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Boophone Disticha Micropropagation and pharmacological evaluation of Boophone disticha Lee Cheesman Submitted in fulfilment of the academic requirements for the degree of Doctor of Philosophy Research Centre for Plant Growth and Development School of Life Sciences University of KwaZulu-Natal, Pietermaritzburg April 2013 COLLEGE OF AGRICULTURE, ENGINEERING AND SCIENCES DECLARATION 1 – PLAGIARISM I, LEE CHEESMAN Student Number: 203502173 declare that: 1. The research contained 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 reference section. Signed at………………………………....on the.....….. day of ……......……….2013 ______________________________ SIGNATURE i STUDENT DECLARATION Micropropagation and pharmacological evaluation of Boophone disticha I, LEE CHEESMAN Student Number: 203502173 declare that: 1. The research reported in this dissertation, except where otherwise indicated is the result of my own endeavours in the Research Centre for Plant Growth and Development, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg. 2. This dissertation has not been submitted for any degree or examination at any other University. 3. This thesis does not contain data, figures or writing, unless specifically acknowledged, copied from other researchers; and 4. Where I have produced a publication of which I am an author or co-author, I have indicated which part of the publication was contributed by me. Signed at……………………….............….on the.…........ day of …..….…........... 2013 ______________________________ SIGNATURE ii DECLARATION BY SUPERVISORS We hereby declare that we acted as Supervisors for this PhD student: Student’s Full Name: LEE CHEESMAN Student Number: 203502173 Thesis title: Micropropagation and pharmacological evaluation of Boophone disticha Regular consultation took place between the student and us throughout the investigation. We advised the student to the best of our ability and approved the final document for submission to the College of Agriculture, Engineering and Science Higher Degrees Office for examination by the University appointed Examiners. SUPERVISOR: __________________________ PROFESSOR J. VAN STADEN CO-SUPERVISOR: __________________________ PROFESSOR J.F. FINNIE CO-SUPERVISOR: __________________________ DR M.E. LIGHT iii PUBLICATIONS FROM THIS RESEARCH CHEESMAN, L., NAIR, J.J. & VAN STADEN, J. 2012. Antibacterial activity of β-crinane alkaloids from Boophone disticha (Amaryllidaceae). Journal of Ethnopharmacology 140: 405-408 iv CONFERENCE CONTRIBUTIONS FROM THIS RESEARCH 2010 36th Annual Congress of SAAB (South African Association of Botanists) Paper: Boophone disticha: In vitro propagation and secondary metabolite production (L. Cheesman, J. van Staden, J.F. Finnie and M.E. Light). North-West University, Potchefstroom. 2008 34th Annual Congress of SAAB (South African Association of Botanists) Paper: Difficulties encountered during the tissue culture of Boophone disticha (L.f.) Herb. (L. Cheesman, J. van Staden and J.F. Finnie). University of the Witwatersrand, Drakensville Resort, KwaZulu-Natal. v ACKNOWLEDGEMENTS I am very grateful to: My supervisor, Professor J. van Staden – for his continual advice, encouragement and support. My co-supervisor, Professor J.F. Finnie – for all his advice, reassurance and calming influence. My co-supervisor, Dr. M. E. Light – for all her help, support and encouragement. My parents – for all their support, motivation and unconditional love. Thank you so much for all you have done for me. Dr. Gary Stafford – for his support, encouragement and time. For all the hours spent in the field and on the computer enhancing presentations. All the staff and students at the Research Centre for Plant Growth and Development, for all the chats and help in the lab. I am grateful to The National Research Foundation for their financial support during my studies. vi ABSTRACT Boophone disticha (L.f.) Herb is one of the most widely distributed bulbous species in southern Africa. Of Africa’s many bulbous plants, it is widely known for its poisonous and medicinal properties. It is of considerable ethnobotanical interest in traditional medicine because of its hallucinogenic alkaloids and it has great potential as an ornamental due to its fan-shaped foliage and large umbel of bright pink to deep red flowers. In South Africa, many bulbous plants are used in traditional medicine which are collected from wild populations. The high demand for trade and use of such plants, that are destructively harvested, places an enormous pressure on natural populations. According to the Red List of South African Plants, the conservation status of B. disticha has been listed as ‘declining’. It is, therefore, important to develop conservation strategies for these medicinal plants, such as the development of alternative propagation methods. Micropropagation is a useful technique for rapid clonal multiplication of plant material which could alleviate the pressure on the wild plant populations, as well as potentially producing useful secondary metabolites. The in vitro induction of storage organs is especially beneficial as it can limit the loss of plants during acclimatization since bulblets are generally hardier than shoots or plantlets. Thus, the main aim of this research was to establish a micropropagation protocol which could be a valuable tool for conservation of this plant species. In addition, B. disticha plants were assessed in various ethnopharmacological assays to evaluate their medicinal properties, and a preliminary study on the population genetics was also conducted. As part of the development of a suitable micropropagation protocol, the effect of environmental and physiological factors on the initiation and growth of bulblets were investigated. These factors included the effect of various plant growth regulators, carbohydrates, temperature, photoperiod and liquid culture. Different explants (i.e. ovaries, anthers, filaments, pedicels, embryos, seeds and bulb twin-scales) were tested to determine which explants were the most suitable for subsequent experiments. Although success was limited, twin-scales proved to be the most suitable explant and it was demonstrated that activated charcoal, ascorbic acid and N6- benzyladenine were required as media supplements. vii Abstract Antimicrobial activity was tested between different plant parts and seasons. The plant parts (roots, leaves, outer and inner bulb scales) were extracted with a range of differing polarity solvents. These were screened for antibacterial activity against Bacillus subtilis, Staphylococcus aureus, Escherichia coli and Klebsiella pneumoniae, and for antifungal activity against Candida albicans. Extracts from roots of plants collected in spring and summer showed the best antimicrobial activity against B. subtilis, E. coli and K. pneumoniae, indicating that plant part and collection time do affect activity. In vitro grown bulblets also showed antimicrobial activity, demonstrating that antibacterial properties were maintained in cultured plantlets. Extracts from plants collected in summer were tested for mutagenicity using the Ames test (Salmonella/microsome assay; plate incorporation method, with or without metabolic activation). None of the extracts tested were found to induce mutations and also did not modify the effect of the mutagenic compounds (2AA with S9 and 4NQO without S9). Although the results do not indicate a mutagenic response, this does not necessarily confirm that it is not mutagenic nor carcinogenic to other bacterial strains, however, B. disticha must be used with caution, especially considering the levels of alkaloids in the plant. The two major constituent alkaloids of B. disticha were identified as buphanidrine and distichamine. In the antibacterial assay, both compounds exhibited broad-spectrum micromolar- level activity against the two Gram-positive and two Gram-negative bacteria tested. The best MIC value, of 0.063 mg/ml, was found for bupanidrine/distichamine against S. aureus, E. coli and K. pneumonia. The isolated compounds were tested and found to be neither mutagenic nor toxic at the concentrations tested. Thus, buphanidrine and distichamine are thought to be the constituents likely responsible for the medicinal properties of the plant. To determine the level of genetic variation between different populations of B. disticha, plants were collected from six wild populations in KwaZulu-Natal, South Africa. DNA was isolated and tested for genetic variation using ten Inter Simple Sequence Repeat (ISSR) primers. The level of inter-population polymorphism ranged between 23% and 39%, showing that the populations had low genetic polymorphism. From the genetic
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