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The Best of Santalum Album: Essential Oil Composition, Biosynthesis and Genetic Diversity in the Australian Tropical Sandalwood Collection

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The Best of Santalum Album: Essential Oil Composition, Biosynthesis and Genetic Diversity in the Australian Tropical Sandalwood Collection The best of Santalum album: Essential oil composition, biosynthesis and genetic diversity in the Australian tropical sandalwood collection Christopher G. Jones Apologies to Kerstin Bach and Carlos Santana… This thesis is presented for the degree of Doctor of Philosophy The University of Western Australia School of Plant Biology Faculty of Natural and Agricultural Sciences June 2008 i DECLARATION FOR THESIS CONTAINING PUBLISHED WORK AND / OR WORK PREPARED FOR PUBLICATION This thesis contains published work and / or work prepared for publication, some of which has been co-authored. The bibliographic details of the works and where they appear in the thesis are set out below. (The candidate must attach to this declaration a statement detailing the percentage contribution of each author to the work. This must be signed by all authors. Where this is not possible, the statement detailing the percentage contribution of authors should be signed by the candidate‟s co-ordinating supervisor). The following manuscripts have either been published or have been submitted to scientific journals. Chapter 2: Jones CG, Plummer JA (2008) “Sandalwood”. In 'A Compendium of Transgenic Crop Plants: Forest Tree Species'. (Eds C Kole and TC Hall) pp. in press. (Blackwell Publishing: Oxford UK) Chapter 3: Jones CG, Barbour EL, Plummer JA and Byrne M. “Genetic diversity of the Australian tropical sandalwood collection – biogeographic origins and tree improvement potential”. Submitted to Tree Genetics and Genomes (March 2008) Chapter 4: Jones CG, Ghisalberti EL, Barbour EL, Plummer JA. (2006) “Quantitative co-occurrence of sesquiterpenes; a tool for elucidating their biosynthesis in Indian Sandalwood, Santalum album L”. Phytochemistry, 67, 2463-2468 Chapter 5: Jones CG, Keeling CI, Ghisalberti EL, Barbour EL, Plummer JA and Bohlmann J. “Isolation of cDNAs and functional characterisation of two multi-product TPS enzymes from sandalwood, Santalum album L”. Accepted in Archives of Biochemistry and Biophysics (May 2008). The contribution of work for each manuscript is 90% by the candidate of this thesis, Christopher G Jones and 10% for all other authors, except for Chapter Five where the candidate contributed 70%, C I Keeling 20% and 10% for all other authors. Candidate, Christopher G Jones Signature:…………………………………………………………………… Co-ordinating supervisors, Julie A Plummer and Emilio L Ghisalberti Signatures:…………………………………………………………………… ii Statement of Original Contribution The research presented in this thesis constitutes an original contribution to high-value tropical forestry, genetics and secondary metabolite biosynthesis. The ideas and hypotheses are my own, with help and critique from my supervisors to test these. In the experimental sections, other people who have helped in any significant capacity are dutifully acknowledged as co-authors or in the acknowledgements sections of each manuscript. This thesis is presented as a summary of my PhD course at the University of Western Australia, and has not been used elsewhere for credit towards any other endeavours at any other institution. Christopher Graham Jones June 2008 iii Abstract An investigation into the causes of heartwood and essential oil content of Australian plantation sandalwood, Santalum album was undertaken. Genetic diversity of 233 S. album, five S. austrocaledonicum and fifteen S. macgregorii trees growing in the Forest Products Commission arboretum, Kununurra WA, was assessed using nuclear and chloroplast RFLPs. Santalum spicatum was chosen as an out-group. Nuclear genetic diversity of the S. album collection was very low, with observed and expected heterozygosity levels of 0.047. This was lower than the results previously reported in the literature for trees in India, however a different technique was used. Based on allelic patterns, the collection was able to be categorised into 19 genotypes; each representing some shared genetic origin. Some groups were highly redundant with 56 trees being represented, while others were populated by just one tree. The essential oil yield and heartwood contents of trees from these genetic groups were compared. Yields were highly variable both within and between groups of trees which share a common genetic history, suggesting a significant environmental component was contributing to the observed phenotype, despite identical soil and climatic conditions. Ancestral lineages were tested using chloroplast RFLPs, although a lack of shared mutations between species made this difficult. Only one S. album tree originating from Timor was resolved using nuclear RFLPs, with the other trees being grouped with material sourced from India. There was no resolution of Indian S. album from Timorese using chloroplast RFLPs, however one S. album tree grown from Indian seed possessed a single unique mutation. The low genetic diversity of the Australian S. album collection is likely to be a combination of incomplete seed sourcing and highly restricted gene flow during the evolution of the species. Combined with information gathered on the phylogeny of the genus by other researchers, S. album is postulated to have originated from an over-sea dispersal out of northern Australia or Papua New Guinea 3 to 5 million years ago. Essential oil yield and composition was assessed for 100 S. album trees growing in the collection, ranging in age from 8 to 17 years. Oil content of heartwood ranged from 30 mg g-1 to 60 mg g-1, and the transition zone 36 mg g-1 to 90 mg g-1. Sapwood contained almost no sesquiterpene oils. Despite the highly variable total oil yields, the chemical profile of the oil did not vary, suggesting there was limited genetic diversity within this region of the genome. Strong, positive correlations existed between iv sesquiterpenoids in the essential oil of S. album. This was particularly evident in the santalenes and -bergamotene, although trends were also seen in the curcumenes, bisabolene and bisabolol, and an unidentified group of sesquiterpenes. Co-occurrence patterns indicate shared chemical intermediates from which compounds are partitioned, resulting in multiple product formation. To further test the multiple product hypothesis, two terpene synthase (TPS) genes were isolated from S. album leaf and wood cDNA. These were cloned and the enzymes were heterologously expressed in Escherichia coli. One enzyme, SasesquiTPS1 converted the universal sesquiterpene precursor farnesyl diphosphate into germacrene D-4-ol, helminthogermacrene, -bulnesene, -muurolene - and -selinene. The other enzyme, SamonoTPS1 converted geranyl diphosphate into (+) -terpineol and ()-limonene, with small amounts of sabinene, linalool, - terpinolene, myrcene and geraniol. These represent the first TPS genes to be isolated from sandalwood and will enable further elucidation of oil biosynthesis genes. This thesis compiles a three-pronged approach to understanding the underlying causes of oil yield variation in S. album. As a species for which so little is known, the research presented here provides a major leap forward for tree improvement, breeding and silviculture. Hence the best of Santalum album research is presented. v Acknowledgements I am indebted to my supervisors, Julie Plummer and Emilio Ghisalberti for their support, advice and guidance throughout my entire PhD. I‟m yet to meet a student with a sour thing to say about either person. What I have appreciated most is the freedom to explore widely, but also gave sound advice at keeping it relevant and answer the question at hand. This project would not have been possible without the generous support of the Forest Products Commission of Western Australia and the dedication of my industry supervisor, Liz Barbour. Without Liz, the sandalwood project would have surely lost momentum. I am most grateful to Margaret Byrne and the Science Division at the West Australian Department of Environment and Conservation for her solid knowledge of population genetics and molecular biology. Often, there were few people in the entire state of WA who could help me with a specific problem, and Margaret‟s advice was always worth the wait. I owe more than morning tea to Bronwyn and Maggie at the lab, for if it weren‟t for them, the radiation work would have been on the 6 o‟clock news for sure. Also, I thank Lin Wong for her help with DNA extractions and digest preparations. I am most grateful to Jörg Bohlmann, who kindly let me into his lab at the University of British Columbia, Vancouver. I learnt molecular biology for the first time, as well as the finer details of terpenoid biosynthesis in his lab. Without his generous support, this project would not be nearly as exciting. I look forward to many future collaborations with Jörg and his research group. I am appreciative for the funding provided to this Linkage Project by the Australian Research Council and the Forest Products Commission. In addition to this, the generous awards, scholarships and travelling fellowships I have received throughout my PhD have made life much easier. In particular, The Commonwealth Government Department of Agriculture, Fisheries and Forestry Science and Innovation Award vi (2005) enabled me to conduct the gene discovery and biochemical expression studies detailed in Chapter 5. This has opened several doors for future research, including a collaborative project with the Michael Smith Laboratories at UBC. Travel costs were minimised courtesy of the Mike Carroll travelling fellowship and the UWA Postgraduate Students Association Travel Award, as well as the Mary Janet Lindesay of Yanchep
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