A non-targeted metabolomics approach to evaluate the effects of biomass growth and chitosan elicitation on primary and secondary metabolism of Hypericum perforatum in vitro roots

Metabolomics

Volumn 10, Issue 6, 2014, Pages 1186-1196

  Brasili, Elisa ^a   Praticò, Giulia ^a   Marini, Federico ^a   Valletta, Alessio ^a   Capuani, Giorgio ^a   Sciubba, Fabio ^a   Miccheli, Alfredo ^a   Pasqua, Gabriella ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

ASCA modelling; Hypericum perforatum in vitro roots; Metabolic profiling; Metabolomics; NMR spectroscopy

Indexed keywords

EID: 84936753583     PISSN: 15733882     EISSN: 15733890     Source Type: Journal    
DOI: 10.1007/s11306-014-0660-z     Document Type: Article

References (66)

1. 1H-NMR-based metabolomics combined with HPLC-PDA-MS-SPE-NMR for investigation of standardized Ginkgo biloba preparations. Metabolomics,6, 292–302.
2. Ahuja, I., Kissen, R., & Bones, A. M. (2012). Phytoalexins in defense against pathogens. Trends in Plant Science,17, 73–90.
3. Atkinson, R. R. L., Burrell, M. M., Osborne, C. P., Rose, K. E., & Rees, M. (2012). A non-targeted metabolomics approach to quantifying differences in root storage between fast- and slow-growing plants. New Phytologist,196, 200–211.
4. Bais, H. P., Walker, T. S., Schweizer, H. P., & Vivanco, J. M. (2002). Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiology and Biochemistry,40, 983–995.
5. Baque, M. A., Moh, S. H., Lee, E. J., Zhong, J. J., & Paek, K. Y. (2012). Production of biomass and useful compounds from adventitious roots of high-value added medicinal plants using bioreactor. Biotechnology Advances,30, 1255–1267.
6. Benveniste, P. (2004). Biosynthesis and accumulation of sterols. Annual Review of Plant Biology,55, 429–457.
7. Bhat, R. A., & Panstruga, R. (2005). Lipid rafts in plants. Planta,223, 5–19.
8. Birt, D. F., Widrlechner, M. P., Hammer, K. D., Hillwig, M. L., Wei, J., Kraus, G. A., et al. (2009). Hypericum in infection: Identification of anti-viral and anti-inflammatory constituents. Pharmaceutical Biology,47, 774–782.
9. Butterweck, V. (2003). Mechanism of action of St John’s wort in depression: What is known? CNS Drugs,17, 539–562.
10. Capitani, D., Mannina, L., Proietti, N., Sobolev, A. P., Tomassini, A., Miccheli, A., et al. (2010). Monitoring of metabolic profiling and water status of Hayward kiwifruits by nuclear magnetic resonance. Talanta,82, 1826–1838.
11. Caraci, F., Crupi, R., Drago, F., & Spina, E. (2011). Metabolic drug interactions between antidepressants and anticancer drugs: focus on selective serotonin reuptake inhibitors and Hypericum extract. Current Drug Metabolism,12, 570–577.
12. Chakraborty, M., Karun, A., & Mitra, A. (2009). Accumulation of phenylpropanoid derivatives in chitosan-induced cell suspension culture of Cocos nucifera. Journal of Plant Physiology,166, 63–71.
13. Crockett, S. L., Poller, B., Tabanca, N., Pferschy-Wenzig, E. M., Kunert, O., Wedge, D. E., et al. (2011). Bioactive xanthones from the roots of Hypericum perforatum (common St John’s wort). Journal of the Science of Food and Agriculture,91, 428–434.
14. Crockett, S. L., & Robson, N. K. (2011). Taxonomy and chemotaxonomy of the genus Hypericum. Medicinal and Aromatic Plant Science and Biotechnology,5, 1–13.
15. Cui, X. H., Chakrabarty, D., Lee, E. J., & Paek, K. Y. (2010). Production of adventitious roots and secondary metabolites by Hypericum perforatum L. in a bioreactor. Bioresource Technology,101, 4708–4716.
16. Cui, X. H., Murthy, H. N., Jin, Y. X., Yim, Y. H., Kim, J. Y., & Paek, K. Y. (2011). Production of adventitious root biomass and secondary metabolites of Hypericum perforatum L. in a balloon type airlift reactor. Bioresource Technology,102, 10072–10079.
17. Fait, A., Fromm, H., Walter, D., Galili, G., & Fernie, A. R. (2008). Highway or byway: The metabolic role of the GABA shunt in plants. Trends in Plant Science,13, 14–19.
18. 1H-NMR-based metabolomics. Metabolomics. doi:10.1007/s11306-013-056-1.
19. Ferrari, F., Pasqua, G., Monacelli, B., Cimino, P., & Botta, B. (2005). Xanthones from calli of Hypericum perforatum subsp. perforatum. Natural Product Research,19, 171–176.
20. Franklin, G., Conceição, L. F., Kombrink, E., & Dias, A. C. (2009). Xanthone biosynthesis in Hypericum perforatum cells provides antioxidant and antimicrobial protection upon biotic stress. Phytochemistry,70, 60–68.
21. Griebel, T., & Zeier, J. (2010). A role for beta-sitosterol to stigmasterol conversion in plant-pathogen interactions. The Plant Journal,63, 254–268.
22. Hsieh, M. H., & Goodman, H. M. (2005). The Arabidopsis IspH homolog is involved in the plastid non mevalonate pathway of isoprenoid biosynthesis. Plant Physiology,138, 641–653.
23. Hunter, W. N. (2007). The non-mevalonate pathway of isoprenoid precursor biosynthesis. Journal of Biological Chemistry,282, 21573–21577.
24. Hunter, W. N. (2011). Isoprenoid precursor biosynthesis offers potential targets for drug discovery against diseases caused by apicomplexan parasites. Current Topics in Medicinal Chemistry,11, 2048–2059.
25. Iriti, M., & Faoro, F. (2009). Chitosan as a MAMP, searching for a PRR. Plant Signaling and Behavior,4, 66–68.
26. Jahangir, M., Kin, H. K., Choi, Y. H., & Verpoorte, R. (2008). Metabolomic response of Brassica rapa submitted to pre-harvest bacterial contamination. Food Chemistry,107, 362–368.
27. Jansen, J. J., Hoefsloot, H. C., Van der Greef, J., Timmerman, M. E., Westerhuis, J. A., & Smilde, A. K. (2005). ASCA: Analysis of multivariate data obtained from an experimental design. Journal of Chemometrics,19, 469–481.
28. Kiers, H. A., & ten Berge, J. M. (1994). Hierarchical relations between methods for simultaneous component analysis and a technique for rotation to a simple simultaneous structure. British Journal of Mathematical and Statistical Psychology,47, 109–126.
29. Kim, H. K., Choi, Y. H., & Verpoorte, R. (2011). NMR-based plant metabolomics: Where do we stand, where do we go? Trends in Biotechnology,29, 267–275.
30. Kim, H. K., & Verpoorte, R. (2010). Sample preparation for plant metabolomics. Phytochemical Analysis,21, 4–13.
31. Kinnersley, A. M., & Turano, F. J. (2000). Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Reviews in Plant Sciences,19, 479–509.
32. Kuzuyama, T., & Seto, H. (2003). Diversity of the biosynthesis of the isoprene units. Natural Products Reports,20, 171–183.
33. Lian, M. L., Chakrabarty, D., & Paek, K. Y. (2002). Effect of plant growth regulators and medium composition on cell growth and saponin production during cell suspension culture of mountain ginseng (Panax ginseng C.A. Mayer). Journal of Plant Biology,45, 201–206.
34. Manetti, C., Bianchetti, C., Bizzarri, M., Casciani, L., Castro, C., D’Ascenzo, G., et al. (2004). NMR-based metabonomic study of transgenic maize. Phytochemistry,65, 3187–3198.
35. Manetti, C., Bianchetti, C., Casciani, L., Castro, C., Di Cocco, M. E., Miccheli, A., et al. (2006). A metabonomic study of transgenic maize (Zea mays) seeds revealed variations in osmolytes and branched amino acids. Journal of Experimental Botany,57, 2613–2625.
36. Matsuda, F., Ishihara, A., Takanashi, K., Morino, K., Miyazawa, H., Wakasa, H., et al. (2010). Metabolic profiling analysis of genetically modified rice seedlings that overproduce tryptophan reveals the occurrence of its inter-tissue translocation. Plant Biotechnology,27, 17–27.
37. Miccheli, A., Aureli, T., Delfini, M., Di Cocco, M. E., Viola, P., Gobetto, R., et al. (1988). Study on influence of inactivation enzyme techniques and extraction procedures on cerebral phosphorylated metabolite levels by 31P NMR spectroscopy. Cellular and Molecular Biology,34, 591–603.
38. Modarai, M., Yang, M., Suter, A., Kortenkamp, A., & Heinrich, M. (2010). Metabolomic profiling of liquid Echinacea medicinal products with in vitro inhibitory effects on cytochrome P450 3A4 (CYP3A4). Planta Medica,76, 378–385.
39. Motavalizadehkakhky, A. (2012). Antimicrobial activity and chemical composition of essential oils of four Hypericum from Khorasan, Iran. Journal of Medicinal Plant Research,6, 2478–2487.
40. Nahrstedt, A., & Butterweck, V. (2010). Lessons learned from herbal medicinal products: The example of St. John’s Wort (perpendicular). Journal of Natural Products,73, 1015–1021.
41. Nürk, N. M., Madriñán, S., Carine, M. A., Chase, M. W., & Blattner, F. R. (2013). Molecular phylogenetics and morphological evolution of St. John’s wort (Hypericum; Hypericaceae). Molecular Phylogenetics and Evolution,66, 1–16.
42. Paek, K. Y., Murthy, H. N., Hahn, E. J., & Zhong, J. J. (2009). Large scale culture of ginseng adventitious roots for production of ginsenosides. Advances in Biochemical Engineering/Biotechnology,113, 151–176.
43. Pasqua, G., Avato, P., Monacelli, B., Santamaria, A. R., & Argentieri, M. P. (2003). Metabolites in cell suspension cultures, calli, and in vitro regenerated organs of Hypericum perforatum cv. Topas. Plant Science,165, 977–982.
44. Porzel, A., Farag, M. A., Mülbradt, J., & Wessjohann, L. A. (2013). Metabolite profiling and fingerprinting of Hypericum species: A comparison of MS and NMR metabolomics. Metabolomics. doi:10.1007/s11306-013-0609-7.
45. Rao, S. R., & Ravishankar, G. A. (2002). Plant cell cultures: Chemical factories of secondary metabolites. Biotechnology Advances,20, 101–153.
46. 1H-NMR spectral data from complex pharmaceutical preparations: St John’s wort. Planta Medica,72, 556–563.
47. Sacchettini, J. C., & Poulter, C. D. (1997). Creating isoprenoid diversity. Science,277, 1788–1789.
48. Saddiqe, Z., Naeem, I., & Maimoona, A. (2010). A review of the antibacterial activity of Hypericumperforatum. Journal of Ethnopharmacology,131, 511–521.
49. Sasse, J. M. (2003). Physiological actions of brassinosteroids: An update. Journal of Plant Growth Regulation,22, 276–288.
50. Shelp, B. J., Bown, A. W., & McLean, M. D. (1999). Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science,4, 446–452.
51. Sivanandhan, G., Arun, M., Mayavan, S., Rajesh, M., Mariashibu, T. S., Manickavasagam, M., et al. (2012). Chitosan enhances withanolides production in adventitious root cultures of Withania somnifera (L.) Dunal. Industrial Crops and Products,37, 124–129.
52. Smilde, A. K., Jansen, J. J., Hoefsloot, H. C., Lamers, R. J., Van der Greef, J., & Timmerman, M. E. (2005). ANOVA-simultaneous component analysis (ASCA): A new tool for analyzing designed metabolomics data. Bioinformatics,21, 3043–3048.
53. Snedden, W. A., Arazi, T., Fromm, H., & Shelp, B. J. (1995). Calcium/calmodulin activation of soybean glutamate decarboxylase. Plant Physiology,108, 543–549.
54. Tocci, N., D’Auria, F. D., Simonetti, G., Panella, S., Palamara, A. T., Debrassi, A., et al. (2013). Bioassay-guided fractionation of extracts from Hypericumperforatuminvitro roots treated with carboxymethylchitosans and determination of antifungal activity against human fungal pathogens. Plant Physiology and Biochemistry,70, 342–347.
55. Tocci, N., D’Auria, F. D., Simonetti, G., Panella, S., Palamara, A. T., & Pasqua, G. (2012). A three-step culture system to increase the xanthone production and antifungal activity of Hypericum perforatum subsp. angustifoliuminvitro roots. Plant Physiology and Biochemistry,57, 54–58.
56. Tocci, N., Simonetti, G., D’Auria, F. D., Panella, S., Palamara, A. T., Valletta, A., et al. (2011). Root cultures of Hypericum perforatum subsp. angustifolium elicited with chitosan and production of xanthone-rich extracts with antifungal activity. Applied Microbiology and Biotechnology,91, 977–987.
57. Toyomasu, T., Kagahara, T., Okada, K., Koga, J., Hasegawa, M., Mitsuhashi, W., et al. (2008). Diterpene phytoalexins are biosynthesized in and exuded from the roots of rice seedlings. Bioscience, Biotechnology, and Biochemistry,72, 562–567.
58. Vis, D. J., Westerhuis, J. A., Smilde, A. K., & Van der Greef, J. (2007). Statistical validation of megavariate effects in ASCA. BMC Bioinformatics,8, 322.
59. Walker, T. S., Pal, Bais H., & Vivanco, J. M. (2002). Jasmonic acid-induced hypericin production in cell suspension cultures of Hypericumperforatum L. (St. John’s wort). Phytochemistry,60, 289–293.
60. Yaeno, T., Matsuda, O., & Iba, K. (2004). Role of chloroplast trienoic fatty acids in plant disease defense responses. The Plant Journal,40, 931–941.
61. Yang, S. Y., Kim, H. K., Lefeber, A. W., Erkelens, C., Angelova, N., Choi, Y. H., et al. (2006). Application of two-dimensional nuclear magnetic resonance spectroscopy to quality control of ginseng commercial products. Planta Medica,72, 364–369.
62. Yin, H., Fretté, X. C., Christensen, L. P., & Grevsen, K. (2012). Chitosan oligosaccharides promote the content of polyphenols in Greek oregano (Origanum vulgare ssp. hirtum). Journal of Agriculture and Food Chemistry,60, 136–143.
63. Zhang, D. W., Liu, X., Xie, D., Chen, R., Tao, X. Y., Zou, J. H., et al. (2013). Two new diterpenoids from cell cultures of Salvia miltiorrhiza. Chemical & Pharmaceutical Bulletin,61, 576–580.
64. Zhao, J., Davis, L. C., & Verpoorte, R. (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances,23, 283–333.
65. Zobayed, S. M. A., Murch, S. J., Rupasinghe, H. P. V., & Saxena, P. K. (2004). In vitro production and chemical characterization of St. John’s wort (Hypericum perforatum L. cv ‘New Stems’). Plant Science,166, 333–340.
66. Zulak, K. G., Weljie, A. M., Vogel, H. J., & Facchini, P. J. (2008). Quantitative 1H NMR metabolomics reveals extensive metabolic reprogramming of primary and secondary metabolism in elicitor-treated opium poppy cell cultures. BMC Plant Biology,8, 5.