Possible evolution of alliarinoside biosynthesis from the glucosinolate pathway in Alliaria petiolata

FEBS Journal

Volumn 279, Issue 9, 2012, Pages 1545-1562

  Frisch, Tina ^a   Møller, Birger L ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

AOP; cytochrome P450; flavin monooxygenase; hydroxynitrile glucoside; recurrent evolution

Indexed keywords

2 PROPENYLGLUCOSINOLATE; ALLIARINOSIDE; BETA HYDROXYNITRILE GLUCOSIDE; CYTOCHROME P450; GAMMA HYDROXYNITRILE GLUCOSIDE; GLUCOSIDE; GLUCOSINOLATE; GLUCURONOSYLTRANSFERASE 85B1; GLYCOSYLTRANSFERASE; HYDROGEN CYANIDE; UNCLASSIFIED DRUG;

ALLIARIA PETIOLATA; AMINO ACID SEQUENCE; BRASSICACEAE; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CATALYSIS; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; CYANOGENESIS; ENZYME ACTIVITY; MOLECULAR EVOLUTION; NONHUMAN; PHYTOCHEMISTRY; PLANT GENETICS; PRIORITY JOURNAL; REVIEW;

BRASSICACEAE; CYANIDES; CYTOCHROME P-450 ENZYME SYSTEM; EVOLUTION, MOLECULAR; GLUCOSIDES; GLUCOSINOLATES; NITRILES; OXIMES;

ALLIARIA PETIOLATA; BRASSICACEAE;

EID: 84860222540     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08469.x     Document Type: Review

References (118)

1. Fleming F, (1999) Nitrile-containing natural products. Nat Prod Rep 16, 597-606. (Pubitemid 29501614)
2. Legras JL, Chuzel G, Arnaud A, &, Galzy P, (1990) Natural nitriles and their metabolism. World J Microbiol Biotechnol 6, 83-108.
3. Bak S, Paquette S, Morant M, Morant A, Saito S, Bjarnholt N, Zagrobelny M, Jørgensen K, Osmani S, Simonsen H, et al. (2006) Cyanogenic glycosides: a case study for evolution and application of cytochromes P450. Phytochem Rev 5, 309-329. (Pubitemid 44900351)
4. Zagrobelny M, Bak S, Rasmussen AV, Jørgensen B, Naumann CM, &, Møller BL, (2004) Cyanogenic glucosides and plant-insect interactions. Phytochemistry 65, 293-306. (Pubitemid 38152973)
5. Zagrobelny M, Bak S, &, Møller BL, (2008) Cyanogenesis in plants and arthropods. Phytochemistry 69, 1457-1468.
6. Bjarnholt N, &, Møller BL, (2008) Hydroxynitrile glucosides. Phytochemistry 69, 1947-1961.
7. Mikolajczak KL, (1977) Cyanolipids. Prog Chem Fats Other Lipids 15, 97-130.
8. Halkier BA, &, Gershenzon J, (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57, 303-333. (Pubitemid 44061027)
9. Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, Halkier BA, &, Glazebrook J, (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell Online 19, 2039-2052. (Pubitemid 47218857)
10. Pedras MSC, Yaya EE, &, Glawischnig E, (2011) The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 28, 1381-1405.
11. Jensen NB, Zagrobelny M, Hjernø K, Olsen CE, Houghton-Larsen J, Borch J, Møller BL, &, Bak S, (2011) Convergent evolution in biosynthesis of cyanogenic defence compounds in plants and insects. Nat Commun 2, 273.
12. Takos AM, Knudsen C, Lai D, Kannangara R, Mikkelsen L, Motawia MS, Olsen CE, Sato S, Tabata S, Jørgensen K, et al. (2011) Genomic clustering of cyanogenic glucoside biosynthetic genes aids their identification in Lotus japonicus and suggests the repeated evolution of this chemical defence pathway. Plant J 68, 273-286.
13. Nafisi M, Sønderby I, Hansen B, Geu-Flores F, Nour-Eldin H, Nørholm M, Jensen N, Li J, &, Halkier B, (2006) Cytochromes P450 in the biosynthesis of glucosinolates and indole alkaloids. Phytochem Rev 5, 331-346. (Pubitemid 44900352)
14. Haribal M, Yang Z, Attygalle AB, Renwick JA, &, Meinwald J, (2001) A cyanoallyl glucoside from Alliaria petiolata, as a feeding deterrent for larvae of Pieris napi oleracea. J Nat Prod 64, 440-443. (Pubitemid 32423867)
15. Cipollini D, &, Gruner B, (2007) Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata. J Chem Ecol 33, 85-94. (Pubitemid 46011204)
16. Nuzzo V, (2000) Element Stewardship Abstract for Alliaria petiolata. The Nature Conservancy, Virginia.
17. Durka W, Bossforf O, Prati D, &, Auge H, (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14, 1697-1706. (Pubitemid 40623406)
18. Meekins J, Ballard H, &, McCarthy B, (2001) Genetic variation and molecular biogeography of a North American invasive plant species (Alliaria petiolata, Brassicaceae). Int J Plant Sci 162, 161-169. (Pubitemid 32116863)
19. Cipollini D, (2002) Variation in the expression of chemical defenses in Alliaria petiolata (Brassicaceae) in the field and common garden. Am J Bot 89, 1422-1430.
20. Haribal M, &, Renwick JA, (1998) Isovitexin 6''-O-[beta]-d- glucopyranoside: a feeding deterrent to Pieris napi oleracea from Alliaria petiolata. Phytochemistry 47, 1237-1240. (Pubitemid 28232505)
21. Renwick JA, Zhang W, Haribal M, Attygalle AB, &, Lopez KD, (2001) Dual chemical barriers protect a plant against different larval stages of an insect. J Chem Ecol 27, 1575-1583. (Pubitemid 32734759)
22. Barto EK, Powell JR, &, Cipollini D, (2010) How novel are the chemical weapons of garlic mustard in North American forest understories? Biol Invasions 12, 3465-3471.
23. Barto KE, &, Cipollini D, (2009) Half-lives and field soil concentrations of Alliaria petiolata secondary metabolites. Chemosphere 76, 71-75.
24. Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, &, Klironomos J, (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89, 1043-1055. (Pubitemid 351620069)
25. Cantor A, Hale A, Aaron J, Traw M, &, Kalisz S, (2011) Low allelochemical concentrations detected in garlic mustard-invaded forest soils inhibit fungal growth and AMF spore germination. Biol Invasions 13, 3015-3025.
26. Prati D, &, Bossdorf O, (2004) Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91, 285-288. (Pubitemid 38261484)
27. Rodgers V, Wolfe B, Werden L, &, Finzi A, (2008) The invasive species Alliaria petiolata (garlic mustard) increases soil nutrient availability in northern hardwood-conifer forests. Oecologia 157, 459-471.
28. Vaughn SF, &, Berhow MA, (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25, 2495-2504. (Pubitemid 29529946)
29. Lin CN, Kuo SH, Chung MI, Ko FN, &, Teng CM, (1997) A new flavone C-glycoside and antiplatelet and vasorelaxing flavones from Gentiana arisanensis. J Nat Prod 60, 851-853.
30. Agerbirk N, Chew FS, Olsen CE, &, Jørgensen K, (2010) Leaf and floral parts feeding by orange tip butterfly larvae depends on larval position but not on glucosinolate profile or nitrogen level. J Chem Ecol 36, 1335-1345.
31. Huang X, Renwick JAA, &, Chew FS, (1994) Oviposition stimulants and deterrents control acceptance of Alliaria petiolata by Pieris rapae and P. napi oleracea. Chemoecology 5, 79-87.
32. Kjær A, (1960) Naturally derived isothiocyanates (mustard oils) and their parent glucosides. In Fortschritte der Chemie Organischer Naturstoffe (, Zechmeister L, ed), pp. 122-176. Springer, Wien.
33. Opitz S, Jensen S, &, Müller C, (2010) Sequestration of glucosinolates and iridoid glucosides in sawfly species of the genus Athalia and their role in defense against ants. J Chem Ecol 36, 148-157.
34. Brown PD, Tokuhisa JG, Reichelt M, &, Gershenzon J, (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62, 471-481. (Pubitemid 36168949)
35. Petersen B, Chen S, Hansen C, Olsen C, &, Halkier B, (2002) Composition and content of glucosinolates in developing Arabidopsis thaliana. Planta 214, 562-571. (Pubitemid 40831771)
36. Blazevic I, &, Mastelic J, (2008) Free and bound volatiles of garlic mustard (Alliaria petiolata). Croatica Chemica Acta 81, 607-613.
37. Cole RA, (1975) 1-cyanoepithioalkanes: major products of alkenylglucosinolate hydrolysis in certain cruciferae. Phytochemistry 14, 2293-2294.
38. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, Gershenzon J, &, Mitchell-Olds T, (2001) Genetic control of natural variation in arabidopsis glucosinolate accumulation. Plant Physiol 126, 811-825. (Pubitemid 32566630)
39. Cipollini D, Mbagwu J, Barto K, Hillstrom C, &, Enright S, (2005) Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. J Chem Ecol 31, 1255-1267. (Pubitemid 40837298)
40. Haribal M, &, Renwick J, (2001) Seasonal and population variation in flavonoid and alliarinoside content of Alliaria petiolata. J Chem Ecol 27, 1585-1594. (Pubitemid 32734760)
41. Durka W, Bossdorf O, &, Gautschi B, (2004) Isolation and characterization of microsatellite loci in the invasive Alliaria petiolata (Brassicaceae). Mol Ecol Notes 4, 173-175. (Pubitemid 38688975)
42. Weiss-Schneeweiss H, &, Schneeweiss G, (2003) Karyological investigations of selected angiosperms from Georgia and Azerbaijan. Acta Biol Crac 45, 49-56. (Pubitemid 39403955)
43. Gadella TWJ, &, Kliphuis E, (1966) Chromosome numbers of flowering plants in the Netherlands II. Proc K Ned Akad Wet C 69, 541-556.
44. Møller BL, (2010) Functional diversifications of cyanogenic glucosides. Curr Opin Plant Biol 13, 337-346.
45. Lechtenberg M, &, Nahrstedt A, (1999) Cyanogenic glycosides. In Naturally Occurring Glycosides (, Ikan R, ed.), pp. 147-191. Wiley, Chichester.
46. Spencer KC, (1988) Chemical mediation of coevolution in the Passiflora-Heliconius interaction. In Chemical Mediation of Coevolution (, Spencer KC, ed.), pp. 167-240. Academic Press, London.
47. Bak S, Kahn RA, Nielsen HL, Møller BL, &, Halkier BA, (1998) Cloning of three A-type cytochromes P450, CYP71E1, CYP98, and CYP99 from Sorghum bicolor (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, 393-405. (Pubitemid 28077013)
48. Kahn RA, Bak S, Svendsen I, Halkier BA, &, Møller BL, (1997) 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, 1661-1670. (Pubitemid 28395270)
49. Kahn RA, Fahrendorf T, Halkier BA, &, Møller BL, (1999) Substrate specificity of the cytochrome P450 enzymes CYP79A1 and CYP71E1 involved in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. Arch Biochem Biophys 363, 9-18. (Pubitemid 29394325)
50. Møller BL, &, Conn EE, (1980) The biosynthesis of cyanogenic glucosides in higher plants. Channeling of intermediates in dhurrin biosynthesis by a microsomal system from Sorghum bicolor (linn) Moench. J Biol Chem 255, 3049-3056.
51. Sibbesen O, Koch B, Halkier BA, &, Møller BL, (1994) Isolation of the heme-thiolate enzyme cytochrome P-450TYR, which catalyzes the committed step in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. Proc Nat Acad Sci USA 91, 9740-9744.
52. Sibbesen O, Koch B, Halkier BA, &, Møller BL, (1995) Cytochrome P-450 is a multifunctional heme-thiolate enzyme catalyzing the conversion of L-tyrosine to p-hydroxyphenylacetaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. J Biol Chem 270, 3506-3511.
53. Hansen KS, Kristensen C, Tattersall DB, Jones PR, Olsen CE, Bak S, &, Møller BL, (2003) The in vitro substrate regiospecificity of recombinant UGT85B1, the cyanohydrin glucosyltransferase from Sorghum bicolor. Phytochemistry 64, 143-151. (Pubitemid 37101800)
54. Jones PR, Møller BL, &, Høj PB, (1999) The UDP-glucose:p-hydroxymandelonitrile-O-glucosyltransferase that catalyzes the last step in synthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor. J Biol Chem 274, 35483-35491. (Pubitemid 129512841)
55. Thorsøe KS, Bak S, Olsen CE, Imberty A, Breton C, &, Lindberg Møller B, (2005) Determination of catalytic key amino acids and UDP sugar donor specificity of the cyanohydrin glycosyltransferase UGT85B1 from Sorghum bicolor. Molecular modeling substantiated by site-specific mutagenesis and biochemical analyses. Plant Physiol 139, 664-673. (Pubitemid 43907097)
56. Andersen MD, Busk PK, Svendsen I, &, Møller BL, (2000) 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, 1966-1975.
57. Forslund K, Morant M, Jorgensen B, Olsen CE, Asamizu E, Sato S, Tabata S, &, Bak S, (2004) Biosynthesis of the nitrile glucosides rhodiocyanoside A and D and the cyanogenic glucosides lotaustralin and linamarin in Lotus japonicus. Plant Physiol 135, 71-84. (Pubitemid 38653654)
58. Jørgensen K, Morant AV, Morant M, Jensen NB, Olsen CE, Kannangara R, Motawia MS, Møller BL, &, Bak S, (2011) Biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in cassava: isolation, biochemical characterization, and expression pattern of CYP71E7, the oxime-metabolizing cytochrome P450 enzyme. Plant Physiol 155, 282-292.
59. Kannangara R, Motawia MS, Hansen NKK, Paquette SM, Olsen CE, Møller BL, &, Jørgensen K, (2011) Characterization and expression profile of two UDP-glucosyltransferases, UGT85K4 and UGT85K5, catalyzing the last step in cyanogenic glucoside biosynthesis in cassava. Plant J 68, 287-301.
60. Sanchez-Perez R, Jørgensen K, Olsen CE, Dicenta F, &, Møller BL, (2008) Bitterness in almonds. Plant Physiol 146, 1040-1052. (Pubitemid 352844121)
61. Bjarnholt N, Rook F, Motawia MS, Cornett C, Jørgensen C, Olsen CE, Jaroszewski JW, Bak S, &, Møller BL, (2008) Diversification of an ancient theme: hydroxynitrile glucosides. Phytochemistry 69, 1507-1516.
62. Cutler AJ, &, Conn EE, (1981) The biosynthesis of cyanogenic glucosides in Linum usitatissimum (linen flax) in vitro. Arch Biochem Biophys 212, 468-474.
63. Nielsen JS, &, Møller BL, (2000) Cloning and expression of cytochrome P450 enzymes catalyzing the conversion of tyrosine to p-hydroxyphenylacetaldoxime in the biosynthesis of cyanogenic glucosides in Triglochin maritima. Plant Physiol 122, 1311-1322.
64. Nielsen JS, &, Møller BL, (1999) Biosynthesis of cyanogenic glucosides in Triglochin maritima and the involvement of cytochrome P450 enzymes. Arch Biochem Biophys 368, 121-130. (Pubitemid 29372312)
65. Nielsen KA, Olsen CE, Pontoppidan K, &, Møller BL, (2002) Leucine-derived cyano glucosides in barley. Plant Physiol 129, 1066-1075. (Pubitemid 34801078)
66. Olsen KM, Hsu SC, &, Small LL, (2008) Evidence on the molecular basis of the ac/ac adaptive cyanogenesis polymorphism in white clover (Trifolium repens L.). Genetics 179, 517-526.
67. Nelson D, &, Werck-Reichhart D, (2011) A P450-centric view of plant evolution. Plant J 66, 194-211.
68. Morant AV, Bjarnholt N, Kragh ME, Kjærgaard CH, Jørgensen K, Paquette SM, Piotrowski M, Imberty A, Olsen CE, Møller BL, et al. (2008) The β-glucosidases responsible for bioactivation of hydroxynitrile glucosides in Lotus japonicus. Plant Physiol 147, 1072-1091. (Pubitemid 352844263)
69. Takos A, Lai D, Mikkelsen L, bou Hachem M, Shelton D, Motawia MS, Olsen CE, Wang TL, Martin C, &, Rook F, (2010) Genetic screening identifies cyanogenesis-deficient mutants of Lotus japonicus and reveals enzymatic specificity in hydroxynitrile glucoside metabolism. Plant Cell 22, 1605-1619.
70. Franzl S, Ackermann I, &, Nahrstedt A, (1989) Purification and characterization of a beta-glucosidase (linamarase) from the haemolymph of Zygaena trifolii; Esper, 1783 (Insecta, Lepidoptera). Cell Mol Life Sci 45, 712-718.
71. Nielsen K, Hrmova M, Nielsen J, Forslund K, Ebert S, Olsen C, Fincher G, &, Møller B, (2006) Reconstitution of cyanogenesis in barley (Hordeum vulgare; L.) and its implications for resistance against the barley powdery mildew fungus. Planta 223, 1010-1023.
72. Slaughter JC, (1999) The naturally occurring furanones: formation and function from pheromone to food. Biological Rev 74, 259-276. (Pubitemid 29381271)
73. Sung WS, Jung HJ, Park K, Kim HS, Lee IS, &, Lee DG, (2007) 2,5-Dimethyl-4-hydroxy-3(2H)-furanone (DMHF); antimicrobial compound with cell cycle arrest in nosocomial pathogens. Life Sci 80, 586-591. (Pubitemid 46038330)
74. Fahey JW, Zalcmann AT, &, Talalay P, (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56, 5-51. (Pubitemid 32063165)
75. Rodman JE, Soltis PS, Soltis DE, Sytsma KJ, &, Karol KG, (1998) Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies. Am J Bot 85, 997-1006.
76. Kuchernig JC, Backenköhler A, Lübbecke M, Burow M, &, Wittstock U, (2011) A thiocyanate-forming protein generates multiple products upon allylglucosinolate breakdown in Thlaspi arvense. Phytochemistry 72, 1699-1709.
77. Wittstock U, &, Burow M, (2007) Tipping the scales-specifier proteins in glucosinolate hydrolysis. IUBMB Life 59, 744-751. (Pubitemid 351412075)
78. Gershenzon J, &, Müller C, (2009) Phytochemistry reviews-special issue on glucosinolates. Phytochem Rev 8, 1-2.
79. Müller C, (2009) Role of glucosinolates in plant invasiveness. Phytochem Rev 8, 227-242.
80. Sonderby IE, Geu-Flores F, &, Halkier BA, (2010) Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci 15, 283-290.
81. Hansen CH, Wittstock U, Olsen CE, Hick AJ, Pickett JA, &, Halkier BA, (2001) Cytochrome P450 CYP79F1 from Arabidopsis catalyzes the conversion of dihomomethionine and trihomomethionine to the corresponding aldoximes in the biosynthesis of aliphatic glucosinolates. J Biol Chem 276, 11078-11085. (Pubitemid 38089290)
82. Wittstock U, &, Halkier BA, (2000) Cytochrome P450 CYP79A2 from Arabidopsis thaliana L. catalyzes the conversion of l-phenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate. J Biol Chem 275, 14659-14666. (Pubitemid 30339757)
83. Bak S, &, Feyereisen R, (2001) The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis. Plant Physiol 127, 108-118. (Pubitemid 32925541)
84. Hansen CH, Du L, Naur P, Olsen CE, Axelsen KB, Hick AJ, Pickett JA, &, Halkier BA, (2001) CYP83B1 is the oxime-metabolizing enzyme in the glucosinolate pathway in Arabidopsis. J Biol Chem 276, 24790-24796.
85. Hull AK, Vij R, &, Celenza JL, (2000) Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc Nat Acad Sci USA 97, 2379-2384. (Pubitemid 30134077)
86. Mikkelsen MD, Hansen CH, Wittstock U, &, Halkier BA, (2000) Cytochrome P450 CYP79B2 from arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275, 33712-33717.
87. Naur P, Hansen CH, Bak S, Hansen BG, Jensen NB, Nielsen HL, &, Halkier BA, (2003) CYP79B1 from Sinapis alba converts tryptophan to indole-3-acetaldoxime. Arch Biochem Biophys 409, 235-241. (Pubitemid 36042921)
88. Chen S, Glawischnig E, Jørgensen K, Naur P, Jørgensen B, Olsen CE, Hansen CH, Rasmussen H, Pickett JA, &, Halkier BA, (2003) CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J 33, 923-937. (Pubitemid 36339382)
89. Zang YX, Kim DH, Park BS, &, Hong SB, (2009) Metabolic engineering of indole glucosinolates in Chinese cabbage hairy roots expressing Arabidopsis CYP79B2, CYP79B3, and CYP83B1. Biotechnol Bioprocess Eng 14, 467-473.
90. Hansen BG, Kliebenstein DJ, &, Halkier BA, (2007) Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 50, 902-910. (Pubitemid 46855038)
91. Li J, Hansen BG, Ober JA, Kliebenstein DJ, &, Halkier BA, (2008) Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol 148, 1721-1733. (Pubitemid 352847524)
92. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, &, Mitchell-Olds T, (2001) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell Online 13, 681-693. (Pubitemid 32265384)
93. Neal C, Fredericks D, Griffiths C, &, Neale A, (2010) The characterisation of AOP2: a gene associated with the biosynthesis of aliphatic alkenyl glucosinolates in Arabidopsis thaliana. BMC Plant Biol 10, 170.
94. Gao M, Li G, Yang B, McCombie WR, &, Quiros CF, (2004) Comparative analysis of a Brassica BAC clone containing several major aliphatic glucosinolate genes with its corresponding Arabidopsis sequence. Genome 47, 666-679. (Pubitemid 39342534)
95. Reintanz B, Lehnen M, Reichelt M, Gershenzon J, Kowalczyk M, Sandberg G, Godde M, Uhl R, &, Palme K, (2001) bus, a Bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13, 351-367. (Pubitemid 32207688)
96. Schlaich NL, (2007) Flavin-containing monooxygenases in plants: looking beyond detox. Trends Plant Sci 12, 412-418. (Pubitemid 47362800)
97. Geu-Flores F, Moldrup ME, Böttcher C, Olsen CE, Scheel D, &, Halkier BA, (2011) Cytosolic γ-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell Online 23, 2456-2469.
98. Koch M, Haubold B, &, Mitchell-Olds T, (2001) Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am J Bot 88, 534-544. (Pubitemid 33644899)
99. Bennett RN, Kiddle G, &, Wallsgrove RM, (1997) Biosynthesis of benzylglucosinolate, cyanogenic glucosides and phenylpropanoids in Carica papaya. Phytochemistry 45, 59-66. (Pubitemid 27175464)
100. Olafsdottir ES, Bolt Jørgensen L, &, Jaroszewski JW, (2002) Cyanogenesis in glucosinolate-producing plants: Carica papaya and Carica quercifolia. Phytochemistry 60, 269-273. (Pubitemid 34947532)
101. Saupe SG, (1981) Cyanogenic compounds and angiosperm phylogeny. In Phytochemistry and Angiosperm Phylogeny (, Young DA, &, Seigler DS, eds), pp. 80-116. Praeger, New York.
102. Seigler DS, Pauli GF, Nahrstedt A, &, Leen R, (2002) Cyanogenic allosides and glucosides from Passiflora edulis and Carica papaya. Phytochemistry 60, 873-882.
103. Spencer KC, &, Seigler DS, (1984) Cyanogenic glycosides of carica papaya and its phylogenetic position with respect to the violales and capparales. Am J Bot 71, 1444-1447.
104. Ettlinger M, &, Hodgekins J, (1956) The mustard oil of papaya seed. J Organic Chem 21, 204-205.
105. Gmelin R, &, Kjær A, (1970) Glucosinolates in the Caricaceae. Phytochemistry 9, 591-593.
106. Nahrstedt A, Walther A, &, Wray V, (1982) Sarmentosin epoxide, a new cyanogenic compound from Sedum cepaea. Phytochemistry 21, 107-110.
107. Brinker AM, &, Seigler DS, (1992) Determination of cyanide and cyanogenic glycosides from plants. In Plant Toxin Analysis (, Linskens HF, &, Jackson JF, eds), pp. 359-381. Springer, Berlin, Heidelberg.
108. Bark LS, &, Higson HG, (1963) A review of methods available for detection and determination of small amounts of cyanide. Analyst 88, 751-760.
109. Rubio R, Galceran MT, &, Rauret G, (1990) Nitriles and isonitriles as interferents in cyanide determination in polluted waters. Analyst 115, 959-963. (Pubitemid 20277046)
110. König W, (1904) Über eine neue, vom Pyridin derivierende Klasse von Farbstoffen. J Praktische Chemie 69, 105-137.
111. Lambert JL, Ramasamy J, &, Paukstelis JV, (1975) Stable reagents for the colorimetric determination of cyanide by modified Koenig reactions. Anal Chem 47, 916-918.
112. Aldridge WN, (1944) A new method for the estimation of micro quantities of cyanide and thiocyanate. Analyst 69, 262-265.
113. Epstein J, (1947) Estimation of microquantities of cyanide. Anal Chem 19, 272-274.
114. Seto Y, (2002) Peer reviewed: false cyanide detection. Anal Chem 74, 134-141.
115. Sharma A, &, Thibert RJ, (1985) The effect of barbituric acid concentration in the spectrophotometric determination of cyanide and thiocyanate by the pyridine-barbituric acid method. Microchimica Acta 85, 357-363.
116. Glawischnig E, Hansen BG, Olsen CE, &, Halkier BA, (2004) Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc Nat Acad Sci USA 101, 8245-8250. (Pubitemid 38698085)
117. Naur P, Petersen BL, Mikkelsen MD, Bak S, Rasmussen H, Olsen CE, &, Halkier BA, (2003) CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol 133, 63-72. (Pubitemid 37144082)
118. Bak S, Tax FE, Feldmann KA, Galbraith DW, &, Feyereisen R, (2001) CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13, 101-111. (Pubitemid 32177036)