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Journal of Chemical Ecology

, Volume 12, Issue 4, pp 823–834 | Cite as

Toxicological action and ecological importance of plant photosensitizers

  • K. R. Downum
  • E. Rodriguez
Article

Abstract

This review discusses the biochemical action and ecological significance of phototoxic phytochemicals. Mechanistic details of photosensitization as well as cellular and molecular targets of plant-derived phototoxins in model biological systems (microbial and in vitro) and in herbivorous insects are described. Findings from these studies suggest the potential importance of phototoxic plant metabolites in plant-insect interactions. Aspects of phototoxin distribution and significance in diverse ecosystems are considered, and areas for future research are suggested.

Key words

Phototoxic phytochemicals insect photosensitization mechanisms of photosensitization plant-insect interactions 

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References

  1. Abeysekera, B.F., Abramowski, Z., andTowers, G.H.N. 1983. Genotoxicity of the natural furochromones, khellin and visnagin and the identification of a khellin-thymine photoadduct.Photochem. Photobiol. 38:311–315.Google Scholar
  2. Aregullin, M. 1985. Chemistry and biology of benzofurans and benzopyrans inFlourensia and related genera. Dissertation. Irvine, University of California.Google Scholar
  3. Arnason, T., Wat, C.-K., Downum, K.R., Yamamoto, E., Graham, E., andTowers, G.H.N. 1980. Photosensitization ofEscherichia coli andSaccharomyces cerevisiae by phenylheptatriyne fromBidens pilosa.Can. J. Microbiol. 26:698–705.Google Scholar
  4. Arnason, T., Chan, G.F.Q., Wat, C.-K., Downum, K., andTowers, G.H.N. 1981a. Oxygen requirement for near-UV mediated cytotoxicity of alpha-terthienyl toEscherichia coli andSaccharomyces cerevisiae.Photochem. Photobiol. 33:821–824.Google Scholar
  5. Arnason, T., Swain, T., Wat, C.-K., Graham, E.A., Partington, S., Towers, G.H.N., andLam, J. 1981b. Mosquito larvicidal activity of polyacetylenes from species in the Asteraceae.Biochem. Syst. Ecol. 9:63–68.Google Scholar
  6. Arnason, T., Towers, G.H.N., Philogene, B.J.R., andLambert, J.D.H. 1983. The role of natural photosensitizers in plant resistance to insects, pp. 139–151,in P.A. Hedin (ed.). Plant Resistance to Insects. ACS Symposium Series No. 208, American Chemical Society, Washington, D.C.Google Scholar
  7. Ashwood-Smith, M.J. 1978. Frameshift mutations in bacteria produced in the dark by several furocoumarins; absence of activity of 4,5′,8-trimetliylpsoralen.Mutat. Res. 58:23–27.Google Scholar
  8. Ashwood-Smith, M.J., Towers, G.H.N., Abramowski, Z., Poulton, G.A., andLiu, M. 1982. Photobiological studies with dictamnine, a furoquinoline alkaloid.Mutat. Res. 102:401–412.Google Scholar
  9. Averbeck, D., Moustacchi, E., andBisagni, E. 1978. Biological effects and repair of damage photoinduced by a derivative of psoralen substituted at 3,4 reaction site—photoreactivity of this compound and lethal effects in yeast.Biochim. Biophys. Acta 518:464–481.Google Scholar
  10. Bakker, J., Gommers, F.J., Nieuwenhuis, I., andWynberg, H. 1979. Photoactivation of the nematicidal compound alpha-terthienyl from roots of marigolds (Tagetes species). A possible singlet oxygen role.J. Biol. Chem. 254:1841–1844.Google Scholar
  11. Bakker, J., Gommers, F.J., Smits, L., Fuchs, A., andDe Vries, F.W. 1983. Photoactivation of isoflavonoid phytoalexins: Involvement of free radicals.Photochem. Photobiol. 38:323–329.Google Scholar
  12. Berenbaum, M. 1978. Toxicity of a furanocoumarin to armyworms: A case of biosynthetic escape from insect herbivores.Science 201:532–534.Google Scholar
  13. Bohlmann, F., Burkhardt, T., andZdero, C. 1973. Naturally Occurring Acetylenes. Academic Press, London.Google Scholar
  14. Bowers, W.S. 1982. Toxicology of the precocenes, pp. 403–427,in J. Coats (ed.). Insecticide Mode of Action. Academic Press, Inc. New York.Google Scholar
  15. Camm, E.L., Towers, G.H.N., andMitchell, J.C. 1975. UV-mediated antibiotic activity of some Compositae species.Phytochemistry 14:2007–2011.Google Scholar
  16. Dall'acqua, F., Marciani, G., Ciavatta, L., andRodighiero, G. 1971. Formation of interstrand cross-linking in photoreactions between furocoumarins and DNA.Z. Naturforsch. 26:561–569.Google Scholar
  17. Downum, K.R. 1986. Photoactivated biocides from higher plants, pp. 197–205,in M. Green and P.A. Hedin (eds.). Natural Plant Resistance to Pests: Roles of Allelochemicals. ACS Symposium Series No. 296, American Chemical Society, Washington, D.C.Google Scholar
  18. Downum, K.R., andTowers, G.H.N. 1983. Analysis of thiophenes in the Tageteae (Asteraceae) by HPLC.J. Nat. Prod. 46:98–103.Google Scholar
  19. Downum, K.R., Hancock, R.E.W., andTowers, G.H.N. 1982. Mode of action of alpha-terthienyl onEscherichia coli: Evidence for a photodynamic effect on membranes.Photochem. Photobiol. 36:517–523.Google Scholar
  20. Downum, K.R., Rosenthal, G.A., andTowers, G.H.N. 1984. Phototoxicity of the allelochemical, alpha-terthienyl, to larvae ofManduca sexta (L.) (Sphingidae).Pest. Biochem. Physiol. 22:104–109.Google Scholar
  21. Downum, K.R., Keil, D.J., andRodriguez, E. 1985. Distribution of acetylenic thiophenes in the Pectidinae.Biochem. Syst. Ecol. 13:109–113.Google Scholar
  22. Downum, K.R.,Villegas, S.,Keil, D.J., andRodriguez, E. 1986. Plant photosensitizers: A survey of their significance in arid and semi-arid land plants.Biochem. Syst. Ecol. In review.Google Scholar
  23. Dubbelman, T.M.A.R., Haasnoot, C., andvan Steveninck, J. 1980. Temperature dependence of photodynamic red cell membrane damage.Biochim. Biophys. Acta 601:220–227.Google Scholar
  24. Fisch, M.H., Gramain, J.C., andOlesen, J.A. 1971. Photooxidation of amines.Chem. Commun. 663:71.Google Scholar
  25. Granger, M., andHelene, C. 1983. Photoaddition of 8-methoxypsoralen toE. coli DNA polymerase I. Role of psoralen photoadducts in the photosensitized alterations of Pol I enzymatic activities.Photochem. Photobiol. 38:563–568.Google Scholar
  26. Heitz, J.R. 1982. Xanthene dyes as pesticides, pp. 429–457,in J.R. Coats (ed.) Insecticide Mode of Action. Academic Press, New York.Google Scholar
  27. Heywood, V.H. 1978. Flowering Plants of the World. Mayflower, New York.Google Scholar
  28. Hunziker, J.H., Palacios, R.A., Poggio, L., Naranjo, C.A., andYang, T.W. 1977. Geographic distribution, morphology, hybridization, cytogenetics and evolution, pp. 10–47,in T.J. Mabry, J.H. Hunziker, and D.R. DiFeo Jr. (eds.). Creosote Bush, Biology and Chemistry ofLarrea in New World Deserts. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania.Google Scholar
  29. Kagan, J., Chan, G., Dhawan, S.N., Arora, S.K., andProkash, I. 1983. The effect of ultraviolet light on the toxicity of natural products toward the eggs ofDrosophila melanogaster.J. Nat. Prod. 46:646–650.Google Scholar
  30. Kagan, J., Tadema-Wielandt, K., Chan, G., Dhawan, S.N., Jaworsky, J., Prakash, I., andArora, S.K. 1984. Oxygen requirement for near-UV mediated cytotoxicity of phenylheptatriyne toEscherichia coli.Photochem. Photobiol. 39:465–467.Google Scholar
  31. Knox, J.P., andDodge, A.D. 1985. Singlet oxygen and plants.Phytochemistry 24:889–896.Google Scholar
  32. Krinsky, N.I. 1985. Detection and biological function of active oxygen species.Photochem. Photobiol. 41(Suppl.):96S.Google Scholar
  33. Lamola, A.A., andDoleiden, F.H. 1980. Cross-linking of membrane proteins and protoporphyrin-sensitized photohemolysis.Photochem. Photobiol. 31:597–601.Google Scholar
  34. Mabry, T.J., DeFeo, D.R., Jr., Sakakibara, M., Bohnstedt, C.F., Jr., andSiegler, D. 1977. The natural products chemistry ofLarrea, pp. 115–134,in T.J. Mabry, J.H. Hunziker, and D.R. DiFeo, Jr. (eds.). Creosote Bush, Biology and Chemistry ofLarrea in New World Deserts. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania.Google Scholar
  35. McLachlan, D., Arnason, J.T., Philogene, B.J.R., andChampagne, D. 1982. Antifeedant activity of the polyacetylene, phenylheptatriyne (PHT), from the Asteraceae toEuxoa messoria (Lepidoptera, Noctuidae).Experientia 38:1061–1062.Google Scholar
  36. McLachlan, D., Arnason, J.T., andLam, J. 1984. The role of oxygen in photosensitizations with polyacetylenes and thiophene derivatives.Photochem. Photobiol. 39:177–182.Google Scholar
  37. Ou, C.N., andSong, P.-S., 1978. Photobinding of 8-methoxypsoralen to transfer-RNA and 5-fluorouracil-enriched transfer RNA.Biochemistry 17:1054–1059.Google Scholar
  38. Pfyffer, G.E., andTowers, G.H.N. 1982. Photochemical interaction of dictamnine, a furoquinoline alkaloid, with fungal DNA in vitro and in vivo.Can. J. Microbiol. 28:468–473.Google Scholar
  39. Pfyffer, G.E., Panfil, I., andTowers, G.H.N. 1982. Monofunctional covalent photobinding of dictamnine, a furoquinoline alkaloid, to DNA as target in vitro.Photochem. Photobiol. 35:63–68.Google Scholar
  40. Philogene, B.J.R., Arnason, J.T., Towers, G.H.N., Campos, F., Champagne, D., andMcLachlan, D. 1984. Berberine: A naturally occurring phototoxic alkaloid.J. Chem. Ecol. 10:115–123.Google Scholar
  41. Proksch, P., andRodriguez, E. 1983. Chromenes and benzofurans of the Asteraceae, their chemistry and biological significance.Phytochemistry 22:2335–2348.Google Scholar
  42. Proksch, P., Proksch, M., Towers, G.H.N., andRodriguez, E. 1983. Phototoxic and insecticidal activities of chromenes and benzofurans fromEncelia.J. Nat. Prod. 46:331–334.Google Scholar
  43. Rawls, H.R., andVan Santen, P.J. 1970. A possible role for singlet oxygen in initiation of fatty acid autoxidation.J. Am. Oil Chem. Soc. 47:121–125.Google Scholar
  44. Rahimtula, A.D., Hawco, F.J., andO'Brien, P.J. 1978. Involvement of (1O2) in inactivation of mixed-function oxidase and peroxidation of membrane lipids during photosensitized oxidation of liver microsomes.Photochem. Photobiol. 28:811–815.Google Scholar
  45. Rehr, S.S., Janzen, D.H., andFeeny, P.P. 1973.l-Dopa in legume seeds: A chemical barrier to insect attack.Science 181:81–82.Google Scholar
  46. Rhoades, D.F. 1976. Integrated antiherbivore, antidesiccant and ultraviolet screening properties of creosote bush resin.Biochem. Syst. Ecol. 5:281–290.Google Scholar
  47. Rhoades, D.F. 1977. The antiherbivore chemistry ofLarrea, pp. 135–175,in T.J. Mabry, J.H. Hunziker and D.R. Difeo, Jr. (eds.). Creosote Bush, Biology and Chemistry ofLarrea in New World Deserts. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania.Google Scholar
  48. Robinson, H. 1981. A Revision of the Tribal and Subtribal Limits of the Heliantheae (Asteraceae). Smithsonian Institution Press, Washington, D.C.Google Scholar
  49. Smith, L.L., andStroud, J.P. 1978. Sterol metabolism. 42. Interception of singlet molecular oxygen by sterols.Photochem. Photobiol. 28:479–485.Google Scholar
  50. Song, P.-S., andTapley, K.J., Jr., 1979. Photochemistry and photobiology of psoralens.Photochem. Photobiol., 29:1177–1197.Google Scholar
  51. Spikes, J.D. 1977. Photosensitization, pp. 87–112,in K.C. Smith (ed.). The Science of Photobiology. Plenum Press, New York.Google Scholar
  52. Suwa, K., Kimura, T., andSchaap, A.P. 1978. Reaction of singlet oxygen with cholesterol in liposomal membranes—effect of membrane fluidity on photooxidation of cholesterol.Photochem. Photobiol. 28:469–473.Google Scholar
  53. Teng, J.I., andSmith, L.L. 1973. Sterol metabolism. 24. Unlikely participation of singlet-molecular oxygen in several enzyme oxygenations.J. Am. Chem. Soc. 95:4060–4061.Google Scholar
  54. Towers, G.H.N. 1984. Interactions of light with phytochemicals in some natural and novel systems.Can. J. Bot. 62:2900–2911.Google Scholar
  55. Towers, G.H.N., andAbramowski, Z. 1983. UV-mediated genotoxicity of furanoquinoline and of certain tryptophan-derived alkaloids.J. Nat. Prod. 46:576–581.Google Scholar
  56. Towers, G.H.N., Wat, C.-K., Graham, E.A., Bandoni, R.J., Chan, G.F.Q., Mitchell, J.C., andLam, J. 1977. UV mediated antibiotic activity of species of Compositae caused by polyacetylenic compounds.Lloydia 40:487–498.Google Scholar
  57. Towers, G.H.N., Graham, E.A., Spenser, I.D., andAbramowski, Z. 1981. Phototoxic furanoquinolines of the Rutaceae.Planta Med. J. Med. Plant. Res. 41:136–142.Google Scholar
  58. Veronese, F.M., Schiavon, O., Bevilacqua, R., Bordin, F., andRodighiero, G. 1982. Photoinactivation of enzymes by linear and angular furocoumarins.Photochem. Photobiol. 36:25–30.Google Scholar
  59. Wat, C.-K., MacRae, W.D., Yamamoto, E., Towers, G.H.N., andLam, J. 1980. Phototoxic effects of naturally occurring polyacetylenes and alpha-terthienyl on human erythrocytes.Photochem. Photobiol. 32:167–172.Google Scholar
  60. Wat, C.-K., Prasad, S.K., Graham, E.A., Partington, S., Arnason, T., andTowers, G.H.N. 1981. Photosensitization of invertebrates by natural polyacetylenes.Biochem. Syst. Ecol. 9:59–62.Google Scholar
  61. Wisdom, C.F., Smiley, J.T., andRodriguez, E. 1983. Toxicity and deterrency of sesquiterpene lactones and chromenes to the corn earworm (Lepidoptera, Noctuidae).J. Econ. Entomol. 76:993–998.Google Scholar
  62. Yamamoto, E., Wat, C.-K., MacRae, W.D., andTowers, G.H.N. 1979. Photoinactivation of human erythrocyte enzymes by alpha-terthienyl and phenylheptatriyne, naturally occurring compounds in the Asteraceae.FEBS Lett. 107:134–136.Google Scholar

Copyright information

© Plenum Publishing Corporation 1986

Authors and Affiliations

  • K. R. Downum
    • 1
  • E. Rodriguez
    • 1
  1. 1.Phytochemical Laboratory Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvine

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