Abstract
The C3-CAM intermediate Clusia minor L. and the C3 obligate Clusia multiflora H.B.K. plants were exposed for 7 d to a combination of drought stress and high irradiance of about 1200 µmol m−2 s−1 for 12 h per day. In both species under these conditions a strong decrease in stomatal conductance was observed at dawn and dusk. Changes in stomatal behaviour of C. minor were accompanied by only a low nocturnal accumulation of malate and citrate. Thus, in C. minor drought stress applied in combination with high irradiance limited CAM expression, and possibly this is the main reason why C. minor prefers semi-shaded sites in the field. The mitochondrial MnSOD, in both well watered and stressed plants of two species showed strong diurnal oscillations with maximum activity at dusk. These oscillations can be explained by the engagement of mitochondria in dissipation of an excess of reducing equivalents. In plants which are able to carry out CAM metabolism tricarboxylic acid cycle is expected to be down regulated in the dark period to prevent breakdown of the entire malate and citrate.
Similar content being viewed by others
Abbreviations
- A:
-
antheraxanthin
- BSA:
-
bovine serum albumin
- COX:
-
cytochrome c oxidase
- CuZnSOD:
-
CuZn-superoxide dismutase
- DTT:
-
dithiothreitol
- EPS:
-
epoxidation state of the xanthophyll cycle pigments
- gs :
-
stomatal conductance
- H2EDTA:
-
ethylenediaminetetraacetic acid
- HEPES:
-
N-(2-hydroxyethyl)piperazine-N′-(ethanesulphonic acid)
- MnSOD:
-
Mn-superoxide dismutase
- PAGE:
-
polyacrylamide gel electrophoresis
- PEG:
-
polyethylene glycol
- PEPC:
-
phosphoenolpyruvate carboxylase
- PFD:
-
photon flux density
- PVPP:
-
polyvinylpolypyrrolidone
- ROS:
-
reactive oxygen species
- TCA cycle:
-
tricarboxylic acid cycle
- V:
-
violaxanthin
- Z:
-
zeaxanthin
References
Adams III, W.W., Demmig-Adams, B.: Operation of the xanthophylls cycle in higher plants in response to diurnal changes in incident sunlight.-Planta 186: 390–398, 1992.
Bartosz, G.: Oxidative stress in plants.-Acta Physiol. Plant. 19: 47–64, 1997.
Beauchamp, C., Fridovich, I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.-Anal. Biochem. 44: 276–287, 1971.
Borland, A.M., Griffiths, H.: A comparative study on the regulation of C3 and C4 carboxylation processes in the constitutive crassulacean acid metabolism (CAM) plant Kalanchoë daigremontiana and the C3-CAM intermediate species Clusia minor.-Planta 201: 368–378, 1997.
Borland, A.M., Griffiths, H., Broadmeadow, M.S.J., Fordham, M.C., Maxwell, C.: Short term changes in carbon-isotope discrimination in the C3/CAM intermediate Clusia minor L. growing in Trinidad.-Oecologia 95: 444–453, 1993.
Borland, A.M., Griffiths, H., Maxwell, C., Fordham, M.C., Broadmeadow, M.S.J.: CAM induction in Clusia minor L. during the transition from wet to dry season in Trinidad: the role of organic acid speciation and decarboxylation.-Plant Cell Environ. 19: 655–664, 1996.
Borland, A.M., Técsi, L.I., Leegood, R.C., Walker, R.P.: Inducibility of crassulacean acid metabolism (CAM) in Clusia species; physiological/biochemical characterisation and intercellular localisation of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM.-Planta 205: 342–351, 1998.
Bradford, M.M.: A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248–254, 1976.
Broetto, F., Lüttge, U., Ratajczak, R.: Influence of light intensity and salt-treatment on mode of photosynthesis and enzymes of the antioxidative response system of Mesembryanthemum crystallinum.-Funct. Plant Biol. 29: 13–23, 2002.
Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D., Van Breusegem, F.: Dual action of active oxygen species during plant stress responses.-Cell mol. Life Sci. 57: 779–795, 2000.
De Mattos, E.A., Herzog, B., Lüttge, U.: Chlorophyll fluorescence during CAM-phases in Clusia minor L. under drought stress.-J. exp. Bot. 50: 253–261, 1999.
De Mattos, E.A., Lüttge, U.: Chlorophyll fluorescence and organic acid oscillations during transition from CAM to C3-photosynthesis in Clusia minor L. (Clusiaceae).-Ann. Bot. 88: 457–463, 2001.
Demmig-Adams, B., Adams III, W.W.: Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species.-Planta 198: 460–470, 1996.
Dodd, A.N., Griffiths, H., Taybi, T., Cushman, J.C., Borland, A.M.: Integrated diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum.-Planta 216: 789–797, 2002.
Franco, A.C., Ball, E., Lüttge, U.: Patterns of gas exchange and organic acid oscillations in tropical trees of the genus Clusia.-Oecologia 85: 108–114, 1990.
Franco, A.C., Lüttge, U.: Midday depression in savana trees: coordinated adjustments in photochemical efficiency, photorespiration, CO2 assimilation and water use efficiency.-Oecologia 131: 356–365, 2002.
Halliwell, B., Gutteridge, J.M.C.: Free Radicals in Biology and Medicine.-Clarendon Press, Oxford 1999.
Hernández, J.A., Escobar, C., Creissen, G., Mullineaux, P.M.: Antioxidant enzyme induction in pea plants under high irradiance.-Biol. Plant. 50: 395–399, 2006.
Herzog, B., Hoffmann, S., Hartung, W., Lüttge, U.: Comparison of photosynthetic responses of the sympatric tropical C3 species Clusia multiflora H.B.K. and the C3-CAM intermediate species Clusia minor L. to irradiance and drought stress in a phytotron.-Plant Biol. 1: 460–470, 1999.
Holtum, J.A.M., Aranda, J., Virgo, A., Gehrig, H.H., Winter, K.: δ13C values and crassulacean acid metabolism in Clusia species from Panama.-Trees 18: 658–668, 2004.
Hong, H.T.K., Nose, A., Agarie, S., Oxidation of various substrates and effects of the inhibitors on purified mitochondria isolated from Kalanchoë pinnata.-Biol. Plant. 49: 201–208, 2005.
Inzé, D., Van Montagu, M.: Oxidative stress in plants.-Curr. Opin. Biotechnol. 6: 153–158, 1995.
Kato, J., Yamahara, T., Tanaka, K., Takio, S., Satoh, T.: Characterization of catalase from green algae Chlamydomonas reinhardtii.-J. Plant Physiol. 151: 262–268, 1997.
Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head bacteriophage T4.-Nature 227: 680–685, 1970.
Lüttge, U.: Nocturnal citrate accumulation and its response to environmental stress in the CAM plant Kalanchoe pinnata (Lam.) Pers.-Plant Cell Environ. 13: 977–982, 1990.
Lüttge, U.: One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM and C3-CAM intermediate behaviour.-Plant Biol. 1: 138–148, 1999.
Lüttge, U.: Light-stress and crassulacean acid metabolism.-Phyton (Austria) 40: 65–82, 2000.
Lüttge, U.: CO2-concentrating: consequences in crassulacean acid metabolism.-J. exp. Bot. 53: 2131–2142, 2002.
Lüttge, U. Photosynthesis: CAM plants.-In: Thomas, B., Murphy, D.J., Murray, B.G. (ed.): Encyclopedia of Applied Plant Sciences. Pp. 688–704. Academic Press, Oxford 2003.
Maxwell, K., Borland, A.M., Haslam, R.P., Helliker, B.R., Roberts, A., Griffiths, H.: Modulation of Rubisco activity during the diurnal phases of the crassulacean acid metabolism plant Kalanchoe daigremontiana.-Plant Physiol. 121: 849–856, 1999.
Miszalski, Z., Kluge, M., Ziegler, H.: Stimulatory effect of sulphite on photosynthetic 14CO2-fixation in Kalanchoe dagremontiana Hamet et Perier.-J. Plant Physiol. 151: 535–540, 1997.
Miszalski, Z., Niewiadomska, E., Ślesak, I., Lüttge, U., Kluge, M., Ratajczak, R.: The effect of irradiation on carboxylating/decarboxylating enzymes and fumarase activities in Mesembryanthemum crystallinum L., exposed to salinity stress.-Plant Biol. 3: 17–23, 2001.
Miszalski, Z., Ślesak, I., Niewiadomska, E., Baczek-Kwinta, R., Lüttge, U., Ratajczak, R.: Subcellular localization and stress responses of superoxide dismutase isoforms from leaves in the C3-CAM intermediate halophyte Mesembryanthemum crystallinum L.-Plant Cell Environ. 21:169–179, 1998.
Mittler, R.: Oxidative stress, antioxidative stress tolerance.-Trends Plant Sci. 7: 405–410, 2002.
Möllering, H.: Malat: Bestimmung mit Malat-Dehydrogenase und Glutamat-Oxalacetat-Transaminase.-In: Bergmeyer, H.U. (ed.): Methoden der Enzymologie. Pp. 1636–1639. Academic Press, New York 1974.
Möllering, H.: Citrate. Determination with citrate lyase, MDH and LDH.-In: Bergmeyer H.U. (ed.): Methods of Enzymatic Analysis. Pp. 2–12. Academic Press, New York 1985.
Niewiadomska, E., Karpinska, B., Romanowska, E., Ślesak, I., Karpinski, S.: A salinity-induced C3-CAM transition increases energy conservation in the halophyte Mesembryanthemum crystallinum L.-Plant Cell Physiol. 45: 789–794, 2004.
Niewiadomska, E., Miszalski, Z., Ślesak, I., Ratajczak, R.: Catalase activity during C3-CAM transition in Mesembryanthemum crystallinum L. leaves.-Free Radical Res. 31: S251–256, 1999.
Nyman, L.P., Benzing, D.H., Temple, P.J., Arditti, J.: Effects of ozone and sulfur dioxide on two epiphytic orchids.-Environ. exp. Bot. 30, 207–213, 1990.
Olivares, E., Faist, K., Kluge, M., Lüttge, U.: 14CO2 pulse-chase labelling in Clusia minor L.-J. exp. Bot. 45: 1527–1533, 1993.
Olszyk, D.M., Bytnerowicz, A., Fox, C.A.: Sulfur dioxide effects on plants exhibiting Crassulacean acid metabolism.-Environ. Pollut. 43: 47–62, 1987.
Osmond, C.B.: Crassulacean acid metabolism: a curiosity in context.-Annu. Rev. Plant Physiol. 29: 379–414, 1978.
Perl-Treves, R., Perl, A.: Oxidative stress an introduction.-In: Inzé, D., Van Montagu, M. (ed.): Oxidative Stress in Plants. Pp. 1–32. Taylor and Francis, London 2002.
Roberts, A., Borland, A.M., Maxwell, K., Griffiths, H.: Ecophysiology of the C3-CAM intermediate Clusia minor L. in Trinidad: seasonal and short-term photosynthetic characteristics of sun and shade leaves.-J. exp. Bot. 49: 1563–1573, 1998.
Scandalios, J.G.: Oxygen stress and superoxide dismutases.-Plant Physiol. 101: 7–12, 1993.
Ślesak, I., Miszalski, Z.: Superoxide dismutase-like protein from roots of the intermediate C3-CAM plant Mesembryanthemum crystalinum L. in in vitro culture.-Plant Sci. 164: 497–505, 2003.
Ślesak, I., Miszalski, Z., Karpinska, B., Niewiadomska, E., Ratajczak, R., Karpinski, S.: Redox control of oxidative stress responses in the C3-CAM intermediate plant Mesembryanthemum crystallinum.-Plant Physiol. Biochem. 40: 669–677, 2002.
Spalding, M.H., Stumpf, D.K., Ku, M.S.B., Burris, R.H., Edwards, G.E.: Crassulacean acid metabolism and diurnal variations of internal CO2 and O2 concentrations in Sedum praealtum DC.-Aust. J. Plant Physiol. 6: 557–567, 1979.
Thayer, S.S., Björkman, O.: Leaf xanthophylls content and composition in sun and shade determinated by HPLC.-Photosynth. Res. 23: 331–343, 1990.
Van Lis, R., Atteia, A.: Control of mitochondrial function via photosynthetic redox signals.-Photosynth. Res. 79:133–148, 2004.
Volin, J.C., Reich, P.B.: 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, 1996.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Miszalski, Z., Kornas, A., Gawronska, K. et al. Superoxide dismutase activity in C3 and C3/CAM intermediate species of Clusia . Biol Plant 51, 86–92 (2007). https://doi.org/10.1007/s10535-007-0018-8
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10535-007-0018-8