Metabolomics of genetically modified crops

International Journal of Molecular Sciences

Volumn 15, Issue 10, 2014, Pages 18941-18966

  Simó, Carolina ^a   Ibáñez, Clara ^a   Valdés, Alberto ^a   Cifuentes, Alejandro ^a   García Cañas, Virginia ^a  

^a INSTITUTE OF FOOD SCIENCE RESEARCH CIAL   (Spain)

Author keywords

Crops; Food; Genetically modified organism; Metabolomics; Transgenic

Indexed keywords

DNA MODIFICATION; GENETIC ENGINEERING; GENETIC TRANSFORMATION; MAIZE; MASS SPECTROMETRY; METABOLOMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POTATO; PRINCIPAL COMPONENT ANALYSIS; REVIEW; RICE; TRANSGENIC PLANT; WHEAT; CHEMISTRY; CROP; DEVICES; GENETICALLY MODIFIED FOOD; GENETICS; METABOLISM; PROCEDURES;

CROPS, AGRICULTURAL; FOOD, GENETICALLY MODIFIED; METABOLOMICS; PLANTS, GENETICALLY MODIFIED;

EID: 84930574811     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms151018941     Document Type: Review

References (94)

1. Lönnerdal, B. Genetically modified plants for improved trace element nutrition. J. Nutr. 2003, 133, 1490S-1493S.
2. McGloughlin, M.N. Modifying agricultural crops for improved nutrition. New Biotechnol. 2010, 30, 494-504.
3. Dunwell, J.M. Transgenic cereals: Current status and future prospects. J. Cereal Sci. 2014, 59, 419-434.
4. Cellini, F.; Chesson, A.; Colquhoun, I.; Constable, A.; Davies, H.V.; Engel, K.H.; Gatehouse, A.M.; Kärenlampi, S.; Kok, E.J.; Leguay, J.J., et al. Unintended effects and their detection in genetically modified crops. Food Chem. Toxicol. 2004, 42, 1089-1125.
5. Ioset, J.R.; Urbaniak, B.; Ndjoko-Ioset, K.; Wirth, J.; Martin, F.; Gruissem, W.; Hostettmann, K.; Sautter, C. Flavonoid profiling among wild type and related GM wheat varieties. Plant Mol. Biol. 2007, 65, 645-654.
6. Shepherd, L.V.T.; McNicol, J.W.; Razzo, R.; Taylor, M.A.; Davies, H.V. Assessing the potential for unintended effects in genetically modified potatoes perturbed in metabolic and developmental processes. Targeted analysis of key nutrients and anti-nutrients. Transgenic Res. 2006, 15, 409-425.
7. Millstone, E.; Brunner, E.; Mayer, S. Beyond “substantial equivalence”. Nature 1999, 401, 525-526.
8. EFSA. Guidance document of the Scientific Panel on Genetically Modified Organisms for the risk assessment of genetically modified plants and derived food and feed. EFSA J. 2006, 99, 1-100.
9. Ad Hoc Technical Expert Group (AHTEG). Final report of the ad hoc technical expert group on risk assessment and risk management under the Cartagena protocol on biosafety. In Proceedings of the United Nations Environment Programme Convention for Biodiversity, Ljubljana, Slovenia, 20-23 April 2010. Available online: https://www.cbd.int/doc/meetings/bs/bsrarm-02/official/bsrarm-02-05-en.pdf (accessed on 15 October 2014).
10. Chassy, B.M. Can-omics inform a food safety assessment? Regul. Toxicol. Pharmacol. 2010, 58, S62-S70.
11. Valdés, A.; Simó, C.; Ibáñez, C.; García-Cañas, V. Foodomics strategies for the analysis of transgenic foods. TrAC Trends Anal. Chem. 2013, 52, 2-15.
12. Schauer, N.; Fernie, A.R. Plant metabolomics: Towards biological function and mechanism. Trends Plant Sci. 2006, 11, 508-516.
13. Hall, R.D. Plant metabolomics: From holistic hope, to hype, to hot topic. New Phytol. 2006, 169, 453-468.
14. Harrigan, G.G.; Martino-Catt, S.; Glenn, K.C. Metabolomics, metabolic diversity and genetic variation in crops. Metabolomics 2007, 3, 259-272.
15. Dixon, R.A.; Gang, D.R.; Charlton, A.J.; Fiehn, O.; Kuiper, H.A.; Reynolds, T.L.; Tjeerdema, R.S.; Jeffery, E.H.; German, J.B.; Ridley, W.P., et al. Applications of metabolomics in agriculture. J. Agric. Food Chem. 2006, 54, 8984-8994.
16. Seger, C.; Sturm, S. Analytical aspects of plant metabolite profiling platforms: Current standings and future aims. J. Proteome Res. 2007, 6, 480-497.
17. Hegeman, A.D. Plant metabolomics-meeting the analytical challenges of comprehensive metabolite analysis. Brief. Funct. Genomics 2010, 9, 139-148.
18. Eisenreich, W.; Bacher, A. Advances of high-resolution NMR techniques in the structural and metabolic analysis of plant biochemistry. Phytochemistry 2007, 68, 2799-2815.
19. Pan, Z.; Raftery, D. Comparing and combining NMR spectroscopy and mass spectrometry in metabolomics. Anal. Bioanal. Chem. 2007, 387, 525-527.
20. García-Cañas, V.; Simó, C.; León, C.; Ibáñez, E.; Cifuentes, A. MS-based analytical methodologies to characterize genetically modified crops. Mass Spectrom. Rev. 2011, 30, 396-416.
21. Herrero, M.; Simó, C.; García-Cañas, V.; Ibáñez, E.; Cifuentes, A. Foodomics: MS-based strategies in modern food science and nutrition. Mass Spectrom. Rev. 2012, 31, 49-69.
22. Ibáñez, C.; García-Cañas, V.; Valdés, A.; Simó, C. Novel MS-based approaches and applications in food metabolomics. TrAC Trends Anal. Chem. 2013, 52, 100-111.
23. Takats, Z; Wiseman, J.M.; Cooks, R.G. Ambient mass spectrometry using desorption electrospray ionization (DESI): Instrumentation, mechanisms and applications in forensics, chemistry, and biology. J. Mass Spectrom. 2005, 40, 1261-1275.
24. Hoekenga, O.A. Using metabolomics to estimate unintended effects in transgenic crop plants: Problems, promises, and opportunities. J. Biomol. Tech. 2008, 19, 159-166.
25. Keymanesh, K.; Darvishi, M.H.; Sardari, S. Metabolome comparison of transgenic and non-transgenic rice by statistical analysis of FTIR and NMR spectra. Rice Sci. 2009, 16, 119-123.
26. Zhou, J.; Ma, C.; Xu, H.; Yuan, K.; Lu, X.; Zhu, Z.; Wu, Y.; Xu, G. Metabolic profiling of transgenic rice with cryIAc and sck genes: An evaluation of unintended effects at metabolic level by using GC-FID and GC-MS. J. Chromatogr. B 2009, 877, 725-732.
27. Shin, Y.M.; Park, H.J.; Yim, S.D.; Baek, N.I.; Lee, C.H.; An, G.; Woo, Y.M. Transgenic rice lines expressing maize C1 and R-S regulatory genes produce various flavonoids in the endosperm. Plant Biol. 2006, 4, 303-315.
28. Takahashi, H.; Hayashi, M.; Goto, F.; Sato, S.; Soga, T.; Nishioka, T.; Tomita, M.; Kawai-Yamada, M.; Uchimiya, H. Evaluation of metabolic alteration in transgenic rice overexpressing dihydroflavonol-4-reductase. Ann. Bot. 2006, 98, 819-825.
29. Jiao, Z.; Si, X.X.; Li, G.K.; Zhang, Z.M.; Xu, X.P. Unintended compositional changes in transgenic rice seeds (Oryza sativa L.) studied by spectral and chromatographic analysis coupled with chemometrics methods. J. Agric. Food Chem. 2010, 58, 1746-1754.
30. Wu, J.; Yu, H.C.; Dai, H.F.; Mei, W.L.; Huang, X.; Zhu, S.F.; Peng, M. Metabolite profiles of rice cultivars containing bacterial blight-resistant genes are distinctive from susceptible rice. Acta Biochim. Biophys. Sin. 2012, 44, 650-659.
31. Chang, Y.; Zhao, C.; Zhu, Z.; Wu, Z.; Zhou, J.; Zhao, Y.; Lu, X.; Xu, G. Metabolic profiling based on LC/MS to evaluate unintended effects of transgenic rice with cry1Ac and sck genes. Plant Mol. Biol. 2012, 78, 477-487.
32. Nagai, Y.S.; Sakulsinghroj, C.; Edwards, G.E.; Satoh, H.; Greene, T.W.; Blakeslee, B.; Okita, T.W. Control of starch synthesis in cereals: Metabolite analysis of transgenic rice expressing an up-regulated cytoplasmic ADP-Glucose pyrophosphorylase in developing seeds. Cell Physiol. 2009, 50, 635-643.
33. Matsuda, F.; Ishihara, A.; Takanashi, K.; Morino, K.; Miyazawa, H.; Wakasa, K.; Miyagawa, H. Metabolic profiling analysis of genetically modified rice seedlings that overproduce tryptophan reveals the occurrence of its inter-tissue translocation. Plant Biotechnol. 2010, 27, 17-27.
34. Kim, J.K.; Park, S.Y.; Lee, S.M.; Lim, S.-H.; Kim, H.J.; Oh, S.-D.; Yeo, Y.; Cho, H.S.; Ha, S.H. Unintended polar metabolite profiling of carotenoid-biofortified transgenic rice reveals substantial equivalence to its non-transgenic counterpart. Plant Biotechnol. Rep. 2013, 7, 121-128.
35. Long, X.; Liu, Q.; Chan, M.; Wang, Q.; Sun, S.S. Metabolic engineering and profiling of rice with increased lysine. Plant Biotechnol. J. 2013, 11, 490-501.
36. Manetti, C.; Bianchetti, C.; Bizzarri, M.; Casciani, L.; Castro, C.; D’Ascenzo, G.; Delfini, M.; di Cocco, M.E.; Lagana, A.; Miccheli, A., et al. NMR-based metabonomic study of transgenic maize. Phytochemistry 2004, 65, 3187-3198.
37. Manetti, C.; Bianchetti, C.; Casciani, L.; Castro, C.; di Cocco, M.E.; Miccheli, A.; Motto, M.; Conti, F. A metabonomic study of transgenic maize (Zea mays) seeds revealed variations in osmolytes and branched amino acids. J. Exp. Bot. 2006, 57, 2613-2625.
38. Castro, C.; Manetti, C. A multiway approach to analyze metabonomic data: A study of maize seeds development. Anal. Biochem. 2007, 371, 194-200.
39. Piccioni, F.; Capitani, D.; Zolla, L.; Mannina, L. NMR metabolic profiling of transgenic maize with the Cry1A(b) gene. J. Agric. Food Chem. 2009, 57, 6041-6049.
40. Levandi, T.; Leon, C.; Kaljurand, M.; García-Cañas, V.; Cifuentes, A. Capillary electrophoresis time-of-flight mass spectrometry for comparative metabolomics of transgenic versus conventional maize. Anal. Chem. 2008, 80, 6329-6335.
41. 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.
42. Bernal, J.L.; Nozal, M.J.; Toribio, L.; Diego, C.; Mayo, R.; Maestre, R. Use of supercritical fluid extraction and gas chromatography-mass spectrometry to obtain amino acid profiles from several genetically modified varieties of maize and soybean. J. Chromatogr. A 2008, 1192, 266-272.
43. Jimenez, J.J.; Bernal, J.L.; Nozal, M.J.; Toribio, L.; Bernal, J. Profile and relative concentrations of fatty acids in corn and soybean seeds from transgenic and isogenic crops. J. Chromatogr. A 2009, 1216, 7288-7295.
44. Frank, T.; Röhlig, R.M.; Davies, H.V.; Barros, E.; Engel, K. Metabolite profiling of maize kernels—genetic modification versus environmental influence. J. Agric. Food Chem. 2012, 60, 3005-3012.
45. Rivera, S.M.; Vilaró, F.; Zhu, C.; Bai, C.; Farré, G.; Christou, P.; Canela-Garayoa, R. Fast quantitative method for the analysis of carotenoids in transgenic maize. J. Agric. Food Chem. 2013, 61, 5279-5285.
46. Barros, E.; Lezar, S.; Anttonen, M.J.; van Dijk, J.P.; Röhlig, R.M.; Kok, E.J.; Engel, K.H. Comparison of two GM maize varieties with a nearisogenic non-GM variety using transcriptomics, proteomics and metabolomics. Plant Biotechnol. J. 2010, 8, 436-451.
47. García-Villalba, R.; León, C.; Dinelli, G.; Segura-Carretero, A.; Fernández-Gutiérrez, A.; Garcia-Cañas, V.; Cifuentes, A. Comparative metabolomic study of transgenic versus conventional soybean using capillary electrophoresis-time-of-flight mass spectrometry. J. Chromatogr. A 2008, 1195, 164-173.
48. Inaba, Y.; Brotherton, J.E.; Ulanov, A.; Widholm, J.M. Expression of a feedback insensitive anthranilate synthase gene from tobacco increases free tryptophan in soybean plants. Plant Cell Rep. 2007, 26, 1763-1771.
49. Giuffrida, A.; León, C.; García-Cañas, V.; Cucinotta, V.; Cifuentes, A. Modified cyclodextrins for fast and sensitive chiral-capillary electrophoresis-mass spectrometry. Electrophoresis 2009, 30, 1734-1742.
50. Clarke, J.D.; Alexander, D.C.; Ward, D.P.; Ryals, J.A.; Mitchell, M.W.; Wulff, J.E.; Guo, L. Assessment of genetically modified soybean in relation to natural variation in the soybean seed metabolome. Sci. Rep. 2013, 3, doi:10.1038/srep03082.
51. Kusano, M.; Baxter, I.; Fukushima, A.; Oikawa, A.; Okazaki, Y.; Nakabayashi, R.; Bouvrette, D.J.; Achard, F.; Jakubowski, A.R.; Ballam, J.M., et al. Assessing metabolomic and chemical diversity of a soybean lineage representing 35 years of breeding. Metabolomics 2014, doi:10.1007/s11306-014-0702-6.
52. Chen, F.; Duran, A.L.; Blount, J.W.; Sumner, L.W.; Dixon, R.A. Profiling phenolic metabolites in transgenic alfalfa modified in lignin biosynthesis. Phytochemistry 2003, 64, 1013-1021.
53. Charlton, A.; Allnutt, T.; Holmes, S.; Chisholm, J.; Bean, S.; Ellis, N.; Mullineaux, P.; Oehlschlager, S. NMR profiling of transgenic peas. Plant Biotechnol. J. 2004, 2, 27-35.
54. Baker, J.M.; Hawkins, N.D.; Ward, J.L.; Lovegrove, A.; Napier, J.A.; Shewry, P.R.; Beale, M.H. A metabolomic study of substantial equivalence of field-grown genetically modified wheat. Plant Biotechnol. J. 2006, 4, 381-392.
55. Roessner, U.; Wagner, C.; Kopka, J.; Trethewney, R.N.; Willmitzer, L. Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 2000, 23, 131-142.
56. Roessner, U.; Willmitzer, L.; Fernie, A.R. High-Resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiol. 2001, 127, 749-764.
57. Roessner, U.; Luedemann, A.; Brust, D.; Fiehn, O.; Linke, T.; Willmitzer, L.; Fernie, A.R. Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 2001, 13, 11-29.
58. Catchpole, G.S.; Beckmann, M.; Enot, D.P.; Mondhe, M.; Zywicki, B.; Taylor, J.; Hardy, N.; Smith, A.; King, R.D.; Kell, D.B., et al. Hierarchical metabolomics demonstrates substantial compositional similarity between genetically modified and conventional potato crops. Proc. Natl. Acad. Sci. USA 2005, 102, 14458-14462.
59. Bianco, G.; Schmitt-Kopplin, P.; Crescenzi, A.; Comes, S.; Kettrup, A.; Cataldi, T.R. Evaluation of glycoalkaloids in tubers of genetically modified virus Y-resistant potato plants (var. Désirée) by non-aqueous capillary electrophoresis coupled with electrospray ionization mass spectrometry (NACE-ESI-MS). Anal. Bioanal. Chem. 2003, 375, 799-804.
60. Iwaki, T.; Guo, L.; Ryals, J.A.; Yasuda, S.; Shimazaki, T.; Kikuchi, A.; Watanabe, K.N.; Kasuga, M.; Yamaguchi-Shinozaki, K.; Ogawa, T., et al. Metabolic profiling of transgenic potato tubers expressing Arabidopsis dehydration response element-binding protein 1A (DREB1A). J. Agric. Food Chem. 2013, 61, 893-900.
61. Defernez, M.; Gunning, Y.M.; Parr, A.J.; Shepherd, L.V.; Davies, H.V.; Colquhoun, I.J. NMR and HPLC-UV profiling of potatoes with genetic modifications to metabolic pathways. J. Agric. Food Chem. 2004, 52, 6075-6085.
62. Kondrák, M.; Marincs, F.; Antal, F.; Juhász, Z.; Bánfalvi, Z. Effects of yeast trehalose-6-phosphate synthase 1 on gene expression and carbohydrate contents of potato leaves under drought stress conditions. BMC Plant Biol. 2012, 12, doi:10.1186/1471-2229-12-74.
63. Noteborn, H.P.; Lommen, A.; van der Jagt, R.C.; Weseman, J.M. Chemical fingerprinting for the evaluation of unintended secondary metabolic changes in transgenic food crops. J. Biotechnol. 2000, 77, 103-114.
64. Roessner-Tunali, U.; Hegemann, B.; Lytovchenko, A.; Carrari, F.; Bruedigam, C.; Granot, D.; Fernie, A.R. Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol. 2003, 133, 84-99.
65. Le Gall, G.; Colquhoun, I.J.; Davis, A.L.; Collins, G.J.; Verhoeyen, M.E. Metabolite profiling of tomato (Lycopersicon esculentum) using 1H NMR spectroscopy as a tool to detect potential unintended effects following a genetic modification. J. Agric. Food Chem. 2003, 51, 2447-2456.
66. Le Gall, G.; DuPont, M.S.; Mellon, F.A.; Davis, A.L.; Collins, G.J.; Verhoeyen, M.E.; Colquhoun, I.J. Characterization and content of flavonoid glycosides in genetically modified tomato (Lycopersicon esculentum) fruits. J. Agric. Food Chem. 2003, 51, 2438-2446.
67. Long, M.; Millar, D.J.; Kimura, Y.; Donovan, G.; Rees, J.; Fraser, P.D.; Bramley, P.M.; Bolwell, G.P. Metabolite profiling of carotenoid and phenolic pathways in mutant and transgenic lines of tomato: Identification of a high antioxidant fruit line. Phytochemistry 2006, 67, 1750-1757.
68. Nicoletti, I.; de Rossi, A.; Giovinazzo, G.; Corradini, D. Identification and quantification of stilbenes in fruits of transgenic tomato plants (Lycopersicon esculentum Mill.) by reversed phase HPLC with photodiode array and mass spectrometry detection. J. Agric. Food Chem. 2007, 55, 3304-3311.
69. Kusano, M.; Redestig, H.; Hirai, T.; Oikawa, A.; Matsuda, F.; Fukushima, A.; Arita, M.; Watanabe, S.; Yano, M.; Hiwasa-Tanase, K., et al. Covering chemical diversity of genetically-modified tomatoes using metabolomics for objective substantial equivalence assessment. PLoS One 2011, 16, e16989.
70. Choi, H.K.; Choi, Y.H.; Verberne, M.; Lefeber, A.W.; Erkelens, C.; Verpoorte, R. Metabolic fingerprinting of wild type and transgenic tobacco plants by 1H NMR and multivariate analysis technique. Phytochemistry 2004, 65, 857-864.
71. Sobolev, A.P.; Segre, A.L.; Giannino, D.; Mariotti, D.; Nicolodi, C.; Brosio, E.; Amato, M.E. Strong increase of foliar inulin occurs in transgenic lettuce plants (Lactuca sativa L.) overexpressing the Asparagine Synthetase A gene from Escherichia coli. J. Agric. Food Chem. 2007, 55, 10827-10831.
72. Sobolev, A.P.; Capitani, D.; Giannino, D.; Nicolodi, C.; Testone, G.; Santoro, F.; Frugis, G.; Iannelli, M.A.; Mattoo, A.K.; Brosio, E., et al. NMR-metabolic methodology in the study of GM foods. Nutrients 2010, 2, 1-15.
73. Sobolev, A.P.; Testone, G.; Santoro, F.; Nicolodi, C.; Iannelli, M.A.; Amato, M.E.; Ianniello, A.; Brosio, E.; Giannino, D.; Mannina, L. Quality traits of conventional and transgenic lettuce (Lactuca sativa L.) at harvesting by NMR metabolic profiling. J. Agric. Food Chem. 2010, 58, 6928-6936.
74. Tagashira, N.; Plader, W.; Filipecki, M.; Yin, Z.; Wiśniewska, A.; Gaj, P.; Szwacka, M.; Fiehn, O.; Hoshi, Y.; Kondo, K., et al. The metabolic profiles of transgenic cucumber lines vary with different chromosomal locations of the transgene. Cell Mol. Biol. Lett. 2005, 10, 697-710.
75. Zawirska-Wojtasiak, R.; Gośliński, M.; Szwacka, M.; Gajc-Wolska, J.; Mildner-Szkudlarz, S. Aroma evaluation of transgenic, thaumatin II-producing cucumber fruits. J. Food Sci. 2009, 74, C204-C210.
76. Malowicki, S.M.M.; Martin, R.; Qian, M.C. Comparison of sugar, acids, and volatile composition in raspberry bushy dwarf virus-resistant transgenic raspberries and the wild type “meeker” (Rubus Idaeus L.). J. Agric. Food Chem. 2008, 56, 6648-6655.
77. Tesniere, C.; Torregrosa, L.; Pradal, M.; Souquet, J.M.; Gilles, C.; Dos Santos, K.; Chatelet, P.; Gunata, Z. Effects of genetic manipulation of alcohol dehydrogenase levels on the response to stress and the synthesis of secondary metabolites in grapevine leaves. J. Exp. Bot. 2006, 57, 91-99.
78. Lange, B.M.; Mahmoud, S.S.; Wildung, M.R.; Turner, G.W.; Davis, E.M.; Lange, I; Baker, R.C.; Boydston, R.A.; Croteau, R.B. Improving peppermint essential oil yield and composition by metabolic engineering. Proc. Natl. Acad. Sci. USA 2011, 108, 16944-16949.
79. Kim, J.K.; Ryu, T.H.; Sohn, S.I.; Kim, J.H.; Chu, S.M.; Yu, C.Y.; Baek, H.J. Metabolic fingerprinting study on the substantial equivalence of Genetically Modified (GM) Chinese cabbage to non-gm cabbage. J. Korean Soc. Appl. Biol. 2009, 52, 186-192.
80. Tripathi, S.; Suzuki, J.Y.; Carr, J.B.; McQuate, G.T.; Ferreira, S.A.; Manshardt, R.M.; Pitz, K.Y.; Wall, M.M.; Gonsalves, D. Nutritional composition of Rainbow papaya, the first commercialized transgenic fruit crop. J. Food Compos. Anal. 2011, 24, 140-147.
81. Jiao, Z.; Deng, J.C.; Li, G.K.; Zhang, Z.M.; Cai, Z.W. Study on the compositional differences between transgenic and non-transgenic papaya. J. Food Compos. Anal. 2010, 23, 640-647.
82. Srivastava, V.; Obudulu, O.; Bygdell, J.; Löfstedt, T.; Rydén, P.; Nilsson, R.; Ahnlund, M.; Johansson, A.; Jonsson, P.; Freyhult, E., et al. OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI-superoxide dismutase Populus plants. BMC Genomics 2013, 14, doi:10.1186/1471-2164-14-893.
83. Kogel, K.H.; Voll, L.M.; Schäfer, P.; Jansen, C.; Wu, Y.; Langen, G.; Imani, J.; Hofmann, J.; Schmiedl, A.; Sonnewald, S., et al. Transcriptome and metabolome profiling of field-grown transgenic barley lack induced differences but show cultivar-specific variances. Proc. Natl. Acad. Sci. USA 2010, 107, 6198-6203.
84. Cantrell, R.P.; Reeves, T.G. The rice genome. The cereal of the world’s poor takes center stage. Science 2002, 296, doi:10.1126/science.1070721.
85. Goff, S.A.; Ricke, D.; Lan, T.H.; Presting, G.; Wang, R.; Dunn, M.; Glazebrook, J.; Sessions, A.; Oeller, P.; Varma, H., et al. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 2002, 296, 92-100.
86. Oikawa, A.; Matsuda, F.; Kusano, M.; Okazaki, Y.; Saito, K. Rice metabolomics. Rice 2008, 1, 63-71.
87. Choudhary, V.K.; Suresh-Kumar, P. Maize production, economics and soil productivity under different organic source of nutrients in eastern himalayan region, India. Int. J. Plant Prod. 2013, 7, 167-186.
88. Skogerson, K.; Harrigan, G.G.; Reynolds, T.L.; Halls, S.C.; Ruebelt, M.; Iandolino, A.; Pandravada, A.; Glenn, K.C.; Fiehn, O. Impact of genetics and environment on the metabolite composition of maize grain. J. Agric. Food Chem. 2010, 58, 3600-3610.
89. Asiago, V.M.; Hazebroek, J.; Harp, T.; Zhong, C. Effects of genetics and environment on the metabolome of commercial maize hybrids: A multisite study. J. Agric. Food Chem. 2012, 60, 11498-11508.
90. Baniasadi, H.; Vlahakis, C.; Hazebroek, J.; Zhong, C.; Asiago, V. Effect of environment and genotype on commercial maize hybrids using LC/MS-based metabolomics. J. Agric. Food Chem. 2014, 62, 1412-1422.
91. Duvernaya, W.H.; Chinna, M.S.; Yencho, G.C. Hydrolysis and fermentation of sweetpotatoes for production of fermentable sugars and ethanol. Ind. Crop Prod. 2013, 42, 527-537.
92. Urbanczyk-Wochniak, E.; Baxter, C.; Kolbe, A.; Kopka, J.; Sweetlove, L.J.; Fernie, A.R. Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves. Planta 2005, 221, 891-903.
93. García-Cañas, V.; Simó, C.; Herrero, M.; Ibáñez, E.; Cifuentes, A. Present and future challenges in food analysis: Foodomics. Anal. Chem. 2012, 84, 10150-10159.
94. Fukushima, A.; Saito, K. Development of the Arabidopsis metabolome database. Plant Physiol. 2014, doi:10.1104/pp.114.240986.