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DOI: 10.1055/s-2001-11743
The Effect of Irradiance on Carboxylating/Decarboxylating Enzymes and Fumarase Activities in Mesembryanthemum crystallinum L. Exposed to Salinity Stress
Publication History
July 3, 2000
October 27, 2000
Publication Date:
31 December 2001 (online)
Abstract
In Mesembryanthemum crystallinum plants, treated for 9 days with 0.4 M NaCl at low light intensities (80 - 90 or 95 - 100 μE m-2 s-1; λ = 400 - 700 nm), no day/night malate level differences (Δmalate) were detected. At high light (385 - 400 μE m-2 s-1) strong stimulation of PEPC activity, accompanied by a Δmalate of 11.3 mM, demonstrated the presence of CAM metabolism. This indicates that, to evolve day/night differences in malate concentration, high light is required. Salt treatment at low light induces and increases the activity of NAD- and NADP-malic enzymes by as much as 3.7- and 3.9-fold, while at high light these values reach 6.4- and 17.7-fold, respectively. The induction of activity of both malic enzymes and PEPC (phospoenolpyruvate carboxylase) take place before Δmalate is detectable. An increase in SOD (superoxide dismutase) was observed in plants cultivated at high light in both control and salt-treated plants. However, in salt-treated plants this effect was more pronounced. Carboxylating and decarboxylating enzymes seem to be induced by a combination of different signals, i.e., salt and light intensity. Plants performing CAM, after the decrease of activity of both the decarboxylating enzymes at the beginning of the light period, showed an increase in these enzymes in darkness when the malate pool reaches higher levels. In CAM plants the activity of fumarase (Krebs cycle) is much lower than that in C3 plants. The role of mitochondria in CAM plants is discussed.
Abbreviations
BICINE: (N,N-bis[2-hydroxyethyl]glycine)
BSA: bovine serum albumin
CAM: Crassulacean acid metabolism
DTT: dithiothreitol
EDTA: ethylenediaminetetraacetic acid
HEPES: N-(2-hydroxyethyl)piperazine-N′-(ethanesulfonic acid)
Δmalate: difference of cell sap malate concentration after the night and after the day
MES: [N-morpholino]ethanesulfonic acid
MDH: malate dehydrogenase (EC 1.1.1.37)
NAD-ME: NAD-malic enzyme (EC 1.1.1.38)
NADP-ME: NADP-malic enzyme (EC 1.1.1.40)
NBT: nitroblue tetrazolium
PAGE: polyacrylamide gel electrophoresis
PEP: phosphoenolpyruvate
PEPC: phosphoenolpyruvate carboxylase (EC 4.1.1.31)
PEPCK: phosphoenolpyruvate carboxykinase (EC 4.1.1.32)
PVP: polyvinylpyrrolidone
SOD: superoxide dismutase (E.C 1.15.1.1)
TEMED: N,N,N′,N′-tetramethyl-ethylenediamine
Tris: Tris(hydroxymethyl)aminomethane
Tricine: N-Tris(hydroxymethyl)-methylglycine
Key words
C3 photosynthesis - Crassulacean acid metabolism (CAM) - fumarase - Mesembryanthemum crystallinum - mitochondria - NAD-malic enzyme - NADP-malic enzyme
References
- 01 Beauchamp, Ch., and Fridovich, I.. (1971); Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal. Biochem.. 44 276-287
- 02 Bradford, M. M.. (1976); A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.. 72 248-254
- 03 Brulfert, J.,, Kluge, M.,, Güçlü, S.,, and Queiroz, O.. (1988); Interaction of photoperiod and drought as CAM inducing factors in Kalanchoë blossfeldiana Poelln., cv. Tom Thumb. J. Plant Physiol.. 133 222-227
- 04 Buchanan-Bollig, I. C., and Smith, J. A. C.. (1984); Circadian rhythms in crassulacean acid metabolism: Phase relationship between gas exchange, leaf water relations and malate metabolism in Kalanchoë daigremontiana. . Planta. 161 314-319
- 05 Chu, C.,, Dai, Z.,, Ku, M. S. B.,, and Edwards, G. E.. (1990); Induction of crassulacean acid metabolism in the facultative halophyte Mesembranthemum crystallinum by abscisic acid. Plant Physiol.. 93 1253-1260
- 06 Cushman, J. C.. (1992); Characterization and expression of a NADP-malic enzyme cDNA induced by salt stress from the facultative crassulacean acid metabolism plant, Mesembryanthemum crystallinum. . Eur. J. Biochem.. 208 259-266
- 07 Cushman, J. C., and Bohnert, H. J.. (1997); Molecular genetics of crassulacean acid metabolism. Plant Physiol.. 113 667-676
- 08 Cushman, J. C.,, Michalowski, C. B.,, and Bohnert, H. J.. (1990); Developmental control of crassulacean acid metabolism inducibility by salt stress in the common ice plant. Plant Physiol.. 94 1137-1142
- 09 Dai, Z.,, Ku, M. S. B.,, Zhang, D.,, and Edwards, G. E.. (1994); Effects of growth regulators on the induction of crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum. . Planta. 192 287-294
- 10 Dittrich, P.. (1976); Nicotinamide adenine dinucleotide-specific “malic” enzyme in Kalanchoë daigremontiana and other plants exhibiting Crassulacean acid metabolism. Plant Physiol.. 57 310-314
-
11 Dittrich, P.. (1979)
Enzymes of Crassulacean acid metabolism. Photosynthesis II. Photosynthetic carbon metabolism and related processes. Encyclopedia of Plant Physiology, New sereies, Vol. 6. Gibbs, M. and Latzko, E., eds. Berlin, Heildelberg, New York; Springer-Verlag pp. 263-270 - 12 Drake, B. G.,, Azcon-Bieto, J.,, Berry, J.,, Bunce, J.,, Dijkstra, P.,, Farrar, J.,, Gifford, R. M.,, Gonzalez-Meler, M. A.,, Koch, G.,, Lambers, H.,, Siedow, J.,, and Wullschleger, S.. (1999); Does elevated atmospheric CO2 concentration inhibit mitochondrial respiration in green plants?. Plant Cell and Environm.. 22 649-657
- 13 Drincovich, M. F.,, Casati, P.,, Andreo, C. S.,, Donahue, R.,, and Edwards, G. E.. (1998); UV-B induction of NADP-malic enzyme in etiolated and green maize seedlings. Plant Cell Environm.. 21 63-70
- 14 Holtum, J. A. M., and Winter, K.. (1982); Activity of enzymes of carbon metabolism during the induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum L. Planta. 155 8-16
- 15 Jiao, J., and Chollet, R.. (1991); Posttranslational regulation of phosphoenolpyruvate carboxylase in C4 and crassulacean acid metabolism plants. Plant Physiol.. 95 981-985
- 16 Kluge, M.. (1968); Untersuchungen über den Gaswechsel von Bryophyllum während der Lichtperiode II. Beziehungen zwischen dem Malatgehalt des Blattgewebes und der CO2-Aufnahme. Planta. 80 359-377
-
17 Kluge, M.. (1976)
Models of CAM regulation. CO2 regulation and plant productivity. Burris, R. H. and Black, C. C., eds. Baltimore, London, Tokio; University Park Press pp. 205-215 - 18 Kluge, M., and Ting, I. P.. (1978) Crassulacean acid metabolism. Analysis of an ecological adaptation. Berlin, Heidelberg, New York; Springer Verlag
- 19 Kore-eda, S.,, Yamashita, T.,, and Kanai, R.. (1996); Induction of light dependent pyruvate transport into chloroplasts of Mesembryanthemum crystallinum by salt stress. Plant Cell Physiol.. 37 257-262
- 20 Krömer, S.. (1995); Respiration during photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol.. 46 45-70
- 21 Laemmli, U. K.. (1970); Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227 680-685
- 22 Lüttge, U.. (1993); The role of crassulacean acid metabolis (CAM) in adaptation of plants to salinity. New Phytol.. 125 59-71
- 23 McElwain, E. F.,, Bohnert, H. J.,, and Thomas, J. C.. (1992); Light mediates the induction of phosphoenolpyruvate carboxylase by NaCl and abscisic acid in Mesembryanthemum crystallinum. . Plant Physiol.. 99 1261-1264
- 24 Miszalski, Z.,, Slesak, I.,, Niewiadomska, E.,, Baczek-Kwinta, R.,, Lüttge, U.,, and Ratajczak, R.. (1998); Subcellular localization and stress responses of superoxide dismutase isoforms from leaves in the C3-CAM intermediate halophyte Mesembryanthemum crystallinum L. Plant Cell Environm.. 21 169-179
-
25 Möllering, H.. (1985)
L-(-)Malate. Methods of enzymatic analysis, Vol. 7. Bergmeyer, H. U., ed. Weinheim; VHC Verlagsgesellschaft pp. 39-47 - 26 Nelson, T., and Langdale, J. A.. (1992); Developmental genetics of C4 photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol.. 98 558-564
- 27 Nimmo, H. G.. (2000); The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science. 5 75-80
- 28 Nobel, P. S.. (1988) Environmental biology of agaves and cacti. Cambridge; Cambridge University Press
- 29 Pierre, J. N., and Queiroz, O.. (1978); Regulation of glycolysis and level of the Crassulacean acid metabolism. Planta. 144 143-151
- 30 Racker, E.. (1950); Spectrophotometric measurement of the enzymatic formation of fumaric and cis acitonic acids. Biochim. Biophys. Acta. 4 211-214
- 31 Saitou, K.,, Agata, W.,, Masui, Y.,, Asakura, M.,, and Kubota, F.. (1994); Isoforms of NADP-malic enzyme from Mesembryanthemum crystallinum L. that are involved in C3 photosynthesis and Crassulacean acid metabolism. Plant Cell Physiol.. 35 1165-1171
- 32 Scheibe, R.. (1991); Redox-modulation of chloroplast enzymes. Plant Physiol.. 96 1-3
- 33 Spalding, M. H.,, Schmitt, M. R.,, Ku, S. B.,, and Edwards, G. E.. (1979); Intracellular localization of some key enzymes of Crassulacean acid metabolism in Sedum praealtum. . Plant Physiol.. 63 738-743
- 34 Sweeney, B. M.. (1987) Rhythmic phenomena in plants. Academic Press Inc. pp. 27-96
-
35 Veen, B. W.. (1980)
Energy cost of ion transport. Engineering of Osmoregulation. Impact on Plant Productivity for Food, Chemicals and Energy. Basic Life Science. Rains, D. W., Valentine, R. C., and Hollaeder, A., eds. London; Plenum Press pp. 187-195 - 36 Volin, J. C., and Reich, P. B.. (1996); Interaction of elevated CO2 and O3 in growth, photosynthesis and respiration of three perennial species grown at low and high nitrogen. Physiol. Plant.. 97 674-684
- 37 Winter, K.,, Arron, G.,, and Edwards, G. E.. (1986); Malate decarboxylation by mitochondria of the inducible Crassulacean acid metabolism plant Mesembryanthemum crystallinum. . Plant Cell Physiol.. 27 1533-1539
- 38 Winter, K.,, Foster, J. G.,, Edwards, G. E.,, and Holtum, J. A. M.. (1982); Intracellular localization of enzymes of carbon metabolism in Mesembryanthemum crystallinum exhibiting C3 photosynthetic characteristics or performing crassulacean acid metabolism. Plant Physiol.. 69 300-307
-
39 Winter, K., and Smith, J. A. C.. (1996)
Crassulacean acid metabolism. Current status and perspectives. Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution. Winter, K. and Smith, J. A. C., eds. Berlin; Springer Verlag pp. 389-426
Z. Miszalski
Polish Academy of Sciences
Department of Plant Physiology
Slawkowska 17
31-016 Cracow
Poland
Email: z. miszalski@zfr.pan.krakow.pl
Section Editor: H. Rennenberg