Complex metabolism of aromatic glucosinolates in Pieris rapae caterpillars involving nitrile formation, hydroxylation, demethylation, sulfation, and host plant dependent carboxylic acid formation

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 2, 2010, Pages 126-137

  Agerbirk, Niels ^a   Olsen, Carl Erik ^a   Poulsen, Eva ^a   Jacobsen, Niels ^a   Hansen, Paul Robert ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Carboxylic acid; Detoxification; Glucosinolate; Nitrilase; Nitrile; Nitrile specifier protein; O Demethylase; P450; Sulfate conjugate

Indexed keywords

CARBOXYLIC ACID; GLUCOSINOLATE; NITRILE; SULFATE;

ANIMAL; ARTICLE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROXYLATION; METABOLISM; METHODOLOGY; METHYLATION; MOTH; PARASITOLOGY; PLANT; SPECTROSCOPY;

ANIMALS; CARBOXYLIC ACIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GLUCOSINOLATES; HYDROXYLATION; METHYLATION; MOTHS; NITRILES; PLANTS; SPECTRUM ANALYSIS; SULFATES;

ARABIS; ARABIS HIRSUTA; ARABIS SOYERI; BRASSICACEAE; PIERIS RAPAE;

EID: 76849103675     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.01.003     Document Type: Article

References (53)

1. Agerbirk N., Olsen C.E., and Nielsen J.K. Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58 (2001) 91-100
2. Agerbirk N., Ørgaard M., and Nielsen J.K. Glucosinolates, flea beetle resistance, and leaf pubescense as taxonomic characters in the genus Barbarea. Phytochemistry 63 (2003) 69-80
3. Agerbirk N., Müller C., Olsen C.E., and Chew F. A common pathway for metabolism of 4-hydroxybenzylglucosinolate in Pieris and Anthocaris (Lepidoptera: Pieridae). Biochem. Syst. Ecol. 34 (2006) 189-198
4. Agerbirk N., Olsen C.E., Topbjerg H.B., and Sørensen J.C. Host plant dependent metabolism of 4-hydroxybenzylglucosinolate in Pieris rapae: substrate specificity and effects of genetic modification and plant nitrile hydratase. Insect Biochem. Mol. Biol. 37 (2007) 1119-1130
5. Agerbirk N., Warwick S.I., Hansen P.R., and Olsen C.E. Sinapis phylogeny and evolution of glucosinolates and specific nitrile degrading enzymes. Phytochemistry 69 (2008) 2937-2949
6. Andersson J., Borg-Karlson A.-K., and Wiklund C. Antiaphrodisiacs in pierid butterflies: a theme with variation. J. Chem. Ecol. 29 (2003) 1489-1499
7. Bak S., Olsen C.E., Petersen B.L., Møller B.L., and Halkier B.A. Metabolic engineering of p-hydroxybenzylglucosinolate in Arabidopsis by expression of the cyanogenic CYP79A1 from Sorghum bicolor. Plant J. 20 (1999) 663-671
8. Becerra J.X., Noge K., and Venable D.L. Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 18062-18066
9. Bennett R., Mellon F.A., and Kroon P.A. Screening crucifer seeds as sources of specific intact glucosinolates using ion-pair high-performance liquid chromatography negative ion electrospray mass spectrometry. J. Agric. Food Chem. 52 (2004) 428-438
10. Berenbaum M., and Feeny P. Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race?. Science 212 (1981) 927-929
11. Brader G., Mikkelsen M.D., Halkier B.A., and Palva E.T. Altering glucosinolate profiles modulates disease resistance in plants. Plant J. 46 (2006) 758-767
12. Brattsten L.B. Metabolic defences against plant allelochemicals. In: Rosenthal G.A., and Berenbaum M.R. (Eds). Herbivores and Their Interactions with Secondary Plant Metabolites vol. 2 (1992), Academic Press, USA, New York 175-242
13. Burow M., Losansky A., Müller R., Plock A., Kliebenstein D.J., and Wittstock U. The genetic basis of constitutive and herbivore-induced ESP-independent nitrile formation in Arabidopsis. Plant Physiol. 149 (2009) 561-574
14. Burow M., Müller R., Gershenzon J., and Wittstock U. Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis. J. Chem. Ecol. 32 (2006) 2333-2349
15. Crozier A., Jaganath I.B., and Clifford M.N. Dietary phenolics: chemistry, bioavailability and effects on health. Nat. Prod. Rep. 26 (2009) 1001-1043
16. Cullen J. Arabis L. In: Davis P.H. (Ed). Flora of Turkey vol. 1 (1965) 422-429
17. Despres L., David J.-P., and Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22 (2007) 298-307
18. De Vos M., Kriksunov K.L., and Jander G. Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae. Plant Physiol. 146 (2008) 916-926
19. Donnini S., Finetti F., Lusini L., Morbidelli L., Cheynier V., Barron D., Williamson G., Waltenberger J., and Ziche M. Divergent effects of quercetin conjugates on angiogenesis. Br. J. Nutr. 95 (2006) 1016-1023
20. Fatouros N.E., Huigens M.E., van Loon J.J.A., Dicke M., and Hilker M. Butterfly anti-aphrodisiac lures parasitic wasps. Nature 433 (2005) 704
21. Fatouros N.E., Broekgaarden C., Bukovinszkine'Kiss G., van Loon J.J.A., Mumm R., Huigens M.E., Dicke M., and Hilker M. Male-derived butterfly anto-aphrodisiac mediates induced indirect plant defense. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 10033-10038
22. Ferreres F., Valentao P., Pereira J.A., Bento A., Noites A., Seabra R.M., and Andrade P.A. HPLC-DAD-MS/MS-ESI screening of phenolic compounds in Pieris brassicae L. reared on Brassica rapa var. rapa L. J. Agric. Food Chem. 56 (2008) 844-853
23. Felgines C., Talavera S., Gonthier M.-P., Texier O., Scalbert A., Lamaison J.-L., and Remesy C. Strawberry anthocyanins are recovered in urine as glucuro- and sulfoconjugates in humans. J. Nutr. 133 (2003) 1296-1301
24. Feyereisen R. Insect P450 enzymes. Annu. Rev. Entomol. 44 (1999) 507-533
25. Frechard A., Fabre N., Pean C., Montaut S., Fauvel M.-T., Rollin P., and Fourasté I. Novel indole-type glucosinolates from woad (Isatis tinctoria L.). Tetrahedron Lett. 42 (2001) 9015-9017
26. Galletti S., Sala E., Leoni O., Cinti S., and Cerato C. Aspergillus flavus transformation of glucosinolates to nitriles by an arylsulfatase and a β-thio-glucosidase. Soil Biol. Biochem. 40 (2008) 2170-2173
27. Geu-Flores F., Olsen C.E., and Halkier B.A. Towards engineering glucosinolates into non-cruciferous plants. Planta 229 (2009) 261-270
28. Geu-Flores F., Nielsen M.T., Nafisi M., Møldrup M.E., Olsen C.E., Motawia M.S., and Halkier B.A. Glucosinolate engineering identifies a γ-glutamyl peptidase. Nature Chem. Biol. 5 (2009) 575-577
29. Ishikawa T., Okazaki K., Kuroda H., Itoh K., Mitsui T., and Hori H. Molecular cloning of Brassica rapa nitrilases and their expression during clubroot development. Mol. Plant Pathol. 8 (2007) 623-637
30. Janowitz T., Trompetter I., and Piotrowski M. Evolution of nitrilases in glucosinolate-containing plants. Phytochemistry 70 (2009) 1680-1686
31. Jones B.M.G., and Akeroyd J.B. Arabis L. In: Tutin T.G., et al. (Ed). Flora Europaea. second ed. vol. 1 (1993) 352-356
32. Jones C.D. The genetic basis of larval resistance to a host plant toxin in Drosophila sechellia. Genet. Res. 78 (2001) 225-233
33. Kissen R., and Bones A.M. Nitrile-specifier proteins involved in glucosinolate hydrolysis in Arabidopsis thaliana. J. Biol. Chem. 284 (2009) 12057-12070
34. Kjaer A., and Schuster A. Glucosinolates in seeds of Arabis hirsuta (L.) Scop.: some new, naturally derived isothiocyanates. Acta Chem. Scand. 26 (1972) 8-14
35. Lambrix V., Reichelt M., Mitchell-Olds T., Kliebenstein D.J., and Gershenzon J. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13 (2001) 2793-2807
36. Legal L., Moulin B., and Jallon J.M. The relation between structures and toxicity of oxygenated aliphatic compounds homologous to the insecticide octanoic acid and the chemotaxis of two species of Drosophila. Pest. Biochem. Physiol. 65 (1999) 90-101
37. Matusheski N.V., Swarup R., Juvik J.A., Mithen R., Bennett R., and Jeffery E.H. Epithiospecifier protein from broccoli (Brassica oleracea L. ssp. italica) inhibits formation of the anticancer agent sulforaphane. J. Agric. Food Chem. 54 (2006) 2069-2076
38. Mellon F.A., Bennett R., Holst B., and Williamson G. Intact glucosinolate analysis in plant extracts by programmed cone voltage electrospray LC/MS: performance and comparison with LC/MS/MS methods. Anal. Biochem. 306 (2002) 83-91
39. Mullen W., Edwards C.A., and Crozier A. Absorption, excretion and metabolite profiling of methyl-, glucuronyl-, glucosyl- and sulpho-conjugates of quercetin in human plasma and urine after ingestion of onions. Br. J. Nutr. 96 (2006) 107-116
40. Müller C., Agerbirk N., and Olsen C.E. Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology 13 (2003) 47-54
41. Mumm R., Burow M., Bukovinszkine'Kiss G., Kazantzidou E., Wittstock U., Dicke M., and Gershenzon J. Formation of simple nitriles upon glucosinolate hydrolysis affects direct and indirect defense against the specialist herbivore, Pieris rapae. J. Chem. Ecol. 34 (2008) 1311-1321
42. Nardini M., Forte M., Vrhovsek U., Mattivi F., Viola R., and Scaccini C. White wine phenolics are absorbed and extensively metabolized in humans. J. Agric. Food Chem. 57 (2009) 2711-2718
43. Piotrowski M. Primary or secondary? Versatile nitrilases in plant metabolism. Phytochemistry 69 (2008) 2655-2667
44. Potter M.J., Vanstone V.A., Davies K.A., and Rathjen A.J. Breeding to increase the concentration of 2-phenylethyl glucosinolate in the roots of Brassica napus. J. Chem. Ecol. 26 (2000) 1811-1820
45. Thies W. Isolation of sinigrin and glucotropaeolin from cruciferous seeds. Fat Sci. Technol. 90 (1988) 311-314
46. Uddin M.M., Ulrichs C., Tokuhisa J.G., and Mewis I. Impact of glucosinolate structure on the performance of the crucifer pest Phaedon cochleariae (F.). J. Appl. Bot. Food Qual. 82 (2009) 108-113
47. Vergara F., Svatos A., Schneider B., Reichelt M., Gershenzon J., and Wittstock U. Glycine conjugates in a lepidopteran insect herbivore - the metabolism of benzylglucosinolate in the cabbage white butterfly, Pieris rapae. ChemBioChem 7 (2006) 1982-1989
48. Vergara F., Svatos A., Schneider B., Reichelt M., Gershenzon J., and Wittstock U. Corrigendum. ChemBioChem 8 (2007) 1751-1758
49. Vorwerk S., Biernacki S., Hillebrand H., Janzik I., Müller A., Weiler E.W., and Piotrowski M. Enzymatic characterization of the recombinant Arabidopsis thaliana nitrilase subfamily encoded by the NIT2/NIT1/NIT3-gene cluster. Planta 212 (2001) 508-516
50. Yang Y., Yue L., Chen S., and Wu Y. Functional expression of Helicoverpa armigera CYP9A12 and CYP9A14 in Saccharomyces cerevisiae. Pesticide Biochem. Physiol. 92 (2008) 101-105
51. Wathelet J.-P., Iori R., Leoni O., Rollin P., Quinsac A., and Palmieri S. Guidelines for glucosinolate analysis in green tissues used for biofumigation. Agroindustria 3 (2004) 257-266
52. Wheat C.W., Vogel H., Wittstock U., Braby M.F., Underwood D., and Mitchell-Olds T. The genetic basis of a plant-insect coevolutionary key innovation. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 20427-20431
53. Wittstock U., Agerbirk N., Stauber E., Olsen C.E., Hippler M., Mitchell-Olds T., Gershenzon J., and Vogel H. Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 4859-4864