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Singlet molecular oxygen and primary mechanisms of photo-oxidative damage of chloroplasts. Studies based on detection of oxygen and pigment phosphorescence

Published online by Cambridge University Press:  05 December 2011

A. A. Krasnovsky Jr
A. A. Krasnovsky Jr
Affiliation:
Department of Biology, Moscow State University, A.N. Bakh Institute of Biochemistry Russian Academy of Sciences, Moscow, Russia
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Synopsis

Photogeneration of singlet oxygen molecules (1O2), their vibrationally excited state and dimols (1O2)2 has been shown by measuring photosensitised delayed luminescence in pigment-containing media. All singlet oxygen species are formed as a result of energy transfer to O2 from triplet pigment molecules. Monomeric pigment molecules are the most efficient singlet oxygen generators. The 1O2 quantum yields are 40–80% in aerobic solutions of monomeric chlorophylls and pheophytins. Pigment aggregation causes a strong decrease in singlet oxygen production. The 1O2 quantum yield in chloroplasts has been estimated using literature and experimental data on formation of the chlorophyll triplet states in the photosynthetic apparatus. The most probable value is 0.1%. One of the major sources of singlet oxygen is likely to be the triplet states of newly formed pigment molecules which are not quenched by carotenoids and can be detected by measuring low-temperature pigment phosphorescence. Quenching of singlet oxygen by the thylakoid components has been analysed and the 1O2 lifetime estimated. The data suggest that carotenoids and chlorophylls are the most efficient physical 1O2 quenchers and the 1O2 lifetime is about 70 ns in thylakoids. The quantum yield of 1O2-induced pigment photodestruction was estimated to be about 10−6–10−5. This value is close to the quantum yield of chlorophyll photobleaching experimentally observed in aerobic suspensions of isolated chloroplasts. The intensity of pigment phosphorescence at 77 K correlates with the rate of chlorophyll photobleaching in plant materials. The data suggest that 1O2 generation by the pigment triplet states is the most likely reason for chloroplast photodamage. The intensity of pigment phosphorescence can be used as an index of the degree of plant photo-oxidative stress.

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Research Article
Information
Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences , Volume 102: Oxygen and Environmental Stress in Plants , 1994 , pp. 219 - 235
Copyright
Copyright © Royal Society of Edinburgh 1994

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References

Aronson, H., Waggoner, C., More, J. & Berg, S. P. 1983. Spin-label studies of the lipid regions of spinach thylakoids and a detergent derived oxygen-evolving photosystem II preparations. Biochimica and Biophysica Ada 725, 519–28.CrossRefGoogle Scholar
Asada, K. & Takahashi, M. 1987. Production and scavenging of active oxygen in photosynthesis. In Kyle, D. J., Osmond, C. B. & Arntzen, C. N. (Eds) Topics in photosynthesis. Photoinhibition (vol. 9), pp. 227–87. Amsterdam: Elsevier Press.Google Scholar
Baker, A. & Kanofsky, J. R. 1992. Quenching of singlet oxygen by biomolecules from L1210 leukemia cells. Photochemistry and Photobiology 55, 523–8.CrossRefGoogle ScholarPubMed
Bonnet, R., McGarvey, D. J., Harriman, A., Land, E. J., Truscott, T. G. & Winfield, U.-J. 1988. Photophysical properties of meso-tetraphenylporphyrin and some meso-tetra (hydroxyphenyl) porphyrins. Photochemistry Photobiology 48, 271–6.CrossRefGoogle Scholar
Borland, C. F., McGarvey, D. J., Truscott, T. J., Cogdell, R. G. & Land, E. J. 1987. Photophysical studies of bacteriochlorophyll a and bacteriopheophytin a - singlet oxygen generation. Journal of Photochemistry and Photobiology B: Biology 1, 93–101.CrossRefGoogle Scholar
Butler, W. L. 1961. Chloroplast development: energy transfer and structure. Archives of Biochemistry and Biophysics 92, 287–95.CrossRefGoogle ScholarPubMed
Dzhagarov, B. M., Gurinovich, G. P., Novichenkov, V. E., Salokhiddinov, K. I., Shulga, A. M. & Ganja, V. A. 1990. Photosensitized formation of singlet oxygen and the quantum yield of intersystem crossing in porphyrins and metalloporphyrins. Soviet Journal of Chemical Physics (English translation) 6, 2098–119.Google Scholar
Egorov, S. Yu. & Krasnovsky, A. A. Jr 1990. Laser-induced luminescence of singlet molecular oxygen. Generation by drugs and pigments of biological importance. SPIE Proceedings 1403, 611–21.CrossRefGoogle Scholar
Egorov, S. Yu., Krasnovsky, A. A. Jr & Vacek, K. 1984. Chlorophyll photosensitized luminescence of singlet oxygen in polystyrene films. Kinetics of decay after a laser flash. Biofizika (Soviet Biophysics) 29, 921–2.Google Scholar
Egorov, S. Yu., Krasnovsky, A. A. Jr & Kulakovskaya, L. I. 1985. Investigation of the mechanism of chloroplast photodestruction: participation of the chlorophyll triplet state. Fiziologia rastenii (Soviet Plant Physiology) 32, 668–73.Google Scholar
Egorov, S. Yu., Kamalov, V. F., Koroteev, N. I., Krasnovsky, A. A. Jr, Toleutaev, B. N. & Zinukov, S. V. 1988. Rise and decay kinetics of photosensitized singlet oxygen luminescence in water. Measuremetns with nanosecond time-correlated photon counting technique. Chemical Physics Letters 163, 421–4.CrossRefGoogle Scholar
Elstner, C. F. 1982. Oxygen activation and oxygen toxicity. Annual Reviews of Plant Physiology 33, 73–96.CrossRefGoogle Scholar
Fiedor, L., Gorman, A. A., Hamblett, I., Rosenbach-Belkin, V., Solomon, Y., Scherz, A. & Tregub, I. 1993. A pulsed laser and pulse radiolysis study of amphifilic chlorophyll derivatives with PDT activity toward malignant melanoma. Photochemistry and Photobiology 58, 506–11.CrossRefGoogle Scholar
Foote, C. S. 1976. Photosensitized oxygenation and singlet oxygen, In Pryor, W. A. (Ed.) Free radicals in biology, vol. 2, pp. 85–133. New York: Academic Press.CrossRefGoogle Scholar
Foyer, C., Rowell, J. & Walker, D. 1983. Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157, 239–44.CrossRefGoogle ScholarPubMed
Kovalev, Yu. V., & Krasnovsky, A. A. Jr 1986. Excitation spectra of chlorophyll phosphorescence in cells of marine alga. Biofizika 31, 444–8.Google Scholar
Kramer, H. & Mathis, P. 1980. Quantum yield and rate of formation of carotenoid triplet state in photosynthetic structures. Biochimica et Biophysica Acta 593, 319–29.CrossRefGoogle Scholar
Krasnovsky, A. A. & Bystrova, M. I. 1980. Self-assembly of chlorophyll aggregated structures. BioSystems 12, 181–94.CrossRefGoogle ScholarPubMed
Krasnovsky, A. A. Jr 1977. Photoluminescence of singlet oxygen in solutions of chlorophyll and pheophytin. Biofizika 22, 927–8.Google Scholar
Krasnovsky, A. A. Jr 1979. Photoluminescence of singlet oxygen in pigment solutions. Photochemistry and Photobiology 29, 29–36.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr 1980. Luminescence of singlet oxygen in solutions of photosensitizers. (Soviet Journal of Applied Spectroscopy) Zhurnal Prikladnoi Spectroskopii 32, 852–6.Google Scholar
Krasnovsky, A. A. Jr 1982a. Luminescence arising under photosensitized formation of singlet oxygen in solutions, In Krasnovsky, A. A. (Ed.) Excited molecules. Kinetics of transformations (in Russian) pp. 32–60. Leningrad: Nauka.Google Scholar
Krasnovsky, A. A. Jr 1982b. Delayed fluorescence and phosphorescence of plant pigments. Photochemistry and Photobiology 36, 733–41.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr 1986. Singlet molecular oxygen in photosensitizing organisms. Mendeleev Chemistry Journal 31, 82–7.Google Scholar
Krasnovsky, A. A. Jr 1988. Mechanism of formation and role of singlet oxygen in photobiological processes. In Rubin, A. B. (Ed.) Molecular mechanisms of biological action of optical radiation (in Russian), pp. 23–40, Moscow: Nauka.Google Scholar
Krasnovsky, A. A. Jr 1990. Singlet molecular oxygen and primary mechanisms of photodynamic action of optical radiation. In Akhmanov, S. A. & Chernyaeva, E. B. (Eds.) Reviews on science and technology. Modern problems of laser physics (in Russian), vol. 3, pp. 63–135. Moscow: All Union Institute of Science and Technology Information.Google Scholar
Krasnovsky, A. A. Jr 1991. Photosensitized luminescence of singlet molecular oxygen: mechanisms and application for photobiology and medicine. In Douglas, R. H., Moan, J. & Ronto, G. Light in biology and medicine, vol. 2, pp. 437–52. New York: Plenum Press.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr 1993. Detection of photosensitized singlet oxygen luminescence in systems of biological importance. Steady-state and time-resolved measurements based on application of S-1 photomultiplier tubes. SPIE Proceedings 1890, 59–60.Google Scholar
Krasnovsky, A. A. Jr & Foote, C. S. 1993. Time-resolved measurements of singlet oxygen dimolsensitized luminescence. Journal of the American Chemical Society 115, 6013–16.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr & Neverov, K. V. 1988. Formation of triplet molecules of chlorophyll and its precursors in leaves treated with 5-aminolevulinic acid. Doklady Akademii Nauk SSSR (Plant Physiology) 302, 252–5.Google Scholar
Krasnovsky, A. A. Jr & Neverov, K. V. 1990. Photoinduced dimol luminescence of singlet molecular oxygen in solutions of photosensitizers. Chemical Physics Letters 167, 591–7.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr & Paramonova, L. I. 1983. Interaction of singlet oxygen with carotenoids: rate constants of physical and chemical quenching. Biofizika 28, 725–9.Google Scholar
Krasnovsky, A. A. Jr & Semenova, A. N. 1981. Parameters of the triplet state and spectral properties of the monomeric chlorophyll in liposomes at -196°. Photobiochemistry and Photobiophysics 3, 11–18.Google Scholar
Krasnovsky, A. A. Jr, Romanik, V. A. & Litvin, F. F. 1973. Phosphorescence and delayed fluorescence of chlorophylls and pheophytins a and b. Doklady Akademii Nauk SSSR (Biophysics) 209, 965–8.Google Scholar
Krasnovsky, A. A. Jr, Lebedev, N. N. & Litvin, F. F. 1974. Spectral characteristics of phosphorescence of chlorophylls and pheophytins. Doklady Akademii Nauk SSSR (Biophysics) 216, 1406–9.Google Scholar
Krasnovsky, A. A. Jr, Lebedev, N. N. & Litvin, F. F. 1975. Detection of the triplet state of chlorophyll and chlorophyll precursors from measurement of their delayed fluorescence and phosphorescence in leaves and chloroplasts. Doklady Akademii Nauk SSSR (Biophysics) 225, 207–10.Google Scholar
Krasnovsky, A. A. Jr, Kovalev, Yu. V. & Faludi-Daniel, A. 1980. Phosphorescence and delayed fluorescence of chlorophyll in mutants of maize with abnormal carotenoid composition. Doklady Akademii Nauk SSSR (Biophysics) 251, 1264–7.Google Scholar
Krasnovsky, A. A. Jr, Venediktov, E. A. & Chernenko, O. V. 1982. Quenching of singlet oxygen by chlorophylls and porphyrins. Biofizika 27, 966–72.Google Scholar
Krasnovsky, A. A. Jr, Minin, A. A. & Kagan, V. E. 1983. Quenching of singlet-oxygen luminescence by fatty acids and lipids. FEBS Letters 155, 233–6.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr, Egorov, S. Yu., Nasarova, O. V., Yartsev, E. I., Ponomarev, G. V. 1988. Photosensitised formation of singlet molecular oxygen in solutions of water-soluble porphyrines. Direct luminescence measurements. Studia biophysica 124, 123–42.Google Scholar
Krasnovsky, A. A. Jr & Neverov, K. V., Egorov, S. Yu., Roeder, B. & Levald, T. 1990. Photophysical studies of pheophorbide a and pheophytin a. Phosphorescence and photosensitized singlet oxygen luminescence. Journal Photochemistry and Photobiology, B: Biology 5, 245–54.CrossRefGoogle ScholarPubMed
Krasnovsky, A. A. Jr, Cheng, P., Blankenship, R. E., Moore, T. A. & Gust, D. 1993. The photophysics of monomeric bacteriochlorophylls c, d and their derivatives: properties of the triplet state and singlet oxygen photogeneration and quenching. Photochemistry and Photobiology 57, 324–30.CrossRefGoogle Scholar
Krasnovsky, A. A. Jr, Lopez, J., Cheng, P., Liddel, P. A., Blankenship, R. E., Moore, T. A. & Gust, D. 1994. Generation and quenching of singlet molecular oxygen by aggregated molecules of bacteriochlorophyll d in model systems and chlorosomes. Photosynthesis Research (in press).CrossRefGoogle Scholar
Krinsky, N. I. 1984. Biology and photobiology of singlet oxygen. In Bors, W., Sarah, M. & Tait, D. (Eds.) Oxygen radicals in chemistry and biology, pp. 45–51. Berlin: Walter de Gruyter Co.Google Scholar
Kyle, D. J. 1987. The biochemical basis for photoinhibition of photosystem II. In Kyle, D. J., Osmond, D. B. & Arntzen, D. J. (Eds.) Topics in photosynthesis. Photoinhibition, vol. 9, 00. 197–226. Amsterdam: Elsevier Press.Google Scholar
Lambert, C. R., Reddi, E., Spikes, J. D., Rodgers, M. A. J. & Jori, J. 1986. The effects of porphyrin structure and aggregation state on photosensitized processes in aqueous and micellar media. Photochemistry and Photobiology 44, 595–601.CrossRefGoogle ScholarPubMed
Lebedev, N. N., Krasnovsky, A. A. Jr & Litvin, F. F. 1991. Phosphorescence of protochlorophyll (ide) and chlorophyll (ide) in etiolated and greening leaves. Assignment of spectral bands. Photosynthesis Research 30, 7–14.CrossRefGoogle ScholarPubMed
Lichtenthaler, H. K. & Park, R. B. 1963. Chemical composition of chloroplast lamellae from spinach. Nature 198, 1070–72.CrossRefGoogle Scholar
Macpherson, A. N., Telfer, A., Barber, J. & Truscott, T. G. 1993. Direct detection of singlet oxygen from isolated Photosystem II reaction centres. Biochimica et Biophysica Acta 1143, 301–9.CrossRefGoogle Scholar
Mathis, P. & Schenck, C. C. 1981. The function of carotenoids in photosynthesis. In Britton, G. & Goodwin, T. W. (Eds.) Carotenoid chemistry and biochemistry, pp. 339–51. Oxford: Pergamon Press.Google Scholar
Matveev, M. Yu. & Darmanyan, A. P. 1990. Quenching of singlet oxygen by ionol and β-carotene. Soviet Journal of Chemical Physics (English translation) 6, 2742–51.Google Scholar
Merzlyak, M. N. 1989. Activated oxygen and oxidation processes in membranes of plant cell. Reviews of Science and Technology. Plant Physiology, vol. 6. Moscow: All Union Institute of Information (in Russian).Google Scholar
Monger, T. G., Cogdell, R. J. & Parson, W. W. 1976. Triplet states of bacteriochlorophyll and carotenoids in chromatophores of photosynthetic bacteria. Biochimica et Biophysica Acta 449, 136–53.CrossRefGoogle ScholarPubMed
Neverov, K. V. & Krasnovsky, A. A. Jr 1992. Assignment for the novel vibronic bands in the spectrum of the photosensitized singlet oxygen luminescence. Chemical Physics Letters 189, 189–92.CrossRefGoogle Scholar
Ogilby, P. R. & Foote, C. S. 1983. Chemistry of singlet oxygen. 42. Effect of solvent, solvent isotopic substitution and temperature on the lifetime of singlet molecular oxygen (1Δg). Journal of the American Chemical Society 105, 3423–40.CrossRefGoogle Scholar
Parker, J. G. & Stanboro, W. D. 1984. Optical determination of the rates of formation and decay of O2 (1Δg) in H2O, D2O and other solvents. Journal of Photochemistry 25, 545.CrossRefGoogle Scholar
Rabinovitch, E. I. 1945. Photosynthesis and related processes, vol. 1. New York: Interscience Publ., Inc.Google Scholar
Salokhiddinov, K. I., Byteva, I. M. & Dzhagarov, B. M. 1979. Duration of the luminescence of singlet oxygen in solution following pulsed laser excitation. Optika i Spektroskopia (Soviet Optics and Spectroscopy) 47, 881–6.Google Scholar
Schmidt, R. 1989. The influence of heavy atoms on the deactiation of singlet oxygen (1Δg) in solution. Journal of the American Chemical Society 93, 4507–10.Google Scholar
Spikes, J. D. & Bommer, J. C. 1991. Chlorophyll and related pigments as photosensitizers in biology and medicine. In: Scheer, H. (Ed.) Chlorophylls, pp. 1182–204. Boca Raton: CRC Press.Google Scholar
Thornber, J. P., Alberte, R. S., Hunter, F. A., Shiozawa, J. A. & Kan, K-S. 1977. The organization of chlorophyll in the plant photosynthetic unit. Brookhaven Symposium in Biology 28, 132–48.Google Scholar
Zinukov, S. V., Kamalov, V. F., Koroteev, N. I. & Krasnovsky, A. A. Jr 1991. Nanosecond measurements of photosensitized luminescence of singlet molecular oxygen in aqueous solutions saturated with air. Effect of temperature and detergent. Optika i Spektroskopia (Soviet Optics and Spectroscopy) 70, 790–94.Google Scholar