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Photosynthesis Research

, Volume 62, Issue 2, pp 165–174 | Cite as

The effect of copper on chlorophyll organization during greening of barley leaves

  • Varda Caspi
  • Magdolna Droppa
  • Gábor Horváth
  • Shmuel Malkin
  • Jonathan B. MarderEmail author
  • Victor I. Raskin
Article

Abstract

The effect of copper on chlorophyll organization and function during greening of barley was examined, using chlorophyll fluorescence and photoacoustic techniques. Copper was found to inhibit pigment accumulation and to retard chlorophyll integration into the photosystems, as evident from low temperature (77 K) fluorescence spectra. Resolution of the minimal fluorescence (F0) into active and inactive parts, indicated a higher inactive fraction with copper treatment. This was attributed to chlorophyll molecules which failed to integrate normally, a conclusion supported by the longer fluorescence lifetime observed in copper treated plants. A lower ratio of chlorophyll a to b and fluorescence induction transients, showing accelerated Photosystem II closure, both indicate that copper treatment resulted in a larger light-harvesting antenna. Another effect of copper treatment was the suppression of oxygen evolution, indicating a decrease in photosynthetic capacity. We suggest that the non-integrated chlorophyll fraction sensitizes photodamage in the membrane, contributing to disruption of electron flow and pigment accumulation.

chlorophyll fluorescence oxygen evolution photoacoustic photodamage Photosystem II 

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References

  1. Abo-Foul S, Raskin VI, Sztejnberg A and Marder JB (1996) Disruption of chlorophyll organization and function in powdery mildew diseased cucumber leaves and its control by the hyperparasite Ampelomyces quisqualis. Phytopathology 86: 195–199Google Scholar
  2. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1–15Google Scholar
  3. Barón M, Arellano JB and Gorge JL (1995) Copper and Photosystem II: A controversial relationship. Physiol Plant 94: 174–180Google Scholar
  4. Baszynski T, Krül M, Krupa Z, Ruszkowska M, Wojcieska U and Wolinska D (1982) Photosynthetic apparatus of spinach exposed to excess copper. Z Pflanzenphysiol 108: 385–395Google Scholar
  5. Baszynski T, Tukendorf A, Skorzynska E and Maksymiec W(1988) Characteristics of the photosynthetic apparatus of copper nontolerant spinach exposed to excess copper. J Plant Physiol 132: 708–713Google Scholar
  6. Björkman O and Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristic at 77 K among vascular plants of diverse origins. Planta 170: 489–504CrossRefGoogle Scholar
  7. Boddi B, Ryberg M and Sundqvist C (1991) The formation of shortwavelength chlorophyllide form at partial phototrransformation of protochlorophyllide in etioplast inner membranes. Photochem. Photobiol. 53: 667–673Google Scholar
  8. Bolhár-Nordenkampf HR, Öquist G (1993) Chlorophyll fluorescence as a tool in photosynthesis research. In: Hall DO, Scurlock JMO, Bolhár-Nordenkampf HR, Leegood RC and Long SP (eds) Photosynthesis and Production in a Changing Environment, pp 193–206. Chapman & Hall, LondonGoogle Scholar
  9. Bults G, Horowitz BA, Malkin S and Cahen D (1982) Photoacoustic measurements of photosynthetic activities in whole leaves photochemistry and gas exchange. Biochem Biophys Acta 679: 452–465Google Scholar
  10. Cook CM, Kostidou A, Vardaka E and Lanaras T (1997) Effects of copper on the growth, photosynthesis and nutrient concentrations of Phaseolus plants. Photosynthetica 34: 179–193Google Scholar
  11. Dau H (1994) Molecular mechanisms and quantitative models of variable Photosystem II fluorescence. Photochem Photobiol 60: 1–23Google Scholar
  12. Davies BH (1976) Cartenoid pigments. In: Goodwin TW (ed) Chemistry and Biochemistry of Plant Pigments, Vol 2, pp 38–155. Academic Press, New YorkGoogle Scholar
  13. Droppa M and Horváth G (1990) The role of copper in photosynthesis. CRC Plant Sci 9: 111–123Google Scholar
  14. Garab GI, Horváth G and Faludi-Dániel Á (1974) Resolution of the fluorescence bands in greening maize. Biochem Biophys Res Commun 56: 1004–1009PubMedGoogle Scholar
  15. Geacintov NE and Breton J (1987) Energy transfer and fluorescence mechanism in photosynthetic membranes. CRC Crit Rev Plant Sci. 5: 1–44Google Scholar
  16. Govindjee (1995) Sixty three years since Kautsky: Chlorophyll a fluorescence. Aust J Plant Physiol 22: 131–160Google Scholar
  17. Hamouri B, Brouers M and Sironval C (1981) Pathways from photoinactive P633–628 protochlorophyllide to the P696-682 chlorophyllide in cucumber etioplast suspensions. Plant Sci Lett 21: 375–379Google Scholar
  18. Horváth G, Arellano JB, Droppa M and Barón M (1998) Alterations in Photosystem II electron transport as revealed by thermoluminescence of Cu-poisoned chloroplasts. Photosynth Res 57: 175–181Google Scholar
  19. Horváth g, Droppa M, Oravecz Á, Raskin VI and Marder JB (1996) Formation of the photosynthetic apparatus during greening of cadmium-poisoned barley leaves. Planta 199: 238–243Google Scholar
  20. Huner NPA, Oquist G and Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3: 224–230Google Scholar
  21. Krause GH and Weiss E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313–349CrossRefGoogle Scholar
  22. Lichtenthaler HK, Rinderle U (1988) The role of chlorophyll fluorescence in the detection of stress conditions in plants. Crit Rev Anal Chem 19: S29–S85Google Scholar
  23. Malkin S and Canaani O (1994) The use and the characteristics of the photoacoustic method in the study of photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45: 493–526Google Scholar
  24. Malkin S and Kok B (1966) Fluorescence induction studies in isolated chloroplasts I. Number of components involved in the reaction and quantum yields. Biochim Biophys Acta 126: 413–432.PubMedGoogle Scholar
  25. Marder JB and Raskin VI (1993) The assembly of chlorophyll into pigment-protein complexes. Photosynthetica 28: 243–248Google Scholar
  26. Marder JB, Caspi V and Raskin VI (1995) Free chlorophyll effects on variable fluorescence. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol III, pp. 305–308. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  27. Marder JB, Droppa M, Caspi V, Raskin VI and Horváth G (1998) Light-independent thermoluminescence from thylakoids of greening barley leaves. Evidence for involvement of oxygen radicals and free chlorophyll. Physiol Plant 104: 713–719Google Scholar
  28. Moran R (1982) Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiol 69: 1376–1381Google Scholar
  29. Ouzounidou G, Moustakas M and Lannoye R (1995) Chlorophyll fluorescence and photoacoustic characteristics in relation to changes in chlorophyll and Ca2+ content of a Cu-tolerant Silene compacta ecotype under Cu treatment. Physiol Plant 93: 551–557Google Scholar
  30. Ouzounidou G, Moustakas M and Strasser RJ (1997) Sites of action of copper in the photosynthetic apparatus of maize leaves: Kinetic analysis of chlorophyll fluorescence, oxygen evolution, absorption changes and thermal dissipation as monitored by photoacoustic signals. Aust J Plant Physiol 24: 81–90Google Scholar
  31. Pätsikkä E, Aro E-M and Tyystjärvi E (1988) Increase in the quantum yield of photoinhibition contributes to copper toxicity in vivo. Plant Physiol 117: 619–627Google Scholar
  32. Parekh D, Puranik RM and Srivastava HS (1990) Inhibition of chlorophyll biosynthesis by cadmium in greening maize leaf segments. Biochem Physiol Pflanzen 186: 239–242Google Scholar
  33. Poulet P, Cahen D and Malkin S (1983) Photoacoustic detection of photsynthetic oxygen evolution from leaves. Quantitative analysis by phase and amplitude measurements. Biochim. Biophys Acta 724: 433–446Google Scholar
  34. Raskin VI (1981) Protochlorophyllide Photoreduction. Nauka I Technika Publishers, MinskGoogle Scholar
  35. Raskin VI and Kostjukevich YS (1982) Pathways of chlorophyllide spectral forms. Vestsi Acad Nauk BSSR Ser biol 4: 38–41Google Scholar
  36. Raskin VI and Marder JB (1993) How plants limit the photodestructive potential of chlorophyll. In: Yamamoto HY and Smith CM (eds) Photosynthetic Responses to the Environment. Current Topics in Plant Physiology, Vol 8, pp 156–159. American Society of Plant Physiologists, Rockville, MarylandGoogle Scholar
  37. Raskin VI and Marder JB (1997) Chlorophyll organization in darkgrown and light-grown pine (Pinus brutia) and barley (Hordeum vulgare). Physiol Plant 101: 620–626Google Scholar
  38. Ryberg M and Sundqvist C (1988) The regular ultastructure of isolated prolamellar bodies depends on the presence of memebranebound NADPH-protochlorophyllide oxireductase. Physiol Plant 73: 218–226Google Scholar
  39. Sandmann G and Böger P (1980) Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiol 66: 797–800Google Scholar
  40. Spencer RD and Weber G (1969) Measurement of subnanosecond fluorescence lifetimes with a cross-correlation phase fluorometer. Ann NY Acad Sci 158: 361–376Google Scholar
  41. Stiborová M, Doubravová M, Brezinová A and Friedrich A (1986) Effect of heavy metal ions on growth and biochemical characteristics of photosynthesis of barley Hordeum vulgare L. Photosynthetica 20: 418–425Google Scholar
  42. Tuba Z and Csintalan Zs (1992) The effect of pollution on the physiological processes in plants. In: Kovács M, Podoni J, Tuba Z and Turcsányi (eds) Biological Indicators, pp 169–191. Ellis Horwood Ltd Publ, ChichesterGoogle Scholar
  43. Yruela I, Gatzen G, Picorel R and Holzwarth AR (1996a) Cu(II)-Inhibitory effect on Photosystem II from higher plants. A picosecond time-resolved fluorescence study. Biochemistry 35: 9469–9474PubMedGoogle Scholar
  44. Yruela I, Pueyo JJ, Alonso PJ and Picorel R (1996b) Photoinhibition of Photosystem II from higher plants - effect of copper inhibition. J Biol Chem 271: 27408–27415PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Varda Caspi
    • 1
  • Magdolna Droppa
    • 2
  • Gábor Horváth
    • 2
  • Shmuel Malkin
    • 3
  • Jonathan B. Marder
    • 1
    Email author
  • Victor I. Raskin
    • 1
  1. 1.Department of Agricultural BotanyThe Hebrew University of Jerusalem, Faculty of AgricultureRehovotIsrael
  2. 2.Department of Plant PhysiologyUniversity of Horticulture and Food IndustryBudapestHungary
  3. 3.Department of Biological ChemistryThe Weizmann Institute of ScienceRehovotIsrael

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