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University of Kwazulu-Natal UNIVERSITY OF KWAZULU-NATAL PHYTOCHEMICAL INVESTIGATION AND TISSUE CULTURE STUDIES ON THE SOUTH AFRICAN KNOB TREES, ZANTHOXYLUM CAPENSE AND SENEGALIA NIGRESCENS BY BODEDE OLUSOLA SUNDAY 2017 PHYTOCHEMICAL INVESTIGATION AND TISSUE CULTURE STUDIES ON THE SOUTH AFRICAN KNOB TREES, ZANTHOXYLUM CAPENSE AND SENEGALIA NIGRESCENS BODEDE OLUSOLA SUNDAY 2017 A thesis submitted to the School of Chemistry and Physics, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville, for the degree of Doctor of Philosophy. This Thesis has been prepared according to Format 4 as outlined in the guidelines from the College of Agriculture, Engineering and Science which states: This is a thesis in which chapters are written as a set of discrete research papers, with an overall introduction and final discussion where one (or all) of the chapters has already been published. Typically, these chapters will have been published in internationally-recognised, peer- reviewed journals. As the candidate’s supervisor(s), I have approved this thesis for submission. Supervisor: Signed: --------------------------------Name: ------------------------- Date: -------------- Co-Supervisor: Signed: --------------------------------Name: ------------------------- Date: -------------- ii ABSTRACT Zanthoxylum capense and Senegalia nigrescens, of the Rutaceae and Fabaceae families, respectively, are both South African plant species used in traditional medicine and have a common knob-bearing feature. However, there are limited reports on the phytochemistry of these plants that could provide a scientific basis for their ethnomedicinal use. Due to the depletion of these medicinal plants in the wild and the global search for new pharmacologically-active compounds of plant origin, alternative routes to conventional systems of propagation and the harvesting of their bioactive phytocompounds for pharmaceutical applications is deemed necessary. The aim of this research was therefore twofold; firstly, to isolate and characterise the secondary metabolites in the plants and to test them for biological activity and secondly, to promote their conservation using tissue culture techniques. The phytochemical analysis of Z. capense yielded ten compounds including alkaloids, coumarates, lignans, flavonoids, triterpenoids and pigments. Amongst the compounds isolated, chelerythrine (IC50 = 95.4 and 153.9 µM) and dodecyl-trans-p-coumarate (IC50 = 15.1 and 182.4 µM) had the highest cytotoxicity in MCF-7 and in Caco-2 tumor cell lines, respectively. The seeds of Z. capense were subjected to pre-sowing treatments prior to germination, and soaking in hot water or GA3 was found to overcome dormancy in the species. The potential of the leaves, knobs and roots of Z. capense was further evaluated for the green synthesis of silver nanoparticles (AgNPs) and the results showed the leaves to be the most effective bioreductants. The biosynthesised AgNPs were more effective than sodium hypochlorite (NaOCl) and sodium dichloroisocyanurate (NaDCC) in controlling in vitro fungal contamination. Still, the former did not eliminate the fungi but delayed their emergence, thereby promoting the impetus for the iii identification and characterisation of Z. capense fungal endophytic strains using standard DNA extraction and sequencing methods. In S. nigrescens, a series of lupane-type triterpenoids, kaurene diterpenoids, flavonoids and a long-chain alcohol were isolated. A new ent-kaurene diterpenoid (ent-kaur-15-en-18,20-diol) and ent-kaur-15-en-18-ol, found for the first time in the plant, were amongst the compounds isolated. Compounds and crude extracts from S. nigrescens were tested for their antimicrobial potential against nine bacterial strains including a well-known quorum sensing inhibitor indicator strain, Chromobacterium violaceum. The novel ent-kaurene diterpene (ent-kaur-15- en-18,20-diol) and the flavonoids (quercetin-3-O-methyl ether and melanoxetin) showed promising anti-quorum sensing activity, following a qualitative agar-overlay assay. A micropropagation protocol was developed for S. nigrescens using explants derived from its seedlings obtained from mechanically-scarified seeds sown on full strength Murashige and Skoog basal medium (MS). There were no significant differences in the number of shoots produced across all the treatments of kinetin (KIN) and benzylaminopurine (BAP) that were tested, although the treatment containing 1.0 mg L-1 KIN produced a significantly higher shoot length (14.17 mm) than 0.5, 1.0 and 2.0 mg L-1 BAP (7.67, 6.75 and 8.70 mm, respectively). Rooting of S. nigrescens was best achieved using one quarter strength MS supplemented with either indole-3-acetic acid (IAA) or indole-3-butyric acid (IBA). The auxin, 2,4- dichlorophenoxyactic acid, was found to be effective for inducing callus from S. nigrescens explants. Spectrochemical analysis of the root-derived calli revealed their potential to produce the phytocompounds, quercetin, quercetin-3-O-methyl ether, ent-kaur-15-en-18-ol and ent- kaur-15-en-18,20-diol. Chemomorphological distribution in Z. capense showed knobs to possess the most biologically-active compounds as chelerythrine and dodecyl-trans-p-coumarate were isolated from knobs only. On the other hand, there was no difference in the phytochemical profile of iv the stem bark and knobs of S. nigrescens. The findings of this research provide a scientific rationale for the use of both species in traditional medicine. The therapeutic potential of the new compounds found in S. nigrescens may be synthetically enhanced to produce new drugs. The identification of the fungal endophytes that caused extensive fungal contamination in Z. capense in vitro cultures can provide much needed information for decontamination protocols such as the selection of fungicides. The micropropagation and callus induction studies on S. nigrescens provide preliminary information towards the large-scale propagation of the plant. v SUMMARY OF ISOLATED COMPOUNDS Compounds (A1 – A10) isolated from Z. capense (chapter three) A1 chelerythrine A2 6-hydroxydihydrochelerythrine A3 rutaecarpine A4 sesamin A5 dodecyl-trans-p-coumarate A6 catechin A7 lupeol A8 β-sitosterol A9 pheophytin a A10 lutein vi vii Compounds (B1 – B11) isolated from S. nigrescens (chapter six) B1 30-hydroxylup-20(29)-en-3β-ol B2 3β-hydroxy-20(29)-en-lupan-30-al B3 lupeol (same as A7) B4 stigmasterol B5 ent-kaur-15-en-18-ol B6 ent-kaur-15-en-18,20-diol B7 tetracosan-1-ol B8 melanoxetin B9 quercetin B10 quercetin-3-O-methyl ether viii ix ABBREVIATIONS 13C-NMR C-13 nuclear magnetic resonance spectroscopy 1H-NMR proton nuclear magnetic resonance spectroscopy 2,4-D 2,4-dichlorophenoxyacetic acid Ac acetate ANOVA analysis of variance BAP benzylaminopurine br broad resonance c concentration CC column chromatography COSY correlated spectroscopy d doublet dd double doublet DEPT distortionless enhancement by polarization transfer DPPH 2,2-diphenyl-1-picrylhydrazyl EIMS electron impact mass spectroscopy FRAP ferric reducing antioxidant potential FTIR fourier transform infrared GC-MS gas chromatography-mass spectrometry HMBC heteronuclear multiple bond coherence x HRMS high resolution mass spectroscopy HSQC heteronuclear single quantum coherence Hz hertz IAA indole-3-acetic acid IBA indole-3-butyric acid IR infrared KIN kinetin m multiplet Me methyl mp melting point MS Murashige and Skoog basal medium NOESY nuclear overhauser effect spectroscopy PGR plant growth regulator RSA radical scavenging activity s singlet t triplet TDZ thidiazuron TLC thin layer chromatography UV ultraviolet xi DECLARATIONS DECLARATION 1 - PLAGIARISM I, Bodede Olusola Sunday, declare that 1. The research reported in this thesis, except where otherwise indicated, is my original research. 2. This thesis has not been submitted for any degree or examination at any other university. 3. This thesis does not contain other persons’ data, pictures, graphs or other information, unless specifically acknowledged as being sourced from other persons. 4. This thesis does not contain other persons' writing, unless specifically acknowledged as being sourced from other researchers. Where other written sources have been quoted, then: a. Their words have been re-written but the general information attributed to them has been referenced. b. Where their exact words have been used, then their writing has been placed in italics and inside quotation marks, and referenced. 5. This thesis does not contain text, graphics or tables copied and pasted from the Internet, unless specifically acknowledged, and the source being detailed in the thesis and in the References sections. Signed: …………………………………. xii DECLARATION 2 - PUBLICATIONS Publication 1 Bodede, O., Moodley, R., Shaik, S., Singh, M. 2017. Phytochemical analysis with antioxidant and cytotoxicity studies of the bioactive principles from Zanthoxylum capense (small knobwood), Anticancer Agents in Medicinal Chemistry, 17 (4), 627 – 634. Publication 2 Bodede, O., Shaik, S., Moodley, R. 2015. Germination response of Zanthoxylum capense (small knobwood) seed to different pre-treatment protocols, African Journal of Traditional, Complementary and Alternative Medicine, 12 (5), 70-73. Publication 3 Bodede, O., Shaik, S., Govinden, R., Moodley, R. 2017. Evaluating the bioreducing potential of the leaves, knobs and roots of Zanthoxylum capense (small knobwood) for the synthesis of silver nanoparticles, applicable to in vitro fungal contamination control, Advances in Natural Sciences: Nanoscience and Nanotechnology, 8 (2017)
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