Cyanogenic glucosides and plant-insect interactions

Phytochemistry

Volumn 65, Issue 3, 2004, Pages 293-306

  Zagrobelny, Mika ^a   Bak, Søren ^a   Rasmussen, Anne Vinther ^a   Jørgensen, Bodil ^a   Naumann, Clas M ^b   Møller, Birger Lindberg ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b ZOOLOGISCHES FORSCHUNGSMUSEUM ALEXANDER KOENIG   (Germany)

Author keywords

Cyanogenesis; Cyanogenic glucosides; Lepidoptera; Linamarin; Lotaustralin; Papilionoidea; Zygaenidae

Indexed keywords

CYANOGENIC GLYCOSIDE; CYTOCHROME P450; ENZYME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CATALYSIS; CHEMOTAXONOMY; CYANOGENESIS; DECARBOXYLATION; DEFENSE MECHANISM; DETOXIFICATION; ENZYME DEGRADATION; ENZYME METABOLISM; ENZYME SPECIFICITY; ENZYME SYNTHESIS; HERBIVORY; MULTIGENE FAMILY; PHYLOGENETIC TREE; PLANT DEFENSE; PLANT INSECT INTERACTION; PROTEIN HYDROLYSIS; REVIEW; STOICHIOMETRY;

ARTHROPODA; CHILOPODA; DIPLOPODA; HEXAPODA; INSECTA; LEPIDOPTERA; PAPILIONOIDEA; ZYGAENIDAE;

EID: 0742320266     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2003.10.016     Document Type: Review

References (91)

1. Andersen M.D., Busk P.K., Svendsen I., Møller B.L. Cytochromes P-450 from cassava (Manihot esculenta Crantz) catalyzing the first steps in the biosynthesis of the cyanogenic glucosides linamarin and lotaustralin. J. Biol. Chem. 275:2000;1966-1976.
2. Bak S., Kahn R.A., Nielsen H.L., Møller B.L., Halkier B.A. Cloning of three A type cytochromes P450, CYP71E1, CYP98, and CYP99 from Sorghum bicolour (L.) Moench by a PCR approach and identification by expression in Escherichia coli of CYP71E1 as a multifunctional cytochrome P450 in the biosynthesis of the cyanogenic glucoside dhurrin. Plant Mol. Biol. 36:1998;393-405.
3. Beesley S.G., Compton S.G., Jones D.A. Rhodanese in insects. J. Chem. Ecol. 11:1985;45-50.
4. Bernays E.A. Relationship between deterrence and toxicity of plant secondary compounds for the grasshopper Schistocerca americana. J. Chem. Ecol. 17:1991;2519-2526.
5. Bernays E.A., Cornelius M. Relationship between deterrence and toxicity of plant secondary compounds for the alfalfa weevil Hypera brunneipennis. Entomologia Experimentalis et Applicata. 64:1992;289-292.
6. Bordo D., Bork P. The rhodanese/Cdc25 phosphatase superfamily - sequence-structure-function relations. EMBO Reports. 3:2002;741-746.
7. Braekman J.C., Daloze D., Pasteels J.M. Cyanogenic and other glucosides in a Neo-Guinean bug Leptocoris isolata - possible precursors in its host-plant. Biochem. Syst. Ecol. 10:1982;355-364.
8. Brattsten L.B., Samuelian J.H., Long K.Y., Kincaid S.A., Evans C.K. Cyanide as a feeding stimulant for the southern armyworm, Spodoptera eridania. Ecol. Entomology. 8:1983;125-132.
9. Brown K.S., Francini R.B. Evolutionary strategies of chemical defense in aposematic butterflies. cyanogenesis in Asteraceae-feeding American Acreinae Chemoecology. 1:1990;52-56.
10. Catric P., Farnden K., Conn E.E. Cyanide metabolism in higher plants. V. The formation of asparagine from β-cyanoalanine Arch. Biochem. Biophys. 152:1972;62-69.
11. Cicek M., Blanchard D.J., Bevan D.R., Esen A. The aglycone specificity-determining sites are different in 2,4-dihydroxy-7-methoxy-1,4- benzoxazin-3-one (DIMBOA)-glucosidase (maize β-glucosidase) and dhurrinase (Sorghum β-glucosidase). J. Biol. Chem. 275:2000;20002-20011.
12. Cicek M., Esen A. Structure and expression of a dhurrinase (β-glucosidase) from Sorghum. Plant Physiol. 116:1998;1469-1478.
13. Compton S.G., Jones D.A. An investigation of the responses of herbivores to cyanogenesis in Lotus corniculatus. Biol. J. Linnean Soc. 26:1985;21-38.
14. Conn E.E. Cyanogenic compounds. Ann. Rev. Plant Physiol. 31:1980;433-451.
15. Conn E.E. The metabolism of a natural product - lessons learned from cyanogenic glycosides. Planta Medica 57, S1-S9. 1991.
16. Czjzek M., Cicek M., Zamboni V., Bevan D.R., Henrissat B., Esen A. The mechanism of substrate (aglycone) specificity in β-glucosidases is revealed by chrystal structures of mutant maize β-glucosidase-DIMBOAGlc, and -dhurrin complexes. Proc. Natl. Acad. Sci. U.S.A. 97:2000;13555-13560.
17. Davis R.H., Nahrstedt A. Linamarin and lotaustralin as the source of cyanide in Zygaena filipendulae (Lepidoptera). Comp. Biochem. Physiol. B-Biochemistry & Molecular Biology. 64:1979;395-397.
18. Davis R.H., Nahrstedt A. Occurrence and variation of the cyanogenic glucosides linamarin and lotaustralin in species of the Zygaenidae (Insecta, Lepidoptera). Comp. Biochem. Physiol. B-Biochemistry & Molecular Biology. 71:1982;329-332.
19. Davis R.H., Nahrstedt A. Cyanogenesis in insects. Kerkut G.A., Gilbert L.I. Comprehensive Insect Physiology, Biochemistry and Pharmacology. 1985;635-654 Pergamon Press, Oxford.
20. Davis R.H., Nahrstedt A. Biosynthesis of cyanogenic glucosides in butterflies and moths- effective incorporation of 2-methylpropanenitrile and 2-methylbutanenitrile into linamarin and lotaustralin by Zygaena and Heliconius species (Lepidoptera). Insect Biochem. 17:1987;689-693.
21. Duffey S.S. Cyanide and arthropods. Vennesland B., Conn E.E., Knowles C.J., Westley J., Wissing F. Cyanide in Biology. 1981;385-414 Academic Press, London.
22. Duffey S.S., Towers G.H.N. On the biochemical basis of HCN production in the millipede Harpaphe haydeniana (Xystodesmidae. Polydesmida) Can. J. Zoo. 56:1978;7-16.
23. Engler H.S., Spencer K.C., Gilbert L.E. Insect metabolism - preventing cyanide release from leaves. Nature. 406:2000;144-145.
24. Esen A. β-Glucosidases - overview. ACS. Symp. Series. 533:1993;1-14.
25. Feyereisen R. Insect P450 enzymes. Ann. Rev. Entomology. 44:1999;507-533.
26. Franzl S., Ackermann I., Nahrstedt A. Purification and characterization of a β-glucosidase (linamarase) from the haemolymph of Zygaena trifolii Esper, 1783 (Insecta, Lepidoptera). Experientia. 45:1989;712-718.
27. Franzl S., Nahrstedt A., Naumann C.M. Evidence for site of biosynthesis and transport of the cyanoglucosides linamarin and lotaustralin in larvae of Zygaena trifolii (Insecta, Lepidoptera). J. Insect Physiol. 32:1986;705-709.
28. Franzl S., Naumann C.M. Cuticular cavities - storage chambers for cyanoglucoside - containing defensive secretions in larvae of a Zygaenid moth. Tissue & Cell. 17:1985;267-278.
29. Franzl S., Naumann C.M., Nahrstedt A. Cyanoglucoside storing cuticle of Zygaena larvae (Insecta, Lepidoptera) - morphological and cyanoglucoside changes during the molt. Zoomorphology. 108:1988;183-190.
30. Gaunt M.W., Miles M.A. An insect molecular clock dates the origin of the insects and accords with paleantological and biogeographic landmarks. Mol. Biol. Evol. 19:2002;748-761.
31. Gebrehiwot L., Beuselinck P.R. Seasonal variations in hydrogen cyanide concentration of three Lotus species. Agronomy J. 93:2001;603-608.
32. Gleadow R.M., Woodrow I.E. Constraints on effectiveness of cyanogenic glycosides in herbivore defense. J. Chem. Ecol. 28:2002;1301-1313.
33. Halkier B.A. Catalytic reactivities and structure/function relationships of cytochrome P450 enzymes. Phytochemistry. 43:1996;1-21.
34. Halkier B.A., Møller B.L. Biosynthesis of the cyanogenic glucoside dhurrin in seedlings of Sorghum bicolour (L.) Moench and partial purification of the enzyme system involved. Plant Physiol. 90:1989;1552-1559.
35. Hansen K.S., Kristensen C., Tattersall D.B., Jones P.R., Olsen C.E., Bak S. Møller, B. L., The in vitro substrate regiospecificity of UGT85B1, the cyanohydrin glucosyltransferase from Sorghum bicolour. Phytochemistry. 64:2003;143-151.
36. Hickel A., Hasslacher M., Griengl H. Hydroxynitrile lyases. functions and properties Physiologia Plantarum. 98:1996;891-898.
37. Holzkamp G., Nahrstedt A. Biosynthesis of cyanogenic glucosides in the Lepidoptera - incorporation of [U-C-14]-2-methylpropanealdoxime, 2S-[U-C-14]-methylbutanealdoxime and D,L-[U-C-14]-N-hydroxyisoleucine into linamarin and lotaustralin by the larvae of Zygaena trifolii. Insect Biochem. Mol. Biol. 24:1994;161-165.
38. Hösel W., Conn E.E. The aglycone specificity of plant β-glucosidases. Trends Biochem. Sci. 7:1982;219-221.
39. Hösel W., Tober I., Eklund S.H., Conn E.E. Characterization of β-glucosidases with high specificity for the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench seedlings. Arch. Biochem. Biophys. 252:1987;152-162.
40. Hu Z., Poulton J.E. Sequencing, genomic organization, and preliminary promoter analyses of a black cherry (R)-(+)-mandelonitrile lyase gene. Plant Physiol. 115:1997;1359-1369.
41. Hu Z., Poulton J.E. Molecular analysis of (R)-(+)-mandelonitrile lyase microheterogeneity in black cherry. Plant Physiol. 11:1999;1535-1546.
42. Ikegami F., Murakoshi I. Enzyme synthesis of non-protein β-substituted alanines and some higher homologues in plants. Phytochemistry. 35:1994;1089-1104.
43. Ikegami F., Takayama K., Murakoshi I. Purification and properties of β-cyanoalanine synthase from Lathyrus latifolius. Phytochemistry. 27:1988;3385-3389.
44. Jones D.A. Cyanogenesis in animal-plant interactions. Ciba. Found. Symp. 140:1988;151-170.
45. Jones D.A., Rothschild M., Parsons J. Release of hydrocyanic acid from crushed tissues of all stages in life-cycle of species of Zygaeninae (Lepidoptera). Nature. 193:1962;52.
46. Jones D.A. Selective eating of the acyanogenic form of the plant Lotus corniculatus by various animals. Nature. 4820:1962;1109-1110.
47. Jones P.R., Andersen M.D., Nielsen J.S., Høj P.B., Møller B.L. The biosynthesis, degradation, transport and possible function of cyanogenic glucosides. Romero J.T., Ibrahim R., Varin L., De Luca V. Evolution of metabolic pathways. 2000;191-247 Elsevier Science, New York.
48. Jones P.R., Møller B.L., Høj P.B. The UDP-glucose :p-hydroxymandelonitrile-O-glucosyltransferase that catalyzes the last step in synthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor - isolation, cloning, heterologous expression, and substrate specificity. J. Biol. Chem. 274:1999;35483-35491.
49. Kahn R.A., Bak S., Svendsen I., Halkier B.A., Møller B.L. Isolation and reconstitution of cytochrome P450ox and in vitro reconstitution of the entire biosynthetic pathway of the cyanogenic glucoside dhurrin from sorghum. Plant Physiol. 115:1997;1661-1670.
50. Lechtenberg M., Nahrstedt A. Cyanogenic glucosides. Ikan R. Naturally Occurring Glycosides. 1999;147-191 John Wiley & Sons, New York.
51. Levinson N.Z., Kaissling K.-E., Levinson A.R. Olfaction and cyanide sensitivity in the six-spot burnet moth Zygaena fillipendulae and the silk moth Bombyx mori. J. Comp. Physiol. 86:1973;209-215.
52. Meyers D., Ahmad S. Link between L-3-cyanoalanine synthase activity and differential cyanide sensitivity of insects. Biochim. Biophys. Acta. 1075:1991;195-197.
53. Miller J.M., Conn E.E. Metabolism of hydrogen cyanide by higher plants. Plant Physiol. 65:1980;1199-1202.
54. Møller B.L., Conn E.E. The biosynthesis of cyanogenic glucosides in higher plants. Channeling of intermediates in dhurrin biosynthesis by a microsomal system from Sorghum bicolor (L.). Moench. J. Biol. Chem. 255:1980;3049-3056.
55. Møller B.L., Poulton J.E. Cyanogenic glucosides. Lea P.J. Methods in Plant Biochemistry, vol. 9. 1993;183-207 Academic Press, San Diego.
56. Møller B.L., Seigler D.S. Biosynthesis of cyanogenic glucosides, cyanolipids and related compounds. Singh B.K. Plant Amino Acids. 1999;563-609 M. Dekker, New York.
57. Morant M., Bak S., Møller B.L., Werck-Reichhart D. Plant cytochromes P450: tools for pharmacology, plant protection and phytomediation. Curr. Op. Biotechnology. 14:2003;151-162.
58. Müller E., Nahrstedt A. Purification and characterization of an α-hydroxynitrile lyase from the haemolymph of the larvae of Zygaena trifolii. Planta Medica. 56:1990;611-612.
59. Müller T., Ockenfels P., Naumann C.M. Olfactory discrimination between host- and non-host-plants in Zygaena trifolii (Esper, 1783) and Z. transalpiina (Esper, 1780) (Lepidoptera, Zygaenidae). Tremewan W.G., Wipking W., Naumann C.M. Proceedings of the 5th International Symposium on the Biology of the Zygaenidae (Insecta, Lepidoptera). 1993;125-137 Koeltz Scientific Books, Grietherbusch (Germany).
60. Nahrstedt A. Cyanogenic compounds as protecting agents for organisms. Plant Syst. Evol. 150:1985;35-47.
61. Nahrstedt A. Cyanogenesis and the role of cyanogenic compounds in insects. Ciba. Found. Symp. 140:1988;131-150.
62. Nahrstedt A. The significance of secondary metabolites for interactions between plants and insects. Planta Medica. 1989;333-338.
63. Nahrstedt A. Cyanogenesis in the Zygaenidae (Lepidoptera): a review of the state of the art. Tremewan W.G., Wipking W., Naumann C.M. Proceedings of the 5th International Symposium on the Biology of the Zygaenidae (Insecta, Lepidoptera). 1993;17-29 Koeltz Scientific Books, Grietherbusch (Germany).
64. Nahrstedt A. Relationships between the defensive systems of plants and insects. Romeo X., Saunders X., Barbossa X. Recent Advances in Phytochemistry. 1996;217-230 Plenum Press, New York.
65. Nahrstedt A., Davis R.H. The occurrence of the cyanoglucosides, linamarin and lotaustralin, in Acraea and Heliconius butterflies. Comp. Biochem. Physiol. B - Biochemistry & Molecular Biology. 68:1981;575-577.
66. Nahrstedt A., Davis R.H. Occurrence, variation and biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in species of the Heliconiini (Insecta, Lepidoptera). Comp. Biochem. Physiol. B - Biochemistry & Molecular Biology. 75:1983;65-73.
67. Nahrstedt A., Davis R.H. Biosynthesis and quantitative relationships of the cyanogenic glucosides, linamarin and lotaustralin, in genera of the Heliconiini (Insecta, Lepidoptera). Comp. Biochem. Physiol. B - Biochemistry & Molecular Biology. 82:1985;745-749.
68. Nahrstedt A., Müller E. β-Glucosidase (linamarase) of the larvae of the moth Zygaena trifolii and its inhibition by some alkaline-earth metal-ions. ACS. Symp. Series. 533:1993;132-144.
69. Naumann C.M., Tarmann G.M., Tremewan W.G. The Western Palaearctic Zygaenidae: (Lepidoptera). 1999;Apollo Books, Stenstrup, Denmark.
70. Paquette S.M., Møller B.L., Bak S. On the origin of family 1 plant glycosyltransferases. Phytochemistry. 62:2003;399-413.
71. Poulton J.E. Cyanogenesis in plants. Plant Physiol. 94:1990;401-405.
72. Ranson H., Claudianos C., Ortelli F., Abgrall C., Hemingway J., Sharakhova M.V., Unger M.F., Collins F.H., Feyereisen R. Evolution of supergene families associated with insecticide resistance. Science. 298:2002;179-181.
73. Ressler C., Nigam S., Giza Y. Toxic principle in vetch. isolation and identification of γ-L-glutamyl-L-β-cyanoalanine from common vetch seeds: distribution in some legumes J. Amer. Chem. Soc. 91:1969;2758-2765.
74. Schappert P.J., Shore J.S. Effects of cyanogenesis polymorphism in Turnera ulmifolia on Euptoieta hegesia and potential Anolis predators. J. Chem. Ecol. 25:1999;1455-1479.
75. Sibbesen O., Koch B., Halkier B.A. Møller, B. L., Isolation of the heme-thiolate enzyme cytochrome P450Tyr, which catalyzes the committed step in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. Proc. Natl. Acad. Sci. USA. 91:1994;9740-9744.
76. Swain, E., Li, C.P., Poulton, J.E., 1992. Tissue and subcellular localization of enzymes catabolizing (R)-amygdalin in mature Prunus serotina seeds. Plant Physiol. 100, 291-300.
77. Tattersall, D.B., Bak, S., Jones, P.R., Olsen, C.E., Nielsen, J.K., Hansen, M.L., Høj, P.B., Møller, B.L., 2001. Resistance to an herbivore through engineered cyanogenic glucoside synthesis. Science 293, 1826-1828.
78. Tattersall, D.B., Nielsen, K.A., Jones, P.R., Møller, B.L., 2003. Metabolon formation in dhurrin biosynthesis as documented by confocal laser scanning microscopy. Plant Cell (in press).
79. Tijet N., Helvig C., Feyereisen R. The cytochrome P450 gene superfamily in Drosophila melanogaster. annotation, intron-exon organization and phylogeny Gene. 262:2001;189-198.
80. Trummler K., Wajant H. Molecular cloning of acetone cyanohydrin lyase from flax (Linum usitatissimum). Definition of a novel class of hydroxynitrile lyases. J. Biol. Chem. 272:1997;4770-4774.
81. Vetter J. Plant cyanogenic glycosides. Toxicon. 38:2000;11-36.
82. Vogt T., Jones P. Glycosyltransferases in plant natural product synthesis. characterization of a supergene family Trends Plant Sci. 5:2000;380-386.
83. Wajant H., Pfizenmaier K. Identification of potential active-site residues in the hydroxynitrile lyase from Manihot esculenta by site-directed mutagenesis. J. Biol. Chem. 271:1996;25830-25834.
84. Werck-Reichhart D., Bak S., Paquette S.M. Cytochromes P450. Somerville C.R., Meyerowitz E.M. The Arabidopsis Book. 2002;1-28 American Society of Plant Biologists, Rockville. (tab.0028, http://www.aspb.org/publications/arabidosis/ ).
85. Werck-Reichhart D., Feyereisen R. Cytochromes P450. a success story Genome Biology. 1:2000;3003.1-3003.9.
86. Werck-Reichhart D., Hehn A., Didierjean L. Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci. 5:2000;116-123.
87. Witthohn K., Naumann C.M. Qualitative and quantitative studies on the compounds of the larval defensive secretion of Zygaena trifolii (Esper, 1783) (Insecta, Lepidoptera, Zygaenidae). Comp. Biochem. Physiol. C - Pharmacology Toxicology & Endocrinology. 79:1984;103-106.
88. Witthohn K., Naumann C.M. Cyanogenesis - a general phenomenon in the Lepidoptera. J. Chem. Ecol. 13:1987;1789-1809.
89. Witthohn K., Naumann C.M. Genus Zygaena F and related taxa (Insecta, Lepidoptera). 53. Active cyanogenesis - in Zygaenids and other Lepidoptera. Z. Naturforsch. 42c:1987;1319-1322.
90. Wray V., Davis R.H., Nahrstedt A. Biosynthesis of cyanogenic glycosides in butterflies and moths - incorporation of valine and isoleucine into linamarin and lotaustralin by Zygaena and Heliconius species (Lepidoptera). Z. Naturforsch. 38c:1983;583-588.
91. Yip W.-K., Yang S. Cyanide metabolism in relation to ethylene production in plant tissues. Plant Physiol. 88:1988;473-476.