biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 51:86-92, 2007 | DOI: 10.1007/s10535-007-0018-8

Superoxide dismutase activity in C3 and C3/CAM intermediate species of Clusia

Z. Miszalski1,2,*, A. Kornas1, K. Gawronska1, I. ¦lesak2, E. Niewiadomska2, J. Kruk3, A. L. Christian4, E. Fischer-Schliebs4, R. Krisch4, U. Lüttge4
1 Institute of Biology, Pedagogical University, Krakow, Poland
2 Institute of Plant Physiology, Polish Academy of Sciences, Krakow, Poland
3 Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland
4 Institute of Botany, Darmstadt University of Technology, Darmstadt, Germany

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.

Keywords: Crassulacean acid metabolism; oxidative stress; stomata
Subjects: antheraxanthin; antioxidants, antioxidant enzymes; carotenoids; Clusia minor; Clusia multiflora; Crassulacean acid metabolism; cytochrome c oxidase; cytokinins; dithiothreitol; drought stress and tolerance; ethylenediaminetetraacetic acid; mitochondria; phosphoenolpyruvate carboxylase; photon flux density (PPFD, PFD); reactive oxygen species (ROS); stomatal conductance; superoxide dismutase (SOD); tricarboxylic acid cycle; xanthophyll cycle

Received: March 31, 2005; Accepted: June 6, 2006; Published: March 1, 2007  Show citation

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Miszalski, Z., Kornas, A., Gawronska, K., ¦lesak, I., Niewiadomska, E., Kruk, J., ... Lüttge, U. (2007). Superoxide dismutase activity in C3 and C3/CAM intermediate species of Clusia. Biologia plantarum, 51(1), 86-92. doi: 10.1007/s10535-007-0018-8
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    References

    1. 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. Go to original source...
    2. Bartosz, G.: Oxidative stress in plants.-Acta Physiol. Plant. 19: 47-64, 1997. Go to original source...
    3. Beauchamp, C., Fridovich, I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.-Anal. Biochem. 44: 276-287, 1971. Go to original source...
    4. 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. Go to original source...
    5. 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. Go to original source...
    6. 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. Go to original source...
    7. 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. Go to original source...
    8. 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. Go to original source...
    9. 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. Go to original source...
    10. 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. Go to original source...
    11. 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. Go to original source...
    12. 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. Go to original source...
    13. 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. Go to original source...
    14. 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. Go to original source...
    15. 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. Go to original source...
    16. 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. Go to original source...
    17. Halliwell, B., Gutteridge, J.M.C.: Free Radicals in Biology and Medicine.-Clarendon Press, Oxford 1999.
    18. 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. Go to original source...
    19. 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. Go to original source...
    20. 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. Go to original source...
    21. 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. Go to original source...
    22. Inzé, D., Van Montagu, M.: Oxidative stress in plants.-Curr. Opin. Biotechnol. 6: 153-158, 1995. Go to original source...
    23. 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. Go to original source...
    24. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head bacteriophage T4.-Nature 227: 680-685, 1970. Go to original source...
    25. 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. Go to original source...
    26. 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. Go to original source...
    27. Lüttge, U.: Light-stress and crassulacean acid metabolism.-Phyton (Austria) 40: 65-82, 2000. Go to original source...
    28. Lüttge, U.: CO2-concentrating: consequences in crassulacean acid metabolism.-J. exp. Bot. 53: 2131-2142, 2002. Go to original source...
    29. 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. Go to original source...
    30. 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. Go to original source...
    31. 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. Go to original source...
    32. Miszalski, Z., Niewiadomska, E., ¦lesak, 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. Go to original source...
    33. Miszalski, Z., ¦lesak, 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. Go to original source...
    34. Mittler, R.: Oxidative stress, antioxidative stress tolerance.-Trends Plant Sci. 7: 405-410, 2002. Go to original source...
    35. 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.
    36. 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.
    37. Niewiadomska, E., Karpinska, B., Romanowska, E., ¦lesak, 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. Go to original source...
    38. Niewiadomska, E., Miszalski, Z., ¦lesak, I., Ratajczak, R.: Catalase activity during C3-CAM transition in Mesembryanthemum crystallinum L. leaves.-Free Radical Res. 31: S251-256, 1999. Go to original source...
    39. 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. Go to original source...
    40. Olivares, E., Faist, K., Kluge, M., Lüttge, U.: 14CO2 pulse-chase labelling in Clusia minor L.-J. exp. Bot. 45: 1527-1533, 1993. Go to original source...
    41. Olszyk, D.M., Bytnerowicz, A., Fox, C.A.: Sulfur dioxide effects on plants exhibiting Crassulacean acid metabolism.-Environ. Pollut. 43: 47-62, 1987. Go to original source...
    42. Osmond, C.B.: Crassulacean acid metabolism: a curiosity in context.-Annu. Rev. Plant Physiol. 29: 379-414, 1978. Go to original source...
    43. 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.
    44. 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. Go to original source...
    45. Scandalios, J.G.: Oxygen stress and superoxide dismutases.-Plant Physiol. 101: 7-12, 1993. Go to original source...
    46. ¦lesak, 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. Go to original source...
    47. ¦lesak, 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. Go to original source...
    48. 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. Go to original source...
    49. Thayer, S.S., Björkman, O.: Leaf xanthophylls content and composition in sun and shade determinated by HPLC.-Photosynth. Res. 23: 331-343, 1990. Go to original source...
    50. Van Lis, R., Atteia, A.: Control of mitochondrial function via photosynthetic redox signals.-Photosynth. Res. 79:133-148, 2004. Go to original source...
    51. 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. Go to original source...

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