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University of Groningen Studies on Anthriscus Sylvestris L University of Groningen Studies on Anthriscus sylvestris L. (Hoffm.) Hendrawati, Oktavia IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2011 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Hendrawati, O. (2011). Studies on Anthriscus sylvestris L. (Hoffm.): metabolic engineering of combinatorial biosynthesis of podophyllotoxin. s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 02-10-2021 StudieS on Anthriscus sylvestris L. (Hoffm.) metabolic engineering of combinatorial biosynthesis of podophyllotoxin Oktavia Hendrawati This PhD project was carried out in the Department of Pharmaceutical Biology, Department of Molecular Biology of Plants and Department of Plant Physiology according to the requirements of the Graduate School of Science (Faculty of Mathematics and Natural Sciences, University of Groningen). This work was financially supported by Ubbo Emmius Fund of the University of Groningen, the Netherlands ISBN: 978-94-6182-027-3 Cover design: Hester Nijhoff, www.hesternijhoff.nl Layout and printing: Off Page, www.offpage.nl This thesis is also available in electronic format at: http://dissertations.ub.rug.nl/ Copyright © 2011 by O. Hendrawati. All rights reserved. No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, without prior permission of the author. RIJKSUNIVERSITEIT GRONINGEN StudieS on Anthriscus sylvestris L. (Hoffm.) metabolic engineering of combinatorial biosynthesis of podophyllotoxin Proefschrift ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr. E. Sterken, in het openbaar te verdedigen op vrijdag 28 oktober 2011 om 14.30 uur door oktavia Hendrawati geboren op 29 oktober 1977 te Surabaya, Indonesië Promotores: Prof. dr. O. Kayser Prof. dr. W.J. Quax Copromotor: Dr. H.J. Woerdenbag Beoordelingscommissie: Prof. dr. R. Verpoorte Prof. dr. J.T.M. Elzenga Prof. dr. E.M.J. Verpoorte The soul filled by love neither tires others nor grows tired Taize Didedikasikan untuk papa, mama, Januar Hendrawati, Yuniarto dan Aprilarto Hendronoto Tjandra Paranimfen: Melanie Foeh Christina Avanti ContentS Scope of the thesis 9 Chapter 1 Metabolic engineering strategies for the optimization of medicinal and aromatic plants: realities and expectations 11 Chapter 2 Seasonal variations in the deoxypodophyllotoxin content and yield of Anthriscus sylvestris L. (Hoffm.) grown in the field and under controlled conditions 45 Chapter 3 Identification of lignans and related compounds in Anthriscus sylvestris by LC-ESI-MS/MS and LC-SPE-NMR 63 Chapter 4 In vitro regeneration of wild chervil (Anthriscus sylvestris L.) 79 Chapter 5 Agrobacterium mediated transformation of Anthriscus sylvestris with human cytochrome P450 3A4 followed by regeneration 93 Summary 111 Samenvatting 113 Ringkasan 116 Acknowledgments 119 SCope of tHe tHeSiS Podophyllotoxin is a lignan, which is used as a precursor of the anticancer drugs etoposide and teniposide. Both drugs are important in the treatment of lung and testicular cancers, Ewing’s sarcoma, lymphoma, glioblastoma and non-lymphomatic leukaemia. Three different methods are known for the production of podophyllotoxin: isolation from Podophyllum and Linum species, production by plant cell cultures, and organic synthesis. To date, podophyllotoxin is commercially only obtained by extraction of the rhizome of Podophyllum species. The availability of Podophyllum species, however, is limited and the continuous demand of podophyllotoxin jeopardizes the natural sources. Podophyllum species are already listed on the endangered species list in India. Using plant cell cultures or organic synthesis for production purposes is not feasible, as the yields are limited and the price cannot compete with the collection of plants from wild habitats. In the near future, the availability of podophyllotoxin will become a major bottleneck in supplying pharmaceutical needs. An alternative source of podophyllotoxin may be obtained from the hydroxylation at the C-7 position of the closely related lignan deoyxpodophyllotoxin yielding (epi)podophyllotoxin, the diastereoisomer of podophyllotoxin. The Apiaceae species Anthriscus sylvestris L. (Hoffm.) is a wild plant generally occurring in northern Europe containing deoxypodophyllotoxin as its main lignan constituent. The aim of this thesis is to create and explore an alternative source of (epi) podophyllotoxin by production from deoxypodophyllotoxin. Current engineering strategies for the optimization of medicinal and aromatic plants are discussed in the introductory chapter 1. Deoxypodophyllotoxin is found in all parts of A. sylvestris at concentrations between 0.03 and 0.15% (dw). To get a clear picture of the deoxypodophyllotoxin content over the developmental stages of the plant, we studied the variations of deoxypodophyllotoxin during different developmental stages. The results are described in chapter 2. We followed one biannual life cycle of A. sylvestris collected from 13 different locations in Europe that were grown in the field and in a climate room. Based on the results, we could indicate the best harvesting time of the plant for deoxypodophyllotoxin isolation and for choosing a suitable candidate plant for on-going cultivation. In chapter 3, we identified 14 compounds in the root extract of A. sylvestris using combined method of LC-ESI-MS/MS and LC-SPE-NMR. Based on these results, we propose a hypothetical biosynthetic pathway of 6-hydroxy-aryltetralin lignans in A. sylvestris. A. sylvestris allows an interesting approach for genetic modification to directly produce (epi)podophyllotoxin in the plant. Human cytochrome P450 3A4 was cloned in A. sylvestris via Agrobacterium tumefaciens. For transformation purposes we first needed to establish a regeneration protocol for A. sylvestris. Different media and combinations of auxins and cytokinins were used for regeneration and the outcome is discussed in chapter 4. The transformation of A. sylvestris with human cytochrome P450 3A4 was achieved and discussed in chapter 5. The findings and the interpretation of the results of our study are highlighted in the summary. 9 Chapter Metabolic engineering strategies for the optimization of medicinal and aromatic plants: realities and expectations Oktavia Hendrawati Herman J. Woerdenbag Jacques Hille 1 Oliver Kayser Journal of Medicinal and Spice Plants 2010; 15(3): 111-126 1 Metabolic engineering strategies AbStrACt In recent years, strategies and techniques for the production of natural compounds (plant derived fine chemicals) and/ or the breeding of medicinal and aromatic plants has expanded. Efficient production of high value natural products with medicinal and cosmetic purpose (e.g. essential oils, paclitaxel, artemisinin, and vincristine) is the main target. Metabolic engineering and pathway optimization with the aim to reduce costs and increase productivity are the main focus of academia and industry. Until now, only a limited number of plant cell cultures and isolated enzymes gave sufficiently high production for commercial purposes. Therefore research strategies have been shifted to metabolic engineering. Engineering of microorganisms has proven to be a valuable tool and the concept has been transferred to plant science opening new promising perspectives. Engineering has been conducted for crop plants, but the application of this technique to medicinal plants has not yet been explored well so far. Nowadays the cloning and expression of multiple genes and genomic integration are of high interest. This allows the reconstitution of biosynthetic pathways in heterologous organisms, being either plants or microorganisms. Combining basic science and applied engineering in this research area has been named combinatorial biosynthesis and later as synthetic biology. Synthetic biology comprises a large number of subareas, including enzymology, protein assembly and interactions, metabolomics, gene regulation, signal transduction and computational biology and is considered as an important future approach for biotechnological plant optimization. Synthetic biology has exciting perspectives for the exploitation of medicinal and aromatic plants, in order to increase the level of desired natural products, to gain insight in metabolic pathways even for new similar chemicals, to improve nutritional and
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