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Universidade Do Algarve UNIVERSIDADE DO ALGARVE FACULDADE DE CIÊNCIAS E TECNOLOGIA PHYTOCHEMICAL STUDIES AND BIOLOGICAL ACTIVITY OF CARNIVOROUS PLANTS FROM THE MEDITERRANEAN REGION (Tese para a obtenção do grau de doutor no ramo de Ciências Biotecnológicas, especialidade de Biotecnologia Vegetal) TOMÁS GREVENSTUK FARO 2010 UNIVERSIDADE DO ALGARVE FACULDADE DE CIÊNCIAS E TECNOLOGIA PHYTOCHEMICAL STUDIES AND BIOLOGICAL ACTIVITY OF CARNIVOROUS PLANTS FROM THE MEDITERRANEAN REGION (Tese para a obtenção do grau de doutor no ramo de Ciências Biotecnológicas, especialidade de Biotecnologia Vegetal) TOMÁS GREVENSTUK Orientador: Prof. Doutora Anabela Romano FARO 2010 DECLARATION This thesis contains results that were, or will be published in collaboration with A Romano, S Gonçalves, J Vervoort, JJJ van der Hooft, P de Waard, C Quintas, N Gaspar, AL Escapa, N Coelho, S Almeida, JMF Nogueira and N Neng. I hereby declare that this thesis is a presentation of original research work. Wherever contributions of others are involved, every effort is made to indicate this clearly, with due reference to the literature, and acknowledgement of collaborative research and discussions. Faro, September 2010 Tomás Grevenstuk i ACKNOWLEDGEMENTS I would like to express my sincere gratitude and appreciation to my supervisor, Professor Dr. Anabela Romano, for offering me the chance to apply as a PhD student at the Plant Biotechnology Laboratory. I am very grateful for her help with outlining this research project, guidance, encouragement, good spirits and for the special bond that was created and strengthened throughout the past years, but also for taking the time for the thorough revision of this thesis. I am very grateful to Dr. Sandra Gonçalves, my “unofficial” co-supervisor, without whose support, motivation and encouragement, I would possibly not have considered a career following this direction. I am very grateful for her help with planning and guidance of great part of the experimental work, for the proof-reading, for solving countless setbacks and for giving her opinion on so many occasions. I would like to thank Professor Dr. Jacques Vervoort for welcoming me at the Wageningen NMR Centre (Wageningen University), where it was possible to work with state-of-the-art LC-MS and LC-NMR equipment and learn the basics of NMR fundaments and interpretation of spectra for structure elucidation. I am thankful for his revision of Chapter 3 of this thesis and would like to add that his expertise and understanding in this field was inspiring and added considerably to my graduate experience. I am very grateful to Justin van der Hooft for the training and help in the operation of the analytical equipment, interpretation of results, for his many comments and suggestions, but mostly for his patience in helping a rookie in NMR analysis. I would also like to thank Dr. Pieter de Waard for assistance in NMR experiments. I am also grateful to Professors Drs. Célia Quintas and Nelma Gaspar (Laboratory of Microbiology, ISE, Algarve University) for their help with the antimicrobial activity assays. I am grateful to Professor Dr. Gabriela Bernardo-Gil for receiving me at the Supercritical Extraction Laboratory (IST, Technical University of Lisbon) and for putting the supercritical extraction equipment at our disposal. I would also like to thank Paula Pereira and Dr. Maria João Cebola for their assistance and guidance with the experiments. I would also like to thank Professor Dr. José Manuel Florêncio Nogueira and Nuno Neng of the Laboratory of Chromatography and Capillary Electrophoresis (FC, iii University of Lisbon) for the help given with the quantification of plumbagin by HPLC in Chapter 5. Also, I would like to thank Natacha Coelho and Sara Almeida for their help with the bioassay experiments, and Ana Luísa Escapa and once more Natacha Coelho for helping with the development of micropropagation protocols. I would also like to thank my lab colleagues and Rosália Almeida, our lab technician, for their help and kind disposition. I am very grateful to Dr. Miguel Porto for providing information on the location of natural populations of D. intermedia, D. rotundifolia and to Professor Dr. Henrique Pereira (Peneda-Gerês National Park, ICNB) and Mr. António Rebelo who very kindly provided seeds of P. vulgaris. I am also grateful to Dr. Jorge Jesus for collecting P. lusitanica seeds. I greatly appreciate the financial support of the Portuguese Foundation for Science and Technology by funding the PhD fellowship (FCT, Grant SFRH/BD/31777/2006) and the European Community activity Large-Scale Facility Wageningen NMR Center (FP6- 2004-026164 (2006–2009), which supported the research activities held at Wageningen, the Netherlands. I would also like to thank my parents for their loving support and for creating an environment in which following this path seemed so natural, and my dear friends, for their company, high spirits and for not reminding me of work in their presence! And last but not least Alexandra, not necessarily for coming along at the right time, but for the very special person she is, and for the incredible amount of patience she had with me during the redaction of this manuscript. And of course, the right kind of inspiration is always welcome… iv LIST OF ABBREVIATIONS δ chemical shift 1D one-dimensional 2D two-dimensional AAPH 2,2’-azobis-2-methyl-propanimidamide dihydrochloride ABTS 2,2’-azinobis(3-ethylbenzothiazoline-6-sulfonic acid ABTS•+ ABTS radical cation amu atomic mass units ANOVA analysis of variance AOC antioxidant capacity ATCC American type culture collection AUC area under curve BA 6-benzyladenine CFU colony forming units COSY correlation spectroscopy DAD diode array detector (or diode array detection) DMSO dimethyl sulfoxide DQF double-quantum-filtered EI electron impact ESI electrospray ionization F-C Folin-Ciocalteu g, mg, µg gram, milligram, microgram GAE gallic acid equivalent h, min, s hour, minute, second HAT hydrogen atom transfer HMBC heteronuclear multiple bond coherence HPLC high performance liquid chromatography HSQC heteronuclear single quantum coherence HTS high throughput screening Hz, kHz, MHz, GHz Hertz, kiloHertz, megaHertz, gigaHertz i.d. internal diameter IAA indole-3-acetic acid IBA indole-3-butyric acid INADEQUATE Incredible Natural Abundance Double Quantum Transfer Spectroscopy IZD inhibition zone diamters K Kelvin Kin kinetin L, mL, µL liter, milliliter, microliter cm, mm, nm centimeter, millimeter, nanometer m/z mass to charge ratio MAE microwave-assisted extraction mAU milli absorbance units MDR multidrug resistance pumps MHA Mueller Hinton agar MHB Mueller Hinton broth MIC minimum inhibitory concentration mM, µM milllimolar, micromolar v MPa megaPascal MRSA methicillin-resistant Staphylococcus aureus MS mass spectrometer (or mass spectrometry) MS Murashige and Skoog culture medium NAA 2-naphthaleneacetic acid NCCLS national committee for clinical laboratory standards NMR nuclear magnetic resonance NOESY nuclear-Overhauser-effect spectroscopy ºC degree Celsius ORAC oxygen radical absorption capacity P statistical probability PCA plate count agar PGR plant growth regulator ppm part per milion ROESY rotational frame nuclear Overhauser effect spectroscopy ROS reactive oxygen species rpm revolutions per minute S/N signal to noise ratio SE standard error SET single electron transfer SFE supercritical fluid extraction SPE solid phase extraction SPSS statistical package for the social sciences TE trolox equivalent TEAC trolox equivalent antioxidant capacity TOCSY total-correlation spectroscopy TOF time of flight tR retention time UAE ultrasound assisted extraction UV ultraviolet v/v volume per volume w/v weight per volume Zea zeatin vi ABSTRACT In this thesis several studies were conducted with four carnivorous plant species which occur on Portuguese territory: Pinguicula lusitanica, Pinguicula vulgaris, Drosera intermedia and Drosera rotundifolia. Most habitats of these plants are threatened and natural populations are scarce, therefore micropropagation protocols were developed to produce biomass for the subsequent studies. Efficient micropropagation protocols were developed for P. lusitanica and D. intermedia enabling large scale biomass production, while protocols for the other two species have still to be optimized (in Chapter 2). The in vitro established cultures represent active germplasm collections of Portuguese natural populations and contribute therefore for their conservation. In Chapter 3 extracts prepared from micropropagated plant material were analyzed using state of the art HPLC-ESI-MS and HPLC-SPE-NMR equipment which enabled the identification of the major secondary metabolites produced by P. lusitanica and D. intermedia, directly from essentially crude extracts. The metabolites identified in P. lusitanica belong to the iridoid glucosides and caffeoyl phenylethanoid glycosides and D. intermedia was shown to produce mainly flavonoid glucosides, ellagic acid derivatives and the naphthoquinone plumbagin. The evaluation of the biological activities of these extracts, compiled in Chapter 4, showed that the methanol extract of P. lusitanica has considerable antioxidant activity and that the n-hexane extract of D. intermedia has high antimicrobial potential. In Chapter 5 a method for the extraction of plumbagin from micropropagated D. intermedia plants was optimized and its potential as an alternative for bioprospection evaluated. It was shown that the commercial exploitation of plumbagin from D. intermedia cultures might be viable and that UAE
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