Singlet oxygen and plants

Abstract The generation, occurrence and action of singlet oxygen in plant tissue is reviewed. Particular emphasis is placed upon its formation from triplet sensitizers and its reactivity with molecules of biological importance such as lipids and amino acids. The possibility of singlet oxygen generation in chloroplasts is discussed in relation to potential quenching systems such as carotenoid pigments, ascorbate and α-tocopherol. The problems associated with carotenoid diminution and some stress and herbicide treatment conditions are related to the possibility of damage by singlet oxygen. The action of a number of secondary plant substances, including quinones, furanocoumarins, polyacetylenes and thiophenes, as plant defence agents is discussed in relation to the photodynamic generation of singlet oxygen.

[1]  U. Takahama,et al.  Suppression of lipid peroxidation by β-carotene in illuminated chloroplast fragments: Evidence for β-carotene as a quencher of singlet molecular oxygen in chloroplasts , 1978 .

[2]  F. T. Wolf,et al.  Psoralen, an inhibitor in the seeds of Psoralea subacaulis (Leguminosae) , 1967 .

[3]  R. Mummery,et al.  The Effect of Light on Carotenoids of Etiolated Mung Bean Seedlings , 1969 .

[4]  W. Haag,et al.  Singlet oxygen in surface waters — Part I: Furfuryl alcohol as a trapping agent , 1984 .

[5]  G. Cohen-bazire,et al.  Inhibition of Carotenoid Synthesis in Photosynthetic Bacteria: Specific Inhibition of Carotenoid Synthesis in a Photosynthetic Bacterium and its Physiological Consequences , 1958, Nature.

[6]  M. Berenbaum Patterns of Furanocoumarin Distribution and Insect Herbivory in the Umbelliferae: Plant Chemistry and Community Structure , 1981 .

[7]  G. Miller,et al.  Singlet oxygen generation on soil surfaces , 1983 .

[8]  S. Briggs,et al.  Changes in tobacco cell membrane composition and structure caused by cercosporin. , 1983, Plant physiology.

[9]  P. G. Bartels,et al.  Chloroplast Development in 4-Chloro-5-(dimethylamino)-2-(α,α,α-trifluoro-m-tolyl)-3 (2H)-pyridazinone (Sandoz 6706)-treated Wheat Seedlings: A Pigment, Ultrastructural, and Ultracentrifugal Study 1 , 1970 .

[10]  J. Bakker,et al.  Photoactivation of the nematicidal compound alpha-terthienyl from roots of marigolds (Tagetes species). A possible singlet oxygen role. , 1979, The Journal of biological chemistry.

[11]  A. Dodge,et al.  Isolation and activity of the photodynamic pigment hypericin , 1985 .

[12]  G. Cohen-bazire,et al.  Function of Carotenoids in Photosynthesis , 1955, Nature.

[13]  C. Foote,et al.  Chemistry of singlet oxygen. X. Carotenoid quenching parallels biological protection. , 1970, Journal of the American Chemical Society.

[14]  T. Izod,et al.  PHOTODYNAMIC INACTIVATION OF E. COLI BY ROSE BENGAL IMMOBILIZED ON POLYSTYRENE BEADS , 1978, Photochemistry and photobiology.

[15]  P. Proksch,et al.  Phototoxic and insecticidal activities of chromenes and benzofurans from Encelia , 1983 .

[16]  J. Kuc,et al.  Xanthotoxin: A phytoalexin of Pastinaca sativa root☆ , 1973 .

[17]  P. C. Joshi,et al.  Production of singlet oxygen and superoxide radicals by psoralens and their biological significance. , 1983, Biochemical and biophysical research communications.

[18]  R. Larson,et al.  Quenching of singlet oxygen by alkaloids and related nitrogen heterocycles , 1984 .

[19]  R. Sager,et al.  Pigments and Photosynthesis in a Carotenoid-Deficient Mutant Of chlamydomonas , 1958, Nature.

[20]  E. Ruppel,et al.  Ultrastructure of lesions produced by Cercospora beticola in leaves of Beta vulgaris , 1979 .

[21]  S. Agarwala,et al.  Effect of Molybdenum Status on the Ascorbic Acid Content of Plants in Sand Culture , 1950, Nature.

[22]  P. C. Joshi,et al.  Production of active oxygen species (1O2 and O2-.) by psoralens and ultraviolet radiation (320-400 nm). , 1984, Biochimica et biophysica acta.

[23]  U. Takahama SUPPRESSION OF LIPID PHOTOPEROXIDATION BY QUERCETIN AND ITS GLYCOSIDES IN SPINACH CHLOROPLASTS , 1983 .

[24]  C. Rees CHEMORECEPTOR SPECIFICITY ASSOCIATED WITH CHOICE OF FEEDING SITE BY THE BEETLE, CHRYSOLINA BRUNSVICENSIS ON ITS FOODPLANT, HYPERICUM HIRSUTUM , 1969 .

[25]  A. Dodge,et al.  Photodynamic damage to plant leaf tissue by rose bengal , 1984 .

[26]  P. V. Hasselt,et al.  PHOTO-OXIDATION OF LEAF PIGMENTS IN CUCUMIS LEAF DISCS DURING CHILLING , 1972 .

[27]  J. J. Rensen Molecular mechanisms of herbicide action near photosystem II , 1982 .

[28]  P. Song,et al.  PHOTOCHEMISTRY AND PHOTOBIOLOGY OF PSORALENS , 1979, Photochemistry and photobiology.

[29]  D. Robertson,et al.  Role of Carotenoids in Protecting Chlorophyll From Photodestruction. , 1960, Plant physiology.

[30]  B. Bielski,et al.  SOME PROPERTIES OF THE ASCORBATE FREE RADICAL * , 1975, Annals of the New York Academy of Sciences.

[31]  N. Doke Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity , 1983 .

[32]  T. Murphy,et al.  MECHANISM OF PHOTOINACTIVATION OF PLANT PLASMA MEMBRANE ATPASE , 1984 .

[33]  W. Haag,et al.  Singlet oxygen in surface waters — Part II: Quantum yields of its production by some natural humic materials as a function of wavelength , 1984 .

[34]  E. Bell,et al.  Secondary plant products , 1980 .

[35]  J. Barltrop,et al.  Evidence for photodynamic action by a naturally occurring hydrilla‐growth inhibitor , 1983 .

[36]  P. H. Leeuwen,et al.  Photosynthetic inhibition in Phaseolus vulgaris II. The influence of light on herbicidal action , 1974 .

[37]  N. Wolfe,et al.  Singlet oxygen in natural waters , 1977, Nature.

[38]  N. Doke Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components , 1983 .

[39]  W. Wergin,et al.  The effects of fluometuron on the ultrastructural development, chlorophyll accumulation and photosynthetic competence in developing velvetleaf seedlings , 1975 .

[40]  L. Grossweiner,et al.  RESEARCH NOTE PHOTODYNAMIC SENSITIZATION BY 8‐METHOXYPSORALEN VIA THE SINGLET OXYGEN MECHANISM * , 1975, Photochemistry and photobiology.

[41]  H. Lichtenthaler,et al.  Effect of the Herbicide San 6706 on Biosynthesis of Photosynthetic Pigments and Prenylquinones in Raphanus and in Hordeum Seedlings , 1977 .

[42]  C. Foote,et al.  Cercosporin, a Singlet Oxygen Generator , 1983 .

[43]  J. Teasdale,et al.  Influence of Light and Temperature on Bentazon Phytotoxicity to Cucumber (Cucumis sativus) , 1983, Weed Science.

[44]  H. Wynberg,et al.  DITHIOPHENES AS SINGLET OXYGEN SENSITIZERS , 1982 .

[45]  M. Nishikimi Oxidation of ascorbic acid with superoxide anion generated by the xanthine-xanthine oxidase system. , 1975, Biochemical and biophysical research communications.

[46]  P. Weitzman,et al.  Rose bengal immobilized on sepharose — a new tool for protein photo‐oxidation , 1976, FEBS letters.

[47]  R. Hancock,et al.  MODE OF ACTION OF α‐TERTHIENYL ON ESCHERICHIA COLI: EVIDENCE FOR A PHOTODYNAMIC EFFECT ON MEMBRANES , 1982 .

[48]  G. Pfyffer,et al.  MONOFUNCTIONAL COVALENT PHOTOBINDING OF DICTAMNINE, A FUROQUINOLINE ALKALOID, TO DNA AS TARGET IN VITRO , 1982 .

[49]  C. Wells,et al.  Rates of reaction of singlet oxygen with some systemic pyrimidine fungicides and related compounds , 1981 .

[50]  L. Anderson Effect of Light on the Phytotoxicity of Fluridone in American Pondweed (Potamogeton nodosus) and Sago Pondweed (P. pectinatus) , 1981, Weed Science.

[51]  M. Daub,et al.  Cercosporin, a photosensitizing toxin from Cercospora species. , 1982 .

[52]  T. Árnason,et al.  OXYGEN REQUIREMENT FOR NEAR‐UV MEDIATED CYTOXICITY OF α‐TERTHIENYL TO ESCHERICHIA COLI AND SACCHAROMYCES CEREVISIAE , 1981 .

[53]  G. Renger Studies on the structural and functional organization of system II of photosynthesis. The use of trypsin as a structurally selective inhibitor at the outer surface of the thylakoid membrane. , 1976, Biochimica et biophysica acta.

[54]  P. G. Bartels,et al.  Inhibition of Carotenoid Synthesis by Fluridone and Norflurazon , 1978, Weed Science.

[55]  J. Bakker,et al.  PHOTO ACTIVATION OF ISOFLAVONOID PHYTOALEXINS: INVOLVEMENT OF FREE RADICALS , 1983 .

[56]  P. C. Chan,et al.  Ascorbic acid as a scavenger of singlet oxygen , 1979, FEBS letters.

[57]  R. Santus,et al.  A study of the photosensitizing properties of seawater , 1983 .

[58]  A. Fuchs,et al.  The formation of perylenequinones in etiolated cucumber seedlings infected with Cladosporium cucumerinum , 1967 .

[59]  K. Pallett,et al.  Studies into the action of some photosynthetic inhibitor herbicides. , 1980 .

[60]  T. Baszyński Effect of alpha-tocopherol on reconstitution of photosystem I in heptane-extracted spinach chloroplasts. , 1974, Biochimica et biophysica acta.

[61]  G. Towers,et al.  GENOTOXICITY OF THE NATURAL FUROCHROMONES, KHELLIN AND VISNAGIN AND THE IDENTIFICATION OF A KHELLIN‐THYMINE PHOTOADDUCT , 1983, Photochemistry and photobiology.

[62]  T. Yoshihara,et al.  Phleichrome; A New Phytotoxic Compound Produced by Cladosporium phlei , 1975 .

[63]  M. Geoghegan,et al.  Production of cercosporin by Cercospora species , 1977 .

[64]  E. Graham,et al.  Phototoxic furanoquinolines of the Rutaceae. , 1981, Planta medica.

[65]  E. Koren,et al.  Interference in Carotenogenesis as a Mechanism of Action of the Pyridazinone Herbicide Sandoz 6706: Accumulation of C-40 Carotenoid Precursors Inhibition of beta-Carotene Synthesis and Enhancement of Phytoene Epoxidation. , 1974, Plant physiology.

[66]  G. Searle,et al.  Role of β-carotene in the reaction centres of Photosystems I and II of spinach chloroplasts prepared in non-polar solvents , 1978 .

[67]  M. E. Daub Peroxidation of tobacco membrane lipids by the photosensitizing toxin, cercosporin. , 1982, Plant physiology.

[68]  R. Wise,et al.  A comparative study of low-temperature-induced ultrastructural alterations of three species with differing chilling sensitivities , 1983 .

[69]  A. Dodge,et al.  Photodynamic Effects of Rose Bengal on Senescent Flax Cotyledons , 1983 .

[70]  G. Rosenthal,et al.  Phototoxicity of the allelochemical, α-terthienyl, to larvae of Manduca sexta (L.) (Sphingidae) , 1984 .

[71]  R. M. Devlin,et al.  Chlorophyll production and chloroplast development in norflurazon-treated plants , 1976 .

[72]  P. Hasselt,et al.  Photooxidative damage to the photosynthetic apparatus during chilling , 1980 .

[73]  M. Rodgers,et al.  Singlet molecular oxygen , 1981 .

[74]  P. G. Bartels,et al.  A new inhibitor of carotenoid synthesis in higher plants: 4-chloro-5-(dimethylamino)-2- , , ,(trifluoro-m-tolyl)-3(2H)-pyridazinone. , 1972, Biochemical and biophysical research communications.

[75]  G. Towers,et al.  PHOTOTOXIC EFFECTS OF NATURALLY OCCURRING POLYACETYLENES AND α‐TERTHIENYL ON HUMAN ERYTHROCYTES , 1980 .

[76]  M. Berenbaum Toxicity of a Furanocoumarin to Armyworms: A Case of Biosynthetic Escape from Insect Herbivores , 1978, Science.

[77]  K. Fuwa,et al.  Cercosporin, a Novel Photodynamic Pigment Isolated from Cercospora kikuchii , 1975 .

[78]  F. J. Gommers Increase of the Nematicidal Activity of a-Terthienyl and Related Compounds By Light , 1972 .

[79]  M. Berenbaum,et al.  Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? , 1981, Science.

[80]  P. Böger,et al.  Action of EMD-IT 5914 on Chloroplasts , 1978, Weed Science.

[81]  T. Kimura,et al.  Reactivity of singlet molecular oxygen with cholesterol in a phospholipid membrane matrix. A model for oxidative damage of membranes. , 1977, Biochemical and biophysical research communications.

[82]  M. Daub,et al.  Light-induced production of singlet oxygen and superoxide by the fungal toxin, cercosporin. , 1983, Plant physiology.

[83]  K. Tietjen,et al.  Differential response of cultured parsley cells to elicitors from two non-pathogenic strains of fungi. 1. Identification of induced products as coumarin derivatives. , 1983, European journal of biochemistry.

[84]  L. Cavallini,et al.  Lipid peroxidation induced by cercosporin as a possible determinant of its toxicity. , 1979, Chemico-biological interactions.

[85]  W. H. Minshall Influence of Light on the Effect of 3-p-(Chlorophenyl)-1, 1-Dimethylurea on Plants , 1957 .

[86]  D. Mckenna,et al.  Ultra-violet mediated cytotoxic activity of β-carboline alkaloids , 1981 .

[87]  G. B. Henegouwen,et al.  Relation between some photobiological properties of furocoumarins and their extent of singlet oxygen production. , 1981 .

[88]  I. Fridovich,et al.  SUPEROXIDE RADICALS, SUPEROXIDE DISMUTASES and OXYGEN TOXICITY IN PLANTS , 1983 .

[89]  J. Bakker,et al.  Effects of Singlet Oxygen Generated By the Nematicidal Compound α-Terthienyl From Tagetes On the Nematode Aphelenchus a Venae , 1980 .

[90]  P. Song,et al.  Spectroscopic characterization of the Stentor photoreceptor. , 1979, Biochimica et biophysica acta.

[91]  J. Laseter,et al.  Reactions of Singlet Oxygen with Pine Pollen , 1973, Science.

[92]  O. Junttila Allelopathic Inhibitors in Seeds of Hevacleum laciniatum , 1976 .

[93]  J. Hudson,et al.  NATURE OF THE INTERACTION BETWEEN THE PHOTOACTIVE COMPOUND PHENYLHEPTATRIYNE AND ANIMAL VIRUSES , 1982, Photochemistry and photobiology.

[94]  S. A. Reed,et al.  ALPHA‐TERTHIENYL, A NON‐PHOTODYNAMIC PHOTOTOXIC COMPOUND , 1980 .

[95]  J. Maldonado,et al.  PHOTOINACTIVATION OF SPINACH NITRATE REDUCTASE SENSITIZED BY FLAVIN MONONUCLEOTIDE. EVIDENCE FOR THE INVOLVEMENT OF SINGLET OXYGEN , 1982 .

[96]  M. Nishimura,et al.  Formation of singlet molecular oxygen in illuminated chloroplasts. Effects on photoinactivation and lipid peroxidation , 1975 .

[97]  E. Baker,et al.  The fungitoxicities of plant furocoumarins , 1966 .

[98]  T. Swain SECONDARY COMPOUNDS AS PROTECTIVE AGENTS , 1977 .

[99]  M. Berenbaum COUMARINS AND CATERPILLARS: A CASE FOR COEVOLUTION , 1983, Evolution; international journal of organic evolution.

[100]  M. Berenbaum,et al.  Effects of linear furanocoumarins on an adapted specialist insect (Papilio polyxenes) , 1981 .

[101]  P. Böger,et al.  Influence of Bleaching Herbicides on Chlorophyll and Carotenoids , 1979 .

[102]  M. Rodgers,et al.  THE PHOTOSENSITIZED FORMATION AND REACTION OF SINGLET OXYGEN, O2*(1Δ), IN AQUEOUS MICELLAR SYSTEMS , 1976 .

[103]  R. M. Baxter,et al.  Reactions of singlet oxygen in humic waters , 1982 .

[104]  L. H. Grimme,et al.  The Inhibition of Carotenoid Biosynthesis in Green Algae by SANDOZ H 6706: Accumulation of Phytoene and Phytofluene in Chlorella fusca , 1975 .

[105]  P. Ogilby,et al.  Chemistry of singlet oxygen. 42. Effect of solvent, solvent isotopic substitution, and temperature on the lifetime of singlet molecular oxygen (1.DELTA.g) , 1983 .

[106]  N. Krinsky Carotenoid protection against oxidation , 1979 .

[107]  P. Koehler,et al.  Isolation and identification of xanthotoxin (8-methoxypsoralen) and bergapten (5-methoxypsoralen) from celery infected with Sclerotinia sclerotiorum. , 1972, Applied microbiology.

[108]  F. M. Ashton Relationship between Light and Toxicity Symptoms Caused by Atrazine and Monuron , 1965 .

[109]  R. Lynch The metabolism of superoxide anion and its progeny in blood cells. , 1983, Topics in current chemistry.

[110]  A. Dodge,et al.  Photodynamic damage to chloroplast membranes, photosensitized oxidation of chloroplast acyl lipid , 1983 .

[111]  C. Foote,et al.  [3] Characterization of singlet oxygen , 1984 .

[112]  F. M. Ashton,et al.  Structural Changes in Phaseolus vulgaris Induced by Atrazine II. Effects on Fine Structure of Chloroplasts , 1963, Botanical Gazette.

[113]  K. Polewski,et al.  CHEMILUMINESCENCE IN THE PEROXIDATION OF TANNIC ACID , 1979 .

[114]  L. Merlini,et al.  Screening of the genus Cercospora for secondary metabolites , 1977 .

[115]  A. Dorsman,et al.  CHLOROPHYLL METABOLISM IN ETIOLATED GHERKIN SEEDLINGS I. PHOTOINHIBITION OF CHLOROPHYLL ACCUMULATION , 1977, Photochemistry and photobiology.

[116]  A. Vianello,et al.  Photodynamic activity of cercosporin on plant tissues , 1979 .

[117]  G. Towers,et al.  Photoinactivation of human erythrocyte enzymes by α‐terthienyl and phenylheptatriyne, naturally occurring compounds in the asteraceae , 1979, FEBS letters.

[118]  J. Oorschot Photosynthetic inhibition in Phaseolus vulgaris.: I. The analogy between herbicidal action and carbon dioxide starvation , 1974 .

[119]  J. W. Hastings,et al.  Chemical and biological aspects of singlet excited molecular oxygen. , 1970, Photophysiology.

[120]  T. Árnason,et al.  THE ROLE OF OXYGEN IN PHOTOSENSITIZATIONS WITH POLYACETYLENES AND THIOPHENE DERIVATIVES , 1984 .

[121]  P. Song,et al.  PROTECTION OF CHLOROPHYLL a BY CAROTENOID FROM PHOTODYNAMIC DECOMPOSITION , 1978 .

[122]  A. Gennaro,et al.  Notizen: Photosensitized Effects of Furocoumarins: the Possible Role of Singlet Oxygen , 1983, Zeitschrift fur Naturforschung. Section C, Biosciences.

[123]  T. Goodwin,et al.  Studies in carotenogenesis. 28. The effect of illumination on carotenoid synthesis in french-bean (Phaseolus vulgaris) seedlings. , 1960, The Biochemical journal.

[124]  J. Arc Photosynthetic electron transport in relation to thylakoid membrane composition and organization , 1983 .

[125]  O. Lindig,et al.  Dye-sensitized Photooxidation Reactions in the Boll Weevil, Anthonomous grandis , 1975 .

[126]  E. R. Burns,et al.  Inhibition of carotenoid synthesis as a mechanism of action of amitrole, dichlormate, and pyriclor. , 1971, Plant physiology.