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The Killer of Socrates Exposed – Coniine in the Plant Kingdom

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The Killer of Socrates Exposed – Coniine in the Plant Kingdom IENCE C • •S T S E C The killer of Socrates exposed – Coniine in the plant N O H I N kingdom S O I V Dissertation L • O S 135 G Coniine, a piperidine alkaloid, is known from poison hemlock T Y H • R (Conium maculatum L.), twelve Aloe species and Sarracenia flava G I E L VTT SCIEN CE S H E G L. Its biosynthesis is not well understood, although a possible route A I R H C starts with a polyketide formed by a polyketide synthase (PKS). H This study focused on identification and characterization of PKS- 1 3 5 genes involved in coniine formation, induction of callus from plants containing hemlock alkaloids and investigation of the possibility to elicitate the alkaloid pathway in cell culture in order to understand coniine biosynthesis. Plant materials involved in different stages of this study were investigated for their alkaloid content using gas chromatography-mass spectrometry. A novel type of PKS, CPKS5, was identified as the starter candidate for the initiation of coniine biosynthesis by catalysing the synthesis of the carbon backbone from one butyryl-CoA and two malonyl-CoA moieties. When elicitated, poison hemlock cell cultures produced furanocoumarins but no piperidine alkaloids. The hemlock alkaloids are wider distributed than previously has been thought among Sarracenia, and Aloe spp. contain a new alkaloid for the genus. These results together pave the way towards possible utilization of hemlock alkaloids. The killer of Socrates ISBN 978-951-38-8459-8 (Soft back ed.) exposed – Coniine in the T he killer of S o crates exp ose d – C o niine in the plant... ISBN 978-951-38-8458-1 (URL: http://www.vttresearch.com/impact/publications) ISSN-L 2242-119X plant kingdom ISSN 2242-119X (Print) ISSN 2242-1203 (Online) http://urn.fi/URN:ISBN:978-951-38-8458-1 Hannu Hotti VTT SCIENCE 135 The killer of Socrates exposed – Coniine in the plant kingdom Hannu Hotti VTT Technical Research Centre of Finland Ltd Doctoral Programme in Plant Sciences Department of Agricultural Sciences Faculty of Agriculture and Forestry University of Helsinki Thesis for the degree of Doctor of Science (Agriculture and Forestry) to be presented with due permission for public examination and criticism in auditorium 1041 in Biocentre 2 (Viikinkaari 5), at University of Helsinki, on the 14th October 2016 at 12 o'clock. ISBN 978-951-38-8459-8 (Soft back ed.) ISBN 978-951-38-8458-1 (URL: http://www.vttresearch.com/impact/publications) VTT Science 135 ISSN-L 2242-119X ISSN 2242-119X (Print) ISSN 2242-1203 (Online) http://urn.fi/URN:ISBN:978-951-38-8458-1 Copyright © VTT 2016 JULKAISIJA – UTGIVARE – PUBLISHER Teknologian tutkimuskeskus VTT Oy PL 1000 (Tekniikantie 4 A, Espoo) 02044 VTT Puh. 020 722 111, faksi 020 722 7001 Teknologiska forskningscentralen VTT Ab PB 1000 (Teknikvägen 4 A, Esbo) FI-02044 VTT Tfn +358 20 722 111, telefax +358 20 722 7001 VTT Technical Research Centre of Finland Ltd P.O. Box 1000 (Tekniikantie 4 A, Espoo) FI-02044 VTT, Finland Tel. +358 20 722 111, fax +358 20 722 7001 Cover image: Hannu Hotti Juvenes Print, Tampere 2016 Preface This work was carried out as a joint Ph.D. project at VTT Technical Research Centre of Finland Ltd and at the Department of Agricultural Sciences, Faculty of Agriculture and Forestry, University of Helsinki during the years 2009-2016. The Plant Biotech- nology and Metabolomics research team at VTT provided facilities and expertise in plant and cell culture together with possibilities for the chemical analysis of small molecules. I received support from the Gerbera Laboratory of the Department of Agricultural Sciences in cloning and analysing polyketide synthase genes and their products. The management of VTT is acknowledged for providing excellent working facilities. This study was funded by a Doctoral Program in Plant Sciences, VTT, the Academy of Finland (project number 138808, PKRed), Oskar Öflunds Stiftelse, Eteläsuomalaisten ylioppilaiden säätiö, Societas pro Fauna et Flora Fennica, Otto A. Malmin lahjoitusrahasto and University of Helsinki. I am grateful to my supervisors, docent Heiko Rischer, docent Kirsi-Marja Oks- man-Caldentey and professor Teemu Teeri. Your commitment, advice, and support through these long years enabled me to complete this project. Especially I thank my main supervisor Heiko Rischer, who always had time and advice for my work. I thank my follow-up committee, whose members alongside my supervisors were Anneli Ritala and Anna Kärkönen. Also, I thank fellow members in the PKRed- project, Suvi Häkkinen, Juha Kontturi and Milla Pietiäinen along with the project leaders, Heiko Rischer, and Teemu Teeri, for monthly meetings to discuss various research topics related to the project. I thank my co-authors Heiko Rischer, Tuulikki Seppänen-Laakso, Gopal Peddinti, Suvi Häkkinen, Philipp Meier, Mikko Arvas and Teemu Teeri. With you, I have learned a lot about academic writing and all that goes with it. I am grateful for all the advice and expertise I received from Jaana Rikkinen, Tuuli Teikari, and Airi Hyrkäs. My gratitude also goes to Kaj-Roger Hurme in the Isotope Laboratory of the Faculty of Agriculture and Forestry for all things related to radioac- tive work. I thank Lieven Sterck from VIB for Conium transcriptome assembly and Kean-Jin Lim from the Gerbera Laboratory for Trinity-assembly. I thank all the cur- rent and past members of the Plant Biotechnology and Metabolomics research group for assistance and friendship. Words cannot express all the gratitude I feel towards my family for what I have in my heart and my soul. Special thanks go to my parents, Anne and Risto Hotti, who 3 supported me throughout all these years and had the patience to listen to my reflec- tions on my research. I also thank my dear grandmother, Pirkko Hotti, my sister Heidi, brother-in-law Antti and niece Emilia Manninen. Finally, I thank my aunt Mar- jaana and uncle Paavo Pelkonen for inspiring me to reach my academic dream. In Helsinki September, 2016 Hannu Hotti 4 To Margaret F. Roberts and Edward E. Leete (1928-1992) for their work on coniine biosynthesis. Vinum poturus rex, memento te bibere sanguinem terra; cicuta hominum venenum est, cicuta vinum. When you are about to drink wine, o King, remember that you are about to drink the blood of earth. Hemlock is a poison to man, wine a poison to hemlock. -Pliny the Elder, 14.5 Quippe videre licet pinguescere saepe cicuta barbigeras pecudes, homini quae est acre venenum. Sooth, as one oft many see the bearded goats batten upon hemlock which to man is violent poison. -Lucretius, De rerum natura, 5.899-900. 5 Academic dissertation Supervisors Docent Heiko Rischer VTT Technical Research Centre of Finland Ltd Espoo, Finland Docent Kirsi-Marja Oksman-Caldentey VTT Technical Research Centre of Finland Ltd Espoo, Finland Professor Teemu Teeri Department of Agricultural Sciences University of Helsinki, Helsinki, Finland Reviewers Professor Riitta Julkunen-Tiitto Department of Biology University of Eastern Finland, Joensuu, Finland Professor Dr. Robert Verpoorte Institute of Biology Leiden University, Leiden, the Netherlands Opponent Professor Dr. Heribert Warzecha Department of Biology Technische Universität Darmstadt, Darmstadt, Germany Custos Professor Teemu Teeri Department of Agricultural Sciences University of Helsinki, Helsinki, Finland 6 List of publications This thesis is based on the following original publications, which are referred to in the text as Articles I–IV. The publications are reproduced with kind permission from the publishers. I Hotti, H., Seppänen-Laakso, T., Arvas, M., Teeri, T.H. & Rischer, H. 2015. Polyketide synthases from poison hemlock ( Conium maculatum L.). FEBS Journal 282, 4141-4156. doi: 10.1111/febs.13410. II Meier, P., Hotti, H. & Rischer, H. 2015. Elicitation of furanocoumarins in poison hemlock ( Conium maculatum L.) cell culture. Plant Cell, Tissue and Organ Culture 123(3), 443-453. doi: 10.1007/s11240-015-0847-7. III Hotti, H., Häkkinen, S.T., Seppänen-Laakso, T. & Rischer, H. 2016. Polyke- tides in Aloe plant and cell cultures. Manuscript. IV Hotti, H., Gopalacharyulu, P., Seppänen-Laakso, T. & Rischer, H. 2016. Metabolite profiling of the carnivorous pitcher plants Darlingtonia and Sar- racenia . Submitted to PLOSONE. Nota bene: The following results have not been published in the aforementioned articles: • Transcriptome sequencing of Conium maculatum • Testing of optimal pH for CPKS1 and CPKS5 7 Author’s contributions I. The author planned the work together with Heiko Rischer and Teemu Teeri. The author carried out the experimental work, except for the phylogenetic tree analysis and analysis of enzyme product structures. The author interpreted the data and had the main responsibility for writ- ing the publication under the supervision of Heiko Rischer and Teemu Teeri. II. The author planned the work together with Philipp Meier and Heiko Rischer. The author carried out the development of the tested cell line. The author co-authored the publication writing with Philipp Meier under the supervision of Heiko Rischer. III. The author planned the work together with Heiko Rischer and Suvi Häkkinen. The author carried out the experimental work, except for analysis of the structure of N-methylconiine. The author interpreted the data with Suvi Häkkinen and had the main responsibility for writing the publication under the supervision of Heiko Rischer. IV. The author planned the work together with Gopal Peddinti, Tuulikki Seppänen-Laakso, and Heiko Rischer. The author carried out the ex- perimental work. The author co-authored the publication,
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