Metabolomics - A robust bioanalytical approach for the discovery of the modes-of-action of pesticides: A review

Pesticide Biochemistry and Physiology

Volumn 100, Issue 2, 2011, Pages 105-117

  Aliferis, Konstantinos A ^a   Jabaji, Suha ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Bioactive compounds; Crop protection; Functional genomics; Metabolic profiling; Natural products

Indexed keywords

EID: 79955823811     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2011.03.004     Document Type: Review

References (91)

1. European Union Council Directive 91/414/EEC. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CELEX:31991L0414:EN:NOT.
2. United States Environmental Protection Agency's (US EPA), Insecticide, Fungicide, and Rodenticide Act (FIFRA). http://www.epa.gov/agriculture/lfra.html.
3. Hoy M.A. Myths, models and mitigation of resistance to pesticides. Philos. Trans. R. Soc. B - Biol. Sci. 1998, 353:1787-1795.
4. Bates S.L., Zhao J.-Z., Roush R.T., Shelton A.M. Insect resistance management in GM crops: past, present and future. Nat. Biotech. 2005, 23:57-62.
5. Ehler L.E. Integrated pest management (IPM): definition, historical development and implementation, and the other IPM. Pest Manag. Sci. 2006, 62:787-789.
6. Copping L.G., Duke S.O. Natural products that have been used commercially as crop protection agents. Pest Manag. Sci. 2007, 63:524-554.
7. Dayan F.E., Cantrell C.L., Duke S.O. Natural products in crop protection. Bioorg. Med. Chem. 2009, 17:4022-4034.
8. Hüter O. Use of natural products in the crop protection industry. Phytochem. Rev. 2011, 10.1007/s11101-010-9168-y.
9. Herbicide Resistance Action Committee (HRAC). http://www.hracglobal.com/.
10. Insecticide Resistance Action Committee (IRAC). http://www.irac-online.org.
11. Fungicicide Resistance Action Committee (FRAC). http://www.frac.info/frac/index.htm.
12. Casida J.E. Pest toxicology: the primary mechanisms of pesticide action. Chem. Res. Toxicol. 2009, 22:609-619.
13. Trethewey R.N., Krotzky A.J., Willmitzer L. Metabolic profiling: a Rosetta stone for genomics?. Curr. Opin. Plant Biol. 1999, 2:83-85.
14. Fiehn O., Kopka J., Dormann P., Altmann T., Trethewey R.N., Willmitzer L. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 2000, 18:1157-1161.
15. Allwood J.W., Ellis D.I., Goodacre R. Metabolomic technologies and their application to the study of plants and plant-host interactions. Physiol. Plant. 2008, 132:117-135.
16. Dunn W.B. Current trends and future requirements for the mass spectrometric investigation of microbial, mammalian and plant metabolomes. Phys. Biol. 2008, 5:1-24.
17. Baran R., Reindl W., Northen T.R. Mass spectrometry based metabolomics and enzymatic assays for functional genomics. Curr. Opin. Microbiol. 2009, 12:547-552.
18. Bundy J.G., Davey M.P., Viant M.R. Environmental metabolomics: a critical review and future perspectives. Metabolomics 2009, 5:3-21.
19. Carraro S., Giordano G., Reniero F., Perilongo G., Baraldi E. Metabolomics: a new frontier for research in paediatrics. J. Pediatr. 2009, 154:638-644.
20. Cevallos-Cevallos J.M., Reyes-De-Corcuera J.I., Etxeberria E., Danyluk M.D., Rodrick G.E. Metabolomic analysis in food science: a review. Trends Food Sci. Technol. 2009, 20:557-566.
21. Hunter P. Reading the metabolic fine print. The application of metabolomics to diagnostics, drug research and nutrition might be integral to improved health and personalized medicine. EMBO Rep. 2009, 10:20-23.
22. Jansen J.J., Allwood J.W., Marsden-Edwards E., van der Putten W.H., Goodacre R., van Dam N.M. Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 2009, 5:150-161.
23. Kaddurah-Daouk R., Krishnan K.R.R. Metabolomics: a global biochemical approach to the study of central nervous system diseases. Neuropsychopharmacology Rev. 2009, 34:173-186.
24. Spratlin J.L., Serkova N.J., Eckhardt S.G. Clinical applications of metabolomics in oncology: a review. Clin. Cancer Res. 2009, 15:431-440.
25. Vinayavekhin N., Homan E.A., Saghatelian A. Exploring disease through metabolomics. ACS Chem. Biol. 2010, 5:91-103.
26. Madsen R., Lundstedt T., Trygg J. Chemometrics in metabolomics - a review in human disease diagnosis. Anal. Chim. Acta 2010, 659:23-33.
27. Aliferis K.A., Chrysayi-Tokousbalides M. Metabolomics in pesticide research and development: review and future perspectives. Metabolomics 2011, 7:35-53.
28. Villas-Bôas S.G., Mas S., Akesson M., Smedsgaard J., Nielsen J. Mass spectrometry in metabolome analysis. Mass Spectrom. Rev. 2005, 24:613-646.
29. Lindon J.C., Nicholson J.K. Analytical technologies for metabonomics and metabolomics, and multi-omic information recovery. Trends Anal. Chem. 2008, 27:194-204.
30. Wishart D.S. Quantitative metabolomics using NMR. Trends Anal. Chem. 2008, 27:228-237.
31. Aranibar N., Singh B.J., Stockton G.W., Ott K.H. Automated mode of action detection by metabolic profiling. Biochem. Biophys. Res. Commun. 2001, 286:150-155.
32. Ott K.H., Aranibar N., Singh B., Stockton G.W. Metabonomics classifies pathways affected by bioactive compounds. Artificial neural network classification of NMR spectra of plant extracts. Phytochemistry 2003, 62:971-985.
33. Aliferis K.A., Chrysayi-Tokousbalides M. Metabonomic strategy for the investigation of the mode of action of the phytotoxin (5S,8R,13S,16R)-(-)-pyrenophorol using 1H nuclear magnetic resonance fingerprinting. J. Agric. Food. Chem. 2006, 54:1687-1692.
34. Aliferis K.A., Materzok S., Paziotou G., Chrysayi-Tokousbalides M. Lemna minor L. as a model organism for ecotoxicological studies performing 1H NMR fingerprinting. Chemosphere 2009, 76:967-973.
35. Oikawa A., Nakamura Y., Ogura T., Kimura A., Suzuki H., Sakurai N., Shinbo Y., Shibata D., Kanaya S., Ohta D. Clarification of pathway-specific inhibition by Fourier transform ion cyclotron resonance/mass spectrometry-based metabolic phenotyping studies. Plant Physiol. 2006, 142:398-413.
36. Bundy J.G., Lenz E.M., Bailey N.J., Gavaghan C.L., Svendsen C., Spurgeon D., Hankard P.K., Osborn D., Weeks J.M., Trauger S.A., Speir P., Sanders I., Lindon J.C., Nicholson J.K., Tang H. Metabonomic assessment of toxicity of 4-fluoroaniline, 3,5-difluoroaniline and 2-fluoro-4-methylaniline to the earthworm Eisenia veneta (Rosa): identification of new endogenous biomarkers. Environ. Toxicol. Chem. 2002, 21:1966-1972.
37. Taylor N.S., Weber R.J.M., Southam A.D., Payne T.G., Hrydziuszko O., Arvanitis T.N., Viant M.R. A new approach to toxicity testing in Daphnia magna: application of high throughput FT-ICR mass spectrometry metabolomics. Metabolomics 2009, 5:44-58.
38. Taylor N.S., Weber R.J.M., White T.A., Viant M.R. Discriminating between different acute chemical toxicities via changes in the Daphnid metabolome. Toxicol. Sci. 2010, 118:307-317.
39. Schneider D. Using Drosophila as a model insect. Nat. Rev. 2000, 1:218-226.
40. Adams M.D., Celniker S.E., Holt R.A., et al. The genome sequence of Drosophila melanogaster. Science 2000, 287:2185-2195.
41. Holt R.A., Subramanian G.M., Halpern A., et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002, 298:129-149.
42. Coquin L., Feala J.D., McCulloch A.D., Paternostro G. Metabolomic and flux-balance analysis of age-related decline of hypoxia tolerance in Drosophila muscle tissue. Mol. Syst. Biol. 2008, 4:233.
43. Malmendal A., Overgaard J., Bundy J.G., Sørensen J.G., Nielsen N.C., Loeschcke V., Holmstrup M. Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:205-212.
44. Pedersen K.S., Kristensen T.N., Loeschcke V., Petersen B.O., Duus J.O., Nielsen N.C., Malmendal A. Metabolomic signatures of inbreeding at benign and stressful temperatures in Drosophila melanogaster. Genetics 2008, 180:1233-1243.
45. Kamleh M.A., Hobani Y., Dow J.A.T., Watson D.G. Metabolomic profiling of Drosophila using liquid chromatography Fourier transform mass spectrometry. FEBS Lett. 2008, 582:2916-2922.
46. van Vliet E., Morath S., Eskes C., Linge J., Rappsilber J., Honegger P., Hartung T., Coecke S. A novel in vitro metabolomics approach for neurotoxicity testing, proof of principle for methyl mercury chloride and caffeine. Neurotoxicology 2008, 29:1-12.
47. Allen J., Davey H.M., Broadhurst D., Rowland J.J., Oliver S.G., Kell D.B. Discrimination of modes of action of antifungal substances by use of metabolic footprinting. Appl. Environ. Microbiol. 2004, 70:6157-6165.
48. Yi Z.-B., Yu Y., Liang Y.-Z., Zeng B. Evaluation of the antimicrobial mode of berberine by LC/ESI-MS combined with principal component analysis. J. Pharm. Biomed. Anal. 2007, 44:301-304.
49. Yu Y., Yi Z.-B., Liang Y.-Z. Main antimicrobial components of Tinospora capillipes, and their mode of action against Staphylococcus aureus. FEBS Lett. 2007, 581:4179-4183.
50. Matlab, MathWorks, MA, USA. http://www.mathworks.com/products/matlab/.
51. P. Simca, A.B. Umetrics, Umeå, Sweden. http://www.umetrics.com/simca.
52. Kralya J.R., Holcomba R.E., Guana Q., Henry C.S. Review: microfluidic applications in metabolomics and metabolic profiling. Anal. Chim. Acta 2009, 653:23-35.
53. Kruger N.J., Troncoso-Ponce M.A., Ratcliffe R.G. 1H NMR metabolite fingerprinting and metabolomic analysis of perchloric acid extracts from plant tissues. Nat. Protoc. 2008, 3:1001-1012.
54. Kim H.K., Choi Y.H., Verpoorte R. NMR-based metabolomic analysis of plants. Nat. Protoc. 2010, 5:536-549.
55. Biais B., Allwood J.W., Deborde C., Xu Y., Maucourt M., Beauvoit B., Dunn W.B., Jacob D., Goodacre R., Rolin D., Moing A. 1H NMR, GC-EI-TOFMS, and data set correlation for fruit metabolomics: application to spatial metabolite analysis in melon. Anal. Chem. 2009, 81:2884-2894.
56. Leon C., Rodriguez-Meizoso I., Lucio M., Garcia-Cañas V., Ibañez E., Schmitt-Kopplin P., Cifuentes A. Metabolomics of transgenic maize combining Fourier transform-ion cyclotron resonance-mass spectrometry, capillary electrophoresis-mass spectrometry and pressurized liquid extraction. J. Chromatogr. A 2009, 1216:7314-7323.
57. Aliferis K.A., Jabaji S. 1H NMR and GC-MS metabolic fingerprinting of developmental stages of Rhizoctonia solani sclerotia. Metabolomics 2010, 6:96-108.
58. Agnolet S., Jaroszewski J., Verpoorte R., Staerk D. 1H NMR-based metabolomics combined with HPLC-PDA-MS-SPE-NMR for investigation of standardized Ginkgo biloba preparations. Metabolomics 2010, 6:292-302.
59. Saito K., Matsuda F. Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol. 2010, 61:463-489.
60. Fiehn O., Robertson D., Griffin J., et al. The metabolomics standards initiative (MSI). Metabolomics 2007, 3:175-178.
61. Griffin J., Nicholls A., Daykin C., Heald S., Keun H., Schuppe-Koistinen I., Griffiths J., Cheng L., Rocca-Serra P., Rubtsov D., Robertson D. Standard reporting requirements for biological samples in metabolomics experiments: mammalian/in vivo experiments. Metabolomics 2007, 3:179-188.
62. Eriksson L., Johansson E., Kettaneh-Wold N., Wold S. Multi- and Megavariate Data Analysis. Principles and Applications 2001, Umetrics Academy, Umeå, Sweden.
63. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage Daniel, Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
64. Karp P.D., Ouzounis C.A., Moore-Kochlacs C., Goldovsky L., Kaipa P., Ahren D., Tsoka S., Darzentas N., Kunin V., Lopez-Bigas N. Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res. 2005, 19:6083-6089.
65. van Iersel M.P., Kelder T., Pico A.R. Presenting, exploring biological pathways with PathVisio. BMC Bioinform. 2008, 9:399.
66. Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K.F., Itoh M., Kawashima S., Katayama T., Araki M., Hirakawa M. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 2006, 34:D354-D357.
67. Oldiges M., Lütz S., Pflug S., Schroer K., Stein N., Wiendahl C. Metabolomics: current state and evolving methodologies and tools. Appl. Microbiol. Biotechnol. 2007, 76:495-511.
68. Tohge T., Fernie A.R. Web-based resources for mass-spectrometry-based metabolomics: a user's guide. Phytochemistry 2009, 70:450-456.
69. Kastanias M.A., Chrysayi-Tokousbalides M. Herbicidal potential of pyrenophorol isolated from a Drechslera avenae pathotype. Pest Manag. Sci. 2000, 56:227-232.
70. Gill S.S., Cowles E.A., Pietrantonio P.V. The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 1992, 37:615-634.
71. Bravo A., Gill S.S., Soberón M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 2007, 49:423-435.
72. Romeis J., Meissle M., Bigler F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 2006, 24:63-71.
73. Kos M., van Loon J.J., Dicke M., Vet L.E. Transgenic plants as vital components of integrated pest management. Trends Biotechnol. 2009, 27:621-627.
74. FAO/WHO, Safety aspects of genetically modified foods of plant origin, Report of a Joint FAO/WHO Expert Consultation on Foods Derived from Biotechnology, Geneva, Switzerland., 2000. ftp://ftp.fao.org/es/esn/food/gmreport.pdf.
75. Mahajna M., Casida J.E. Oxidative bioactivation of methamidophos insecticide: synthesis of N-hydroxymethamidophos (a candidate metabolite) and its proposed alternative reactions involving N→O rearrangement or fragmentation through a metaphosphate analogue. Chem. Res. Toxicol. 1998, 11:26-34.
76. Wing K.D., Sacher M., Kagaya Y., Tsurubuchi Y., Mulderig L., Connair M., Schnee M. Bioactivation and mode of action of the oxadiazine indoxacarb in insects. Crop Prot. 2000, 19:537-545.
77. Kenneke J.F., Ekman D.R., Mazur C.S., Konwick B.J., Fisk A.T., Avants J.K., Garrison A.W. Integration of metabolomics and in vitro metabolism assays for investigating the stereoselective transformation of triadimefon in rainbow trout. Chirality 2010, 22:183-192.
78. Rochfort S., Ezernieks V., Yen A. NMR-based metabolomics using earthworms as potential indicators for soil health. Metabolomics 2009, 5:95-107.
79. Guo Q., Sidhu J.K., Ebbels T.M.D. Validation of metabolomics for toxic mechanism of action screening with the earthworm Lumbricus rubellus. Metabolomics 2009, 5:72-83.
80. McKelvie J.R., Yuk J., Xu Y., Simpson A.J., Simpson M.J. 1H NMR and GC/MS metabolomics of earthworm responses to sub-lethal DDT and endosulfan exposure. Metabolomics 2009, 5:84-94.
81. Poynton H.C., Varshavsky J.R., Chang B., Cavigiolio G., Chan S., Holman P.S., Loguinov A.V., Bauer D.J., Komachi K., Theil E.C., Perkins E.J., Hughes O., Vulpe C.D. Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ. Sci. Technol. 2006, 41:1044-1050.
82. Hassold E., Backhaus T. Chronic toxicity of five structurally diverse demethylase-inhibiting fungicides to the crustacean Daphnia magna: a comparative assessment. Environ. Toxicol. Chem. 2009, 28:1218-1226.
83. Ward J.L., Baker J.M., Beale M.H. Recent applications of NMR spectroscopy in plant metabolomics. FEBS J. 2007, 274:1126-1131.
84. Kell D.B., Brown M., Davey H.M., Dunn W.B., Spasic I., Oliver S.G. Metabolic footprinting and systems biology: the medium is the message. Nat. Rev. Microbiol. 2005, 3:557-565.
85. Raamsdonk L.M., Teusink B., Broadhurst D. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat. Biotechnol. 2001, 19:45-50.
86. Allen J., Davey H.M., Broadhurst D., Heald J.K., Rowland J.J., Oliver S.G., Kell D.B. High-throughput characterisation of yeast mutants for functional genomics using metabolic footprinting. Nat. Biotechnol. 2003, 21:692-696.
87. Castrillo J.I., Hayes A., Mohammed S., Gaskell S.J., Oliver S.G. An optimized protocol for metabolome analysis in yeast using direct infusion electrospray mass spectrometry. Phytochemistry 2003, 62:929-937.
88. Mohler R.E., Dombek K.M., Hoggard J.C., Pierce K.M., Young E.T., Synovec R.E. Comprehensive analysis of yeast metabolite GCxGC-TOFMS data: combining discovery-mode and deconvolution chemometric software. Analyst 2007, 132:756-767.
89. Smedsgaard J., Nielsen J. Metabolite profiling of fungi and yeast: from phenotype to metabolome by MS and informatics. J. Exp. Bot. 2005, 56:273-286.
90. Forgue P., Halouska S., Werth M., Xu K., Harris S., Powers R. NMR metabolic profiling of Aspergillus nidulans to monitor drug and protein activity. J. Proteome Res. 2006, 5:1916-1923.
91. Liu Y., Wen J., Wang Y., Li Y., Xu W. Postulating modes of action of compounds with antimicrobial activities through metabolomics analysis. Chromatographia 2010, 71:253-258.