta 103, 24–31.
Kluge C,
Lamkemeyer P,
Tavakoli N,
Golldack D,
Kandlbinder A, Dietz KJ
(2003) cDNA cloning of 12 subunits of the V-type ATPase from Mesembryanthemum crystallinum and their expression under stress. Molecular Membrane Biology 20, 171–183.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kluge M
(1969) Veränderliche Markierungsmuster bei 14CO2-Fütterung von Bryophyllum tubiflorum zu verschiedenen Zeitpunkten der Hell-Dunkel-Periode. I. Die Fütterung unter Belichtung. Planta 88, 113–129.
| Crossref |
Kondo A,
Nose A, Ueno O
(2001) Coordinated accumulation of the chloroplastic and cytosolic pyruvate, Pi dikinases with enhanced expression of CAM in Kalanchoë blossfeldiana.
Physiologia Plantarum 111, 116–122.
| Crossref | GoogleScholarGoogle Scholar |
Kondo A,
Nose A,
Yuasa H, Ueno O
(2000) Species variation in the intracellular localization of pyruvate, Pi dikinase in leaves of crassulacean-acid-metabolism plants: an immunogold electron-microscope study. Planta 210, 611–621.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kore-eda S, Kanai R
(1997) Induction of glucose-6-phosphate transport activity in chloroplasts of Mesembryanthemum crystallinum by the C3–CAM transition. Plant and Cell Physiology 38, 895–901.
Kore-eda S,
Yamashita T, Kanai R
(1996) Induction of light dependent pyruvate transport into chloroplasts of Mesembryanthemum crystallinum by salt stress. Plant and Cell Physiology 37, 257–262.
Kore-eda S,
Cushman MA,
Akselrod I,
Bufford D,
Fredrickson M,
Clark E, Cushman JC
(2004) Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum.
Gene 341, 83–92.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kore-eda S,
Noake C,
Ohishi M,
Ohnishi J-I, Cushman JC
(2005) Transcriptional regulation of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum.
Functional Plant Biology 32, 451–466.
| Crossref | GoogleScholarGoogle Scholar |
Ku MSB,
Spalding MH, Edwards GE
(1980) Intracellular localization of phosphoenolpyruvate carboxykinase in leaves of C4 and CAM plants. Plant Science Letters 19, 1–8.
| Crossref | GoogleScholarGoogle Scholar |
Leegood RC, Walker RP
(2003) Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Archives of Biochemistry and Biophysics 414, 204–210.
Leustek T, Saito K
(1999) Sulfate transport and assimilation in plants. Plant Physiology 120, 637–644.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Logan DC, Leaver CJ
(2000) Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. Journal of Experimental Botany 51, 865–871.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Löw R,
Rockel B,
Kirsch M,
Ratajczak R,
Hörtensteiner S,
Martinoia E,
Lüttge U, Rausch T
(1996) Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum.
Plant Physiology 110, 259–265.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U
(1988) Day–night changes in citric-acid levels in crassulacean acid metabolism: phenomenon and ecophysiological significance. Plant, Cell and Environment 11, 445–451.
Lüttge U
(1993) The role of crassulacean acid metabolism (CAM) in the adaption of plants to salinity. New Phytologist 125, 59–71.
Lüttge, U (1996).
Clusia: plasticity and diversity in a genus of C3 / CAM intermediate tropical trees. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 296–311. (Springer-Verlag: Berlin)
Lüttge U
(1999) One morphotype, three physiotypes: sympatric species of Clusia with obligate C3-photosynthesis, obligate CAM and C3–CAM intermediate behaviour. Plant Biology 1, 138–148.
Lüttge U
(2000a) The tonoplast functioning as the master switch for circadian regulation of crassulacean acid metabolism. Planta 211, 761–769.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U
(2000b) Light stress and crassulacean acid metabolism. Phyton 40, 65–82.
Lüttge U
(2002) CO2-concentrating: consequences in crassulacean acid metabolism. Journal of Experimental Botany 53, 2131–2142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U
(2004) Ecophysiology of crassulacean acid metabolism (CAM). Annals of Botany 93, 629–652.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lüttge U, Smith JAC
(1984) Mechanism of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoë daigremontiana.
Journal of Membrane Biology 81, 149–158.
Lüttge U, Ratajczak R
(1997) The physiology, biochemistry and molecular biology of the plant vacuolar ATPase. Advances in Botanical Research 25, 253–296.
Lüttge U,
Smith JAC,
Osmond CB, Marigo G
(1981) Energetics of malate accumulation in the vacuoles of Kalanchoë tubiflora.
FEBS Letters 126, 81–84.
| Crossref | GoogleScholarGoogle Scholar |
Lüttge, U ,
Smith, JAC ,
and
Marigo, G (1982). Membrane transport, osmoregulation, and the control of CAM. In ‘Crassulacean acid metabolism’. pp. 69–91. (American Society of Plant Physiologists: Rockville, MD)
Markovich D, Murer H
(2004) The SLC13 gene family of sodium / sulphate / carboxylate cotransporters. European Journal of Physiology 447, 594–602.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marquardt G, Lüttge U
(1987) Proton translocating enzymes at the tonoplast of leaf cells of the CAM plant Kalanchoë daigremontiana. II. The pyrophosphatase. Journal of Plant Physiology 129, 269–286.
Master RWP
(1959) Organic acid and carbohydrate metabolism in Nopalea cochinellifera.
Experientia 15, 30–31.
| PubMed |
Maxwell K,
von Caemmerer S, Evans JR
(1997) Is a low internal conductance to CO2 diffusion a consequence of succulence in plants with crassulacean acid metabolism? Australian Journal of Plant Physiology 24, 777–786.
Maxwell K,
Badger MR, Osmond CB
(1998) A comparison of CO2 and O2-exchange patterns and the relationship with chlorophyll fluorescence during photosynthesis in C3 and CAM plants. Australian Journal of Plant Physiology 25, 45–52.
McRae SR,
Christopher JT,
Smith JAC, Holtum JAM
(2002) Sucrose transport across the vacuolar membrane of Ananas comosus.
Functional Plant Biology 29, 717–724.
| Crossref | GoogleScholarGoogle Scholar |
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, 441–446.
| Crossref | GoogleScholarGoogle Scholar |
Millhouse J,
Wiskich JT, Beevers H
(1983) Metabolite oxidation and transport in mitochondria of endosperm from germinating castor-bean Ricinus communis.
Australian Journal of Plant Physiology 10, 167–178.
Müller ML, Taiz L
(2002) Regulation of the lemon-fruit V-ATPase by variable stoichiometry and organic acids. Journal of Membrane Biology 185, 209–220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neuhaus HE, Schulte N
(1996) Starch degradation in chloroplasts isolated from C3 or CAM (crassulacean acid metabolism)-induced Mesembryanthemum crystallinum L. The Biochemical Journal 318, 945–953.
| PubMed |
Neuhaus HE, Wagner R
(2000) Solute pores, ion channels, and metabolite transporters in the outer and inner envelope membranes of higher plant plastids. Biochimica et Biophysica Acta 1465, 307–323.
| PubMed |
Neuhaus HE,
Holtum JAM, Latzko E
(1988) Transport of phosphoenolpyruvate by chloroplasts from Mesembryanthemum crystallinum L. exhibiting crassulacean acid metabolism. Plant Physiology 87, 64–68.
Nimmo GA,
Wilkins MB,
Fewson CA, Nimmo HG
(1987) Persistent circadian rhythms in the phosphorylation state of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi leaves and in its sensitivity to inhibition by malate. Planta 170, 408–415.
| Crossref | GoogleScholarGoogle Scholar |
O’Leary MH, Osmond CB
(1980) Diffusional contribution to carbon isotope fractionation during dark carbon dioxide fixation in crassulacean acid metabolism plants. Plant Physiology 66, 931–934.
Olivares E, Medina E
(1990) Carbon dioxide exchange, soluble carbohydrates and acid accumulation in a fructan accumulating plant: Fourcroya humboldtiana Treal. Journal of Experimental Botany 41, 579–586.
Olivares E,
Faist K,
Kluge M, Lüttge U
(1993)
14CO2 pulse-chase labelling in Clusia minor L. Journal of Experimental Botany 44, 497–501.
Osmond CB
(1978) Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29, 379–414.
| Crossref | GoogleScholarGoogle Scholar |
Osmond, CB ,
and
Holtum, JAM (1982). Crassulacean acid metabolism. In ‘The biochemistry of plants. Vol. 8’. pp. 283–370. (Academic Press: New York)
Osmond CB,
Holtum JAM,
O’Leary MH,
Roeske C,
Wong SC,
Summons RE, Avadhani PN
(1988) Regulation of malic acid metabolism in crassulacean acid metabolism plants in the dark and light in-vivo evidence from carbon-13 labeling patterns after carbon-13 dioxide fixation. Planta 175, 184–192.
| Crossref | GoogleScholarGoogle Scholar |
Osmond, CB ,
Popp, M ,
and
Robinson, SA (1996). Stoichiometric nightmares: studies of photosynthetic O2 and CO2 exchange in CAM plants. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 19–30. (Springer-Verlag: Berlin)
Osmond, CB ,
Maxwell, K ,
Popp, M ,
and
Robinson, S (1999). On being thick: fathoming apparently futile pathways of photosynthesis and carbohydrate metabolism in succulent CAM plants. In ‘Plant carbohydrate biochemistry’. pp. 183–200. (BIOS Scientific Publishers: Oxford)
Pajor AM
(2000) Molecular properties of sodium / dicarboxylate cotransporters. Journal of Membrane Biology 175, 1–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pajor AM, Sun N
(1999) Protein kinase C-mediated regulation of the renal Na+ / dicarboxylate cotransporter, NaDC-1. Biochimica et Biophysica Acta 1420, 223–230.
| PubMed |
Pantoja O, Smith JAC
(2002) Sensitivity of the plant vacuolar malate channel to pH, Ca2+ and anion-channel blockers. Journal of Membrane Biology 186, 31–42.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Paul MJ,
Loos K,
Stitt M, Ziegler P
(1993) Starch-degrading enzymes during the induction of CAM in Mesembryanthemum crystallinum.
Plant, Cell and Environment 16, 531–538.
Picault N,
Hodges M,
Palmieri L, Palmieri F
(2004) The growing family of mitochondrial carriers in Arabidopsis.
Trends in Plant Science 9, 138–146.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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, 238–247.
Pucher GW,
Vickery HB,
Abrahams MD, Leavenworth CS
(1949) Studies in the metabolism of crassulacean plants: diurna1 variations of organic acids and starch in excised leaves of Bryophyllum calycinum.
Plant Physiology 24, 610–620.
Quick PW,
Scheibe R, Neuhaus HE
(1995) Induction of hexose-phosphate translocator activity in spinach chloroplasts. Plant Physiology 109, 113–121.
| PubMed |
Ratajczak R,
Richter J, Lüttge U
(1994) Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3–CAM transition and plant age. Plant, Cell and Environment 17, 1101–1112.
Raghavendra AS, Padmasree K
(2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends in Plant Science 8, 546–553.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roberts A,
Borland AM,
Maxwell K, Griffiths H
(1998) Ecophysiology of the C3–CAM intermediate Clusia minor L. in Trinidad: seasonal and short-term photosynthetic characteristics of sun and shade leaves. Journal of Experimental Botany 49, 1563–1573.
| Crossref | GoogleScholarGoogle Scholar |
Robinson SA,
Yakir D,
Ribascarbo M,
Giles L,
Osmond CB,
Siedow JN, Berry JA
(1992) Measurements of the engagement of cyanide-resistant respiration in the crassulacean acid metabolism plant Kalanchoë daigremontiana with the use of online oxygen isotope discrimination. Plant Physiology 100, 1087–1091.
Robinson SA,
Osmond CB, Giles L
(1993) Interpretations of gradients in δ13C value in thick photosynthetic tissues of plants with crassulacean acid metabolism. Planta 190, 271–276.
| Crossref | GoogleScholarGoogle Scholar |
Rockel B,
Ratajczak R,
Becker A, Lüttge U
(1994) Changed densities and diameters of intra-membrane tonoplast particles of Mesembryanthemum crystallinum in correlation with NaCl-induced CAM. Journal of Plant Physiology 143, 318–324.
Rona J-P,
Pitman MG,
Lüttge U, Ball E
(1980) Electrochemical data on compartmentation into cell wall, cytoplasm, and vacuole of leaf cells in the CAM genus Kalanchoë.
Journal of Membrane Biology 57, 25–35.
Rustin P, Queiroz-Claret C
(1985) Changes in oxidative properties of Kalanchoe blossfeldiana leaf mitochondria during development of crassulacean acid metabolism. Planta 164, 415–422.
| Crossref | GoogleScholarGoogle Scholar |
Rustin P, Lance C
(1986) Malate metabolism in leaf mitochondria from the crassulacean acid metabolism plant Kalanchoë blossfeldiana Poelln. Plant Physiology 81, 1039–1043.
Saitou K,
Agata W,
Masui Y,
Asakura M, Kubota F
(1994) Isoforms of NADP-malic enzyme from Mesembryanthemum crystallinum L. that are involved in C3 photosynthesis and crassulacean acid metabolism. Plant and Cell Physiology 35, 1165–1171.
Saltman P,
Kunitake G,
Spolter H, Stitt C
(1956) The dark fixation of CO2 by succulent leaves: the first products. Plant Physiology 31, 464–468.
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 Physiology 23, 38–69.
Smith FA, Raven JA
(1979) Intracellular pH and its regulation. Annual Review of Plant Physiology 30, 289–311.
| Crossref | GoogleScholarGoogle Scholar |
Smith JAC, Heuer S
(1981) Determination of the volume of intercellular spaces in leaves and some values for CAM plants. Annals of Botany 48, 915–917.
Smith, JAC ,
and
Bryce, JH (1992). Metabolic compartmentation and transport in CAM plants. In ‘Plant organelles: compartmentation of metabolism in photosynthetic cells’. pp. 141–167. (Cambridge University Press: Cambridge, UK)
Smith, JAC ,
and
Winter, K (1996). Taxonomic distribution of crassulacean acid metabolism. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 427–436. (Springer-Verlag: Berlin)
Smith JAC,
Marigo G,
Lüttge U, Ball E
(1982) Adenine nucleotide levels during crassulacean acid metabolism and the energetics of malate accumulation in Kalanchoë tubiflora.
Plant Science Letters 26, 13–22.
| Crossref | GoogleScholarGoogle Scholar |
Smith, JAC ,
Ingram, J ,
Tsiantis, MS ,
Barkla, BJ ,
Bartholomew, DM ,
Bettey, M ,
Pantoja, O ,
and
Pennington, AJ (1996). Transport across the vacuolar membrane in CAM plants. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 53–71. (Springer-Verlag: Berlin)
Spalding MH,
Arron GP, Edwards GE
(1980) Malate decarboxylation in isolated mitochondria from the crassulacean acid metabolism plant Sedum praealtum.
Archives of Biochemistry and Biophysics 199, 448–456.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Steudle E,
Smith JAC, Lüttge U
(1980) Water-relation parameters of individual mesophyll cells of the crassulacean acid metabolism plant Kalanchoë daigremontiana.
Plant Physiology 66, 1155–1163.
Struve I,
Weber A,
Lüttge U,
Ball E, Smith JAC
(1985) Increased vacuolar ATPase activity correlated with crassulacean acid metabolism induction in Mesembryanthemum crystallinum and Kalanchoë blossfeldiana cultivar Tom Thumb. Journal of Plant Physiology 117, 451–468.
Sutton BG
(1975a) The path of carbon in CAM plants at night. Australian Journal of Plant Physiology 2, 377–387.
Sutton BG
(1975b) Glycolysis in CAM plants. Australian Journal of Plant Physiology 2, 389–402.
Taniguchi M,
Taniguchi Y,
Kawasaki M,
Takeda S,
Kato T,
Sato S,
Tabata S,
Miyaki H, Sugiyama T
(2002) Identifying and characterizing plastidic 2-oxoglutarate / malate and dicarboxylate transporters in Arabidopsis thaliana.
Plant and Cell Physiology 43, 706–717.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taniguchi Y,
Nagasaki J,
Kawasaki M,
Miyaki H,
Sugiyama T, Taniguchi M
(2004) Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize. Plant and Cell Physiology 45, 187–200.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tsiantis MS,
Bartholomew DM, Smith JAC
(1996) Salt regulation of transcript levels for the c subunit of a leaf vacuolar H+–ATPase in the halophyte Mesembryanthemum crystallinum.
The Plant Journal 9, 729–736.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tsuzuki M,
Miyachi S,
Winter K, Edwards GE
(1982) Localization of carbonic anhydrase EC-4.2.1.1 in crassulacean acid metabolism plants. Plant Science Letters 24, 211–218.
| Crossref | GoogleScholarGoogle Scholar |
Taybi T,
Cushman JC, Borland AM
(2002) Environmental, hormonal and circadian regulation of crassulacean acid metabolism expression. Functional Plant Biology 29, 669–678.
| Crossref | GoogleScholarGoogle Scholar |
Teeri JA,
Tonsor SJ, Turner M
(1981) Leaf thickness and carbon isotope discrimination in the crassulaceae. Oecologia 50, 367–369.
| Crossref | GoogleScholarGoogle Scholar |
Ting IP, Osmond CB
(1973) Activation of plant P-enolpyruvate carboxylases by glucose-6-phosphate. A particular role in crassulacean acid metabolism. Plant Science Letters 1, 123–128.
| Crossref | GoogleScholarGoogle Scholar |
Verbücheln, O ,
and
Steup, M (1984). Carbon metabolism and malate formation in the CAM plant Aloë arborescens. In ‘Advances in photosynthesis research. Vol. 3’. pp. 421–424. (Martinus Nijhoff: The Hague)
Wagner W, Wiemken A
(1986) Properties and subcellular localization of fructan hydrolase in the leaves of barley Hordeum vulgare cultivar Gerbel. Journal of Plant Physiology 123, 429–440.
Walker RP, Leegood RC
(1996) Phosphorylation of phosphoenolpyruvate carboxykinase in plants: studies in plants with C4 photosynthesis and with crassulacean acid metabolism and in germinating seeds. The Biochemical Journal 317, 653–658.
| PubMed |
Walker RP, Chen ZH
(2002) Phosphoenolpyruvate carboxykinase: structure, function and regulation. Advances in Botanical Research 38, 93–189.
Ward JL,
Harris C,
Lewis J, Beale MH
(2003) Assessment of 1H NMR spectroscopy and multivariate analysis as a technique for metabolite fingerprinting of Arabidopsis thaliana.
Phytochemistry 62, 949–957.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
White PJ, Smith JAC
(1989) Proton and anion transport at the tonoplast in crassulacean-acid-metabolism plants: specificity of the malate-influx system in Kalanchoë daigremontiana.
Planta 179, 265–274.
| Crossref | GoogleScholarGoogle Scholar |
White PJ,
Marshall J, Smith JAC
(1990) Substrate kinetics of the tonoplast H+-translocating inorganic pyrophosphatase and its activation by free Mg2+. Plant Physiology 93, 1063–1070.
Winter K
(1982) Properties of phosphoenolpyruvate carboxylase EC-4.1.1.31 in rapidly prepared desalted leaf extracts of the crassulacean acid metabolism plant Mesembryanthemum crystallinum.
Planta 154, 298–308.
| Crossref | GoogleScholarGoogle Scholar |
Winter, K (1985). Crassulacean acid metabolism. In ‘Photosynthetic mechanisms and the environment’. pp. 329–387. (Elsevier: Amsterdam)
Winter, K ,
and
Smith, JAC (1996a). An introduction to crassulacean acid metabolism. Biochemical principles and ecological diversity. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. a. pp. 1–13. (Springer-Verlag: Berlin)
Winter, K ,
and
Smith, JAC (1996b). Crassulacean acid metabolism: current status and perspectives. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. b. pp. 389–426. (Springer-Verlag: Berlin)
Winter K, Holtum JAM
(2002) How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129, 1843–1851.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Winter K,
Foster JG,
Edwards GE, Holtum JAM
(1982) Intracellular localization of enzymes of carbon metabolism in Mesembryanthemum crystallinum exhibiting C3 photosynthesis characteristics or performing crassulacean acid metabolism. Plant Physiology 69, 300–307.
Winter K,
Wallace BJ,
Stocker GC, Roksandic Z
(1983) Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57, 129–141.
| Crossref | GoogleScholarGoogle Scholar |
Winter K,
Arron GP, Edwards GE
(1986) Malate decarboxylation by mitochondria of the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum.
Plant and Cell Physiology 27, 1533–1540.
Wiskich JT, Day DA
(1982) Malate oxidation, rotenone-resistance, and alternative path activity in plant mitochondria. Plant Physiology 70, 959–964.
Wissing F, Smith JAC
(2000) Vacuolar chloride transport in Mesembryanthemum crystallinum L. measured using the fluorescent dye lucigenin. Journal of Membrane Biology 177, 199–208.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
