Advertisement

Metabolomics

, Volume 11, Issue 3, pp 667–683 | Cite as

A metabolomics approach to unravel the regulating role of phytohormones towards carotenoid metabolism in tomato fruit

  • Lieven Van Meulebroek
  • Julie Vanden Bussche
  • Nathalie De Clercq
  • Kathy Steppe
  • Lynn Vanhaecke
Original Article

Abstract

Carotenoids are important secondary metabolites, which have been recognized as an essential component of the human diet because of their valuable beneficial health effects. With this rationale, there is a continuous aim to define the distribution of these compounds in plants, to better understand their metabolism and to increase their concentration levels in fruits and vegetables. This study aimed at deepening the knowledge on the regulatory role of phytohormones in carotenoid metabolism. More specifically, it was envisaged to reveal the phytohormones involved in the metabolism of α-carotene, β-carotene, lycopene, lutein and zeaxanthin. To this purpose, the phytohormone profiles of 50 tomato fruits were determined by high-resolution Orbitrap mass spectrometry and evaluated towards the associated carotenoid levels. Data mining was performed by differential expression and orthogonal partial least squares analyses. This metabolomics approach revealed 5 phytohormonal metabolites, which significantly influenced (Variable Importance in Projection scores ≥0.80) carotenoid metabolism. These metabolites were identified as cis-12-oxo-phytodienoic acid, cucurbic acid, 2-oxindole-3-acetic acid, 1-acetylindole-3-carboxaldehyde, and cis-zeatin-O-glucoside. The involvement of the individual phytohormones towards carotenoid metabolism was investigated by regression analysis (P values ≤0.05, R2 varying between 0.280 and 0.760) and statistical correlation (P values ≤0.01, correlation varying between 0.403 and 0.846). It was concluded that these phytohormones all have significant contributing value in the regulation of carotenoid metabolism, thereby exhibiting down- and up-regulating influences. As a result, this knowledge encloses the potential for improving tomato fruit nutritional quality by targeted control of agronomic conditions, exogenous use of plant bioregulators, or genetic engineering.

Keywords

Metabolomics Tomato Carotenoids Phytohormones Metabolism 

Notes

Acknowledgments

Lynn Vanhaecke is supported by a postdoctoral fellowship from the Research Foundation of Flanders (FWO). Lieven Van Meulebroek is supported by the Institute for the Promotion and Innovation through Science and Technology in Flanders (IWT) Vlaanderen.

Conflict of interest

Lieven Van Meulebroek, Julie Vanden Bussche, Nathalie De Clercq, Kathy Steppe and Lynn Vanhaecke have declared that they have no conflict of interest.

Compliance with Ethical Requirements

The manuscript does not contain clinical studies or patient data.

Supplementary material

11306_2014_728_MOESM1_ESM.docx (66 kb)
Supplementary material 1 (DOCX 66 kb)

References

  1. Allwood, J., & Goodacre, R. (2010). An introduction to liquid chromatography-mass spectrometry instrumentation applied in metabolomic analyses. Phytochemical Analysis, 21(1), 33–47.CrossRefPubMedGoogle Scholar
  2. Bartley, G. E., & Scolnik, P. A. (1995). Plant carotenoids: Pigments for photoprotection, visual attraction, and human health. The Plant Cell, 7(7), 1027–1038.CrossRefPubMedCentralPubMedGoogle Scholar
  3. Bedair, M., & Sumner, L. (2008). Current and emerging mass-spectrometry technologies for metabolomics. Trends in Analytical Chemistry, 27(3), 238–250.CrossRefGoogle Scholar
  4. Bijttebier, S. K. A., D’Hondt, E., Hermans, N., Apers, S., & Voorpoels, S. (2013). Unravelling ionization and fragmentation pathways of carotenoids using orbitrap technology: a first step towards identification of unknowns. Journal of Mass Spectrometry, 48(6), 740–754.CrossRefPubMedGoogle Scholar
  5. Böttcher, C., & Pollmann, S. (2008). Plant oxylipins: Plant responses to 12-oxo-phytodienoic acid are governed by its specific structural and functional properties. The FEBS Journal, 276(17), 4693–4704.CrossRefGoogle Scholar
  6. Bramley, P. M. (2002). Regulation of carotenoid formation during tomato fruit ripening and development. Journal of Experimental Botany, 53(377), 2107–2113.CrossRefPubMedGoogle Scholar
  7. Carvalho, W., de Fonseca, M. E. N., da Silva, H. R., Boiteux, L. S., & de Giordano, L. B. (2005). Indirect estimation of lycopene concentration in fruits of tomato genotypes viachromaticity values. Horticultura Brasileira, 23(3), 819–825.CrossRefGoogle Scholar
  8. Cazzonelli, C. I., & Pogson, B. J. (2010). Source to sink: Regulation of carotenoid biosynthesis in plants. Trends in Plant Science, 15(5), 1360–1385.CrossRefGoogle Scholar
  9. Chamarro, J., Östin, A., & Sandberg, G. (2001). Metabolism of indole-3-acetic acid by orange (Citrus sinensis) flavedo tissue during fruit development. Phytochemistry, 57(2), 179–187.CrossRefPubMedGoogle Scholar
  10. Chen, J., Wang, W., Lv, S., Yin, P., Zhao, X., Lu, X., et al. (2009). Metabonomics study of liver cancer based on ultra performance liquid chromatography coupled to mass spectrometry with HILIC and RPLC separations. Analytica Chimica Acta, 650(1), 3–9.CrossRefPubMedGoogle Scholar
  11. Cheong, J., & Do Chi, Y. (2003). Methyl jasmonate as a vital substance in plants. Trends in Genetics, 19(7), 409–413.CrossRefPubMedGoogle Scholar
  12. Chiwocha, S. D. S., Abrams, S. R., Ambrose, S. J., Cutler, A. J., Loewen, M., Ross, A. R. S., et al. (2003). A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: an analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant Journal, 35(3), 405–417.CrossRefPubMedGoogle Scholar
  13. Chung, M., Vrebalov, J., Alba, R., et al. (2010). A tomato (Solanum lycopersicum) APETALA2/ERF gene, SIAP2a, is a negative regulator of fruit ripening. The Plant Journal, 64(6), 936–947.CrossRefPubMedGoogle Scholar
  14. Concha, C. M., Figueroa, N. E., Poblete, L. A., et al. (2013). Methyl jasmonate treatment induces changes in fruit ripening by modifying the expression of several ripening genes in Fragaria chiloensis fruit. Plant Physiology and Biochemistry, 70, 433–444.CrossRefPubMedGoogle Scholar
  15. Creelman, R. A., & Mullet, J. E. (1995). Jasmonic acid distribution and action in plants: Regulation during development and response to biotic and abiotic stress. Proceedings of the National Academy of Sciences, 92(10), 4114–4119.CrossRefGoogle Scholar
  16. Dathe, W., Schindler, C., Schneider, G., et al. (1991). Cucurbic acid and its 6,7-stereoisomers. Phytochemistry, 30(6), 1909–1914.CrossRefGoogle Scholar
  17. Davey, J. E., & Van Staden, J. (1977). Endogenous cytokinins in the fruits of ripening and non-ripening tomatoes. Plant Science Letters, 11(3–4), 359–364.Google Scholar
  18. DellaPenna, D., & Pogson, B. J. (2006). Vitamin synthesis in plants: tocopherols and carotenoids. Annual Review of Plant Biology, 57, 711–738.CrossRefPubMedGoogle Scholar
  19. Dorais, M., Ehret, D. L., & Papadopoulos, A. P. (2008). Tomato (Solanum lycopersicum) health components: from the seed to the consumer. Phytochemistry Reviews, 7(2), 231–250.CrossRefGoogle Scholar
  20. Eriksson, L., Gottfries, J., Johansson, E., & Wold, S. (2004). Time-resolved QSAR: an approach to PLS modeling of three-way biological data. Chemometrics and Intelligent Laboratory Systems, 73(1), 73–84.CrossRefGoogle Scholar
  21. Eriksson, L., Trygg, J., & Wold, S. (2008). CV-ANOVA for significance testing of PLS and OPLSR models. Journal of Chemometrics, 22(11–12), 594–600.CrossRefGoogle Scholar
  22. Ezura, H. (2009). Tomato is a next-generation model plant for research and development. Journal of Japanese Society for Horticultural Science, 78(1), 1–2.CrossRefGoogle Scholar
  23. Fan, X., Mattheis, J., & Fellman, J. (1998). A role for jasmonate in climacteric fruit ripening. Planta, 204(4), 444–449.CrossRefGoogle Scholar
  24. Fanciullino, A. L., Bidel, L. P. R., & Urban, L. (2013). Carotenoid responses to envirmonmental stimuli: integrating redox and carbon controls into a fruit model. Plant, Cell and Environment,. doi: 10.111/pce.12153.PubMedGoogle Scholar
  25. Fonville, J. M., Richards, S. E., Barton, R. H., et al. (2010). The evolution of partial least squares models and related chemometric approaches in metabonomics and metabolomic phenotyping. Journal of Chemometrics, 24, 636–649.CrossRefGoogle Scholar
  26. Fraser, P. D., Enfissi, E. M. A., & Bramley, P. M. (2009). Genetic engineering of carotenoid formation in tomato fruit and the potential application of systems and synthetic biology approaches. Archives of Biochemistry and Biophysics, 483(2), 196–204.CrossRefPubMedGoogle Scholar
  27. Frenkel, C. (1975). Oxidative turnover of auxins in relation to the onset of ripening in Barlett pear. Plant Physiology, 55(3), 480–484.CrossRefPubMedCentralPubMedGoogle Scholar
  28. Fukui, H., Koshimizu, K., Yamazaki, Y., & Usuda, S. (1977). Structures of plant growth inhibitors in seeds of Cucurbita pepo L. Agricultural and Biological Chemistry, 41, 189–194.CrossRefGoogle Scholar
  29. Gautier, H., Rocci, A., Buret, M., Grassely, D., & Causse, M. (2005). Fruit load or fruit position alters response to temperature and subsequently cherry tomato quality. Science of Food and Agriculture, 85(6), 1009–1016.CrossRefGoogle Scholar
  30. Ghassemian, M., Nambara, E., Cutler, S., et al. (2000). Regulation of abscisic acid signalling by the ethylene response pathway in Arabidopsis. American Society of Plant Physiologists, 12(7), 117–1126.Google Scholar
  31. Gillaspy, G., Ben-David, H., & Gruissem, W. (1993). Fruits: A developmental perspective. The Plant Cell, 5(10), 1439–1451.CrossRefPubMedCentralPubMedGoogle Scholar
  32. Given, N. K., Venis, M. A., & Grierson, D. (1998). Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta, 174(3), 402–406.CrossRefGoogle Scholar
  33. Goméz-Ramos, M. M., Ferrer, C., Malato, O., et al. (2013). Liquif-chromatography-high-resolution mass spectrometry for pesticide residue analysis in fruit and vegetables: Screening and quantitative studies. Journal of Chromatography A, 1287, 24–37.CrossRefPubMedGoogle Scholar
  34. Gulston, M. K., Rubtsov, D. V., Atherton, H. J., et al. (2008). A combined metabolomics and proteomic investigation of the effects of a failure to express dystrophin in the mouse heart. Journal of Proteome Research, 7(5), 2069–2077.CrossRefPubMedGoogle Scholar
  35. Hall, D. (2005). Plant metabolomics: from holistic hope, to hype, to hot topic. New Phytologist, 169(3), 453–468.CrossRefGoogle Scholar
  36. Hawkins, D. M., Basak, S. C., & Mills, D. (2003). Assessing model fit by cross-validation. Journal of Chemical Information and Computer Sciences, 43(2), 579–586.PubMedGoogle Scholar
  37. Hill, D. W., Kertesz, T. M., Fontaine, D., Friedman, R., & Grant, D. F. (2008). Mass spectral metabonomics beyond elemental formula: chemical database querying by matching experimental with computational fragmentation spectra. Analytical Chemistry, 80(14), 5574–5582.CrossRefPubMedGoogle Scholar
  38. Kawaguchi, M., & Syõno, K. (1996). The excessive production of indole-3-acetic acid and its significance in studies of the biosynthesis of this regulator of pant growth and development. Plant Cell Physiology, 37(8), 123–130.CrossRefGoogle Scholar
  39. Kiba, T., Kudo, T., Kojima, M., & Sakakibara, H. (2011). Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. Journal of Experimental Botany, 62(4), 399–1409.CrossRefGoogle Scholar
  40. Kirdar, A. O., Green, K. D., & Rathore, A. S. (2008). Application of multivariate data analysis for identification and successful resolution of a root cause for a bioprocessing application. Biotechnology Progress, 24(3), 720–726.CrossRefPubMedGoogle Scholar
  41. Koshimizu, K., Fukui, H., Usuda, S., & Mitsui, T. (1974) Plant growth inhibitors in seeds of pumpkin. In: Plant Growth Substances Proceedings of the International Conference, 8 (pp. 86–92).Google Scholar
  42. Kumar, P., Rúbies, A., Centrich, F., et al. (2013). Targeted analysis with benchtop quadrupole-orbitrap hybrid mass spectrometer: Application to determination of synthetic hormones in animal urine. Analytica Chimica Acta, 780, 65–73.CrossRefPubMedGoogle Scholar
  43. Lalel, H. J. D., Singh, Z., & Tan, S. C. (2003). Maturity stage at harvest affects fruit ripening, quality and biosynthesis of aroma volatile compounds in ‘Kensinton Pride’ mango. Journal of Horticultural Science and Biotechnology, 78(2), 470–484.Google Scholar
  44. Liu, L., Wei, J., Zhang, M., Zhang, L., Li, L., & Wang, Q. (2012). Ethylene independent induction of lycopene biosynthesis in tomato fruits by jasmonates. Journal of Experimental Botany, 63(16), 5751–5761.CrossRefPubMedCentralPubMedGoogle Scholar
  45. Lu, S., & Li, L. (2008). Carotenoid Metabolism: Biosynthesis, Regulation, and Beyond. Journal of Integrative Plant Biology, 50(7), 778–785.CrossRefPubMedGoogle Scholar
  46. Lu, S., Wang, J., Yanhong, N., et al. (2012). Metabolic profiling reveals growth related FAMA productivity and quality of Chlorella sorokiniana with different inoculum sizes. Biotechnology and Bioengineering, 109(7), 1651–1662.CrossRefPubMedGoogle Scholar
  47. Madala, N. E., Piater, L. A., Steenkamp, P. A., et al. (2014). Multivariate statistical methods of metabolomic data reveals different metabolite distribution patterns in isonitrosoacetophenone-elicited Nicotiana tabacum and Sorghum bicolor cells. SpringerPlus, 3(1), 254–263.CrossRefPubMedCentralPubMedGoogle Scholar
  48. Makarov, A., & Scigelova, M. (2010). Coupling liquid chromatography to Orbitrap mass spectrometry. Journal of Chromatography A, 1217(25), 3938–3945.CrossRefPubMedGoogle Scholar
  49. McAtee, P., Karim, S., Schaffer, R., & David, K. (2013). A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Frontiers in Plant Science, 4(79), 1–7.Google Scholar
  50. McLamore, E. S., Diggs, A., Marzal, P. C., Shi, J., Blakeslee, J. J., Peer, W. A., et al. (2010). Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. The Plant Journal, 63(6), 1004–1016.CrossRefPubMedGoogle Scholar
  51. Miersch, O., Neumerkel, J., Dippe, M., Stenzel, I., & Wasternack, C. (2007). Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signalling. New Phytologist, 177(1), 114–127.PubMedGoogle Scholar
  52. Mochida, K., & Shinozaki, K. (2011). Advances in omics and bioinformaticstools for systems analyses of plant functions. Plant and Cell Physiology, 52(12), 2017–2038.CrossRefPubMedCentralPubMedGoogle Scholar
  53. Mulholland, B. J., Taylor, I. B., Jackson, A. C., & Thompson, A. J. (2003). Can ABA mediate responses of salinity stress tomato. Environmental and Experimental Botany, 50(1), 17–28.CrossRefGoogle Scholar
  54. Neumann, S., & Böcker, S. (2010). Computational mass spectrometry for metabolomics: Identification of metabolites and small molecules. Analytical and Bioanalytical Chemistry, 398, 2779–2788.CrossRefPubMedGoogle Scholar
  55. Nielen, M., van Engelen, M., Zuiderent, R., & Ramaker, R. (2007). Screening and confirmation criteria for hormone residue analysis using liquid chromatography accurate mass time-of-flight, Fourier transform ion cyclotron resonance and orbitrap mass spectrometry techniques. Analytica Chemica Acta, 586(1–2), 122–129.CrossRefGoogle Scholar
  56. Olah, M., Bologa, C., & Oprea, T. I. (2004). An automated PLS search for biologically relevant QSAR descriptors. Journal of Computer-Aided Molecular Design, 18(7–9), 437–449.CrossRefPubMedGoogle Scholar
  57. OlChemIm Ltd. (2012). Catalogue 2012-2014.Google Scholar
  58. Oliver, J., & Palou, A. (2000). Chromatographic determination of carotenoids in foods. Journal of Chromatography A, 881(1–2), 543–555.CrossRefPubMedGoogle Scholar
  59. Peña-Cortés, H., Barrios, P., Dorta, F., et al. (2004). Involvement of jasmonic acid and derivatives in plant responses to pathogens and insects and in fruit ripening. Journal of Plant Growth Regulation, 23(3), 246–260.Google Scholar
  60. Pérez, A. G., Sanz, C., Richardson, D. G., & Olías, J. M. (1993). Methyl jasmonate vapour promotes β-carotene synthesis and chlorophyll degradation in Golden Delicious apple peel. Journal of Plant Growth Regulation, 12(3), 163–167.CrossRefGoogle Scholar
  61. Perry, R., Cooks, R., & Noll, R. (2008). Orbitrap mass spectrometry: instrumentation, ion motion and applications. Mass Spectrometry Reviews, 27(6), 661–669.CrossRefPubMedGoogle Scholar
  62. Piotrowska, A., & Bajguz, A. (2011). Conjugates of abscisic acid, brassinosteroids, ethylene, gibberellins, and jasmonates. Phytochemistry, 72(17), 2097–2112.CrossRefPubMedGoogle Scholar
  63. Rivera, S. M., & Canela-Garayoa, R. (2012). Analytical tools for the analysis of carotenoids in diverse materials. Journal of Chromatography A, 1224, 1–10.CrossRefPubMedGoogle Scholar
  64. Rodo, A. P., Brugière, N., Vankova, R., et al. (2008). Over-expression of a zeatin-O-glucosylation gene in maize leads to growth retardation and tasselseed formation. Journal of Experimental Botany, 59(10), 2673–2686.CrossRefPubMedCentralGoogle Scholar
  65. Roisch, T., & Ehneß, R. (2000). Regulation of source/sink relations by cytokinins. Plant Growth Regulation, 32(2–3), 359–367.CrossRefGoogle Scholar
  66. Roldán-Gutiérrez, J. M., & Luque de Castro, M. D. (2007). Lycopene: The need for better methods for characterization and determination. Trends in Analytical Chemistry, 26(2), 163–170.CrossRefGoogle Scholar
  67. Sandmann, G., Römer, S., & Fraser, P. D. (2006). Understanding carotenoid metabolism as a necessity for genetic engineering of crop plants. Metabolic Engineering, 8(4), 291–302.CrossRefPubMedGoogle Scholar
  68. Saniewski, M., & Czapski, J. (1983). The effect of methyl jasmonate on lycopene and β-carotene accumulation in ripening red tomatoes. Experientia, 39(12), 1373–1374.CrossRefGoogle Scholar
  69. Sérino, S., Gomez, L., Costagliola, G., & Gautier, H. (2009). HPLC assay of tomato carotenoids: validation of a rapid microextraction technique. Journal of Agriculture and Food Chemistry, 57(19), 8753–8760.CrossRefGoogle Scholar
  70. Shah, V. P., Midha, K. K., & Findlay, J. W. A. (2000). Bioanalytical method validation-A revisit with a decade of progress. Pharmaceutical Research, 17(2), 1551–1557.CrossRefPubMedGoogle Scholar
  71. Shumskaya, M., & Wurtzel, E. T. (2013). The carotenoid biosynthesis pathway: Thinking in all dimensions. Plant Science, 208, 58–63.CrossRefPubMedCentralPubMedGoogle Scholar
  72. Srivastava, A., & Handa, A. K. (2005). Hormonal regulation of tomato fruit development: a molecular perspective. Journal of Plant Growth Regulation, 24(2), 67–82.CrossRefGoogle Scholar
  73. Stern, R. A., Flaishman, M., Applebaum, S., & Ben-Arie, R. (2007). Effect of synthetic auxins on fruit development of ‘Bing’ cherry (Prunus avium L.). Scientia Horticulturae, 114(4), 275–280.CrossRefGoogle Scholar
  74. Stintzi, A., Weber, H., Reymond, P., Browse, J., & Farmer, E. E. (2001). Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proceedings of the National Academy of Sciences USA, 98(22), 12837–12842.CrossRefGoogle Scholar
  75. Sumner, L. W., Amberg, A., Barrett, D., et al. (2007). Proposed minimum reporting standards for chemical analysis. Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics, 3(3), 211–221.CrossRefPubMedCentralPubMedGoogle Scholar
  76. Suzuki, M., Kusano, M., Takahashi, H., et al. (2010). Rice-Arabidopsis FOX line screening with FT-NIR-based fingerprinting for GC-TOF/MS based metabolite profiling. Metabolomics, 6, 137–145.CrossRefGoogle Scholar
  77. Taki, N., Sasaki-Sekimoto, Y., Obayashi, T., et al. (2005). 12-Oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. American Society of Plant Biologists, 139(3), 1268–1283.Google Scholar
  78. Trainotti, L., Tadiello, A., & Casadoro, G. (2007). The involvement of auxin in the ripening of climacteric comes of age: the hormone plays a role of its own and has an intense interplay with eythylene in ripening peaches. Journal of Experimental Botany, 58(12), 3299–3308.CrossRefPubMedGoogle Scholar
  79. Trygg, J., Holmes, E., & Lundstedt, T. (2006). Chemometrics in Metabonomics. Journal of Proteome Research, 6(2), 469–479.CrossRefGoogle Scholar
  80. Van Meulebroek, L., Vanden Bussche, J., Steppe, K., & Vanhaecke, L. (2012a). Ultra-high performance liquid chromatography coupled to high resolution Orbitrap mass spectrometry for metabolomic profiling of the endogenous phytohormonal status of the tomato plant. Journal of Chromatography A, 1260, 67–80.CrossRefGoogle Scholar
  81. Van Meulebroek, L., Vanden Bussche, J., Steppe, K., & Vanhaecke, L. (2014). High-resolution Orbitrap mass spectrometry for the analysis of carotenoids in tomato fruit: validation and comparative evaluation towards UV-VIS and tandem mass spectrometry. Analytical and Bioanalytical Chemistry, 406(11), 2613–2626.Google Scholar
  82. Van Meulebroek, L., Vanhaecke, L., De Swaef, T., Steppe, K., & De Brabander, H. F. (2012b). U-HPLC-MS/MS to quantify liposoluble antioxidants in red-ripe tomatoes, grown under different salt stress levels. Journal of Agriculture and Food Chemistry, 60(2), 566–573.CrossRefGoogle Scholar
  83. Van Staden, J., & Papaphilippou, A. P. (1977). Biological activity of O-β-D-glucopyranosylzeatin. Plant Physiology, 60(5), 649–650.CrossRefPubMedCentralPubMedGoogle Scholar
  84. Vanhaecke, L., Verheyden, K., Vanden Bussche, J., Scoutson, F., & De Brabander, H. (2009). UHPLC coupled with Fourier Transform Orbitrap for residue analysis. LCGC Europe, 7(21), 364–374.Google Scholar
  85. Wang, Y., Wang, J., Yao, M., et al. (2008). Metabonomics study on the effects of the Ginsenoside Rg3 in a β-cyclodextrin-based formulation on tumor-bearing rats by a fully automatic hydrophilic interaction/reversed-phase column-switching HPLC-ESI-MS approach. Analytical Chemistry, 80(12), 4680–4688.CrossRefPubMedGoogle Scholar
  86. Wardrop, A. J., & Polva, G. M. (1980). Ligand specificity of bean leaf soluble auxin-binding protein. Plant Physiology, 66(1), 112–118.CrossRefPubMedCentralPubMedGoogle Scholar
  87. Weckwerth, W., & Fiehn, O. (2002). Can we discover novel pathways using metabolomic analysis? Current Opinion in Biotechnology, 13(2), 156–160.CrossRefPubMedGoogle Scholar
  88. Weiler, E. W., Laudert, D., Schaller, F., Stelmach, B., & Hennig, P. (1998). Phytochemical signals and plant-microbe interactions. New York: Plenum Press.Google Scholar
  89. Werner, E., Heiler, J., Ducruix, C., et al. (2008). Mass spectrometry for the identification of the discriminating signals from metabolomics: Current status and future trends. Journal of Chromatography B, 871, 143–163.CrossRefGoogle Scholar
  90. Wiklund, S., Johansson, E., Sjostrom, L., et al. (2008). Visualization of GC/TOF-MS-based metabolomics data for identifation of biochemically interesting compounds using OPLS class models. Analytical Chemistry, 80(1), 116–123.CrossRefGoogle Scholar
  91. Xie, G. X., Ni, Y., Sie, M. M., et al. (2008). Application of ultra-performance LC-TOF MS metabolite profiling techniques to the analysis of medicinal Panax herbs. Metabolomics, 4(3), 248–260.CrossRefGoogle Scholar
  92. Xue, S., Li, Z., Zhi, H., et al. (2012). Metabolic fingerprinting investigation of Tussilago farfara L. by GC-MS and multivariate data analysis. Biochemical Systematics and Ecology, 41, 6–12.CrossRefGoogle Scholar
  93. Zazimalova, E., & Napier, R. M. (2003). Points of regulation for auxin action. Plant Cell Reports, 21(7), 625–634.PubMedGoogle Scholar
  94. Ziosi, V., Bregoli, A. M., Fregola, F., Costa, G., & Torrigiani, P. (2008). Jasmonate-induced ripening delay is associated with up-regulation of polyamine levels in peach fruit. Journal of Plant Physiology, 166(9), 938–946.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Lieven Van Meulebroek
    • 1
    • 2
  • Julie Vanden Bussche
    • 1
  • Nathalie De Clercq
    • 1
  • Kathy Steppe
    • 2
  • Lynn Vanhaecke
    • 1
  1. 1.Laboratory of Chemical Analysis, Department of Veterinary Public Health and Food Safety, Faculty of Veterinary MedicineGhent UniversityMerelbekeBelgium
  2. 2.Laboratory of Plant Ecology, Department of Applied Ecology and Plant Biology, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

Personalised recommendations