Effects of Overexpression of the Endogenous Farnesyl Diphosphate Synthase on the Artemisinin Content in Artemisia annua L.
Supported by the National Natural Science Foundation of China (30171142).
Abstract
Artemisinin is a novel effective antimalarial drug extracted from the medicinal plant Artemisia annua L. Owing to the tight market and low yield of artemisinin, there is great interest in enhancing the production of artemisinin. In the present study, farnesyl diphosphate synthase (FPS) was overexpressed in high‐yield A. annua to increase the artemisinin content. The FPS activity in transgenic A. annua was two‐ to threefold greater than that in non‐transgenic A. annua. The highest artemisinin content in transgenic A. annua was approximately 0.9% (dry weight), which was 34.4% higher than that in non‐transgenic A. annua. The results demonstrate the regulatory role of FPS in artemisinin biosynthesis.
(Managing editor: Wei Wang)
Citing Literature
Number of times cited: 56
- Yujun Zhao, Yifeng Zhang, Ping Su, Jian Yang, Luqi Huang and Wei Gao, Genetic Transformation System for Woody Plant Tripterygium wilfordii and Its Application to Product Natural Celastrol, Frontiers in Plant Science, 8, (2018).
- Kaipa H. Bindu, Jutti B. Mythili and Rohini M. Radhika, Genetic Engineering in Medicinal and Aromatic Plants, Genetic Engineering of Horticultural Crops, 10.1016/B978-0-12-810439-2.00012-X, (249-271), (2018).
- Dongming Ma, Gui Li, Fatima Alejos‐Gonzalez, Yue Zhu, Zhen Xue, Aimin Wang, Hui Zhang, Xing Li, Hechun Ye, Hong Wang, Benye Liu and De‐Yu Xie, Overexpression of a type‐I isopentenyl pyrophosphate isomerase of Artemisia annua in the cytosol leads to high arteannuin B production and artemisinin increase, The Plant Journal, 91, 3, (466-479), (2017).
- Subrata Kundu, Swapna Mukherjee and Biswajit Ghosh, Antimalarial Compound Synthesis from Transgenic Cultures, Transgenesis and Secondary Metabolism, 10.1007/978-3-319-28669-3_22, (123-152), (2017).
- Usha Kiran, Athar Ali, Kamaluddin and Malik Zainul Abdin, Metabolic Engineering of Secondary Plant Metabolism, Plant Biotechnology: Principles and Applications, 10.1007/978-981-10-2961-5_6, (173-190), (2017).
- Lu-yao Wang, Ying Zhang, Xue-qing Fu, Ting-ting Zhang, Jia-wei Ma, Li-da Zhang, Hong-mei Qian, Ke-xuan Tang, Shan Li and Jing-ya Zhao, Molecular cloning, characterization, and promoter analysis of the isochorismate synthase (AaICS1) gene from Artemisia annua青蒿异分支酸合酶基因的克隆及功能分析, Journal of Zhejiang University-SCIENCE B, 10.1631/jzus.B1600223, 18, 8, (662-673), (2017).
- Mohammad Ali, Bilal Haider Abbasi, Nisar Ahmad, Haji Khan and Gul Shad Ali, Strategies to enhance biologically active-secondary metabolites in cell cultures of Artemisia – current trends, Critical Reviews in Biotechnology, 37, 7, (833), (2017).
- Youyou Tu, Metabolic Engineering of Artemisia annua L., From Artemisia Annua L. to Artemisinins, 10.1016/B978-0-12-811655-5.00008-8, (163-208), (2017).
- Nur K. B. K. Ikram and Henrik T. Simonsen, A Review of Biotechnological Artemisinin Production in Plants, Frontiers in Plant Science, 8, (2017).
- Bushra Hafeez Kiani, John Suberu and Bushra Mirza, Cellular engineering of Artemisia annua and Artemisia dubia with the rol ABC genes for enhanced production of potent anti-malarial drug artemisinin, Malaria Journal, 15, 1, (2016).
- 路尧 王, Advances in Molecular Regulation of Artemisinin Biosynthesis, Botanical Research, 05, 03, (113), (2016).
- Suqin Guo, Yongliang Cui, Kunbi Wang, Wei Zhang, Guiyu Tan, Baomin Wang and Liwang Cui, Development of a Specific Monoclonal Antibody for the Quantification of Artemisinin in Artemisia annua and Rat Serum, Analytical Chemistry, 88, 5, (2701), (2016).
- Subrata Kundu, Swapna Mukherjee and Biswajit Ghosh, Antimalarial Compound Synthesis from Transgenic Cultures, Transgenesis and Secondary Metabolism, 10.1007/978-3-319-27490-4_22-1, (1-30), (2016).
- Weimin Jiang, Xueqing Fu, Qifang Pan, Yueli Tang, Qian Shen, Zongyou Lv, Tingxiang Yan, Pu Shi, Ling Li, Lida Zhang, Guofeng Wang, Xiaofen Sun and Kexuan Tang, Overexpression ofAaWRKY1Leads to an Enhanced Content of Artemisinin inArtemisia annua, BioMed Research International, 2016, (1), (2016).
- Yan Zhang, Zhi‐Xia Li, Xiu‐Dao Yu, Jia Fan, John A. Pickett, Huw D. Jones, Jing‐Jiang Zhou, Michael A. Birkett, John Caulfield, Johnathan A. Napier, Guang‐Yao Zhao, Xian‐Guo Cheng, Yi Shi, Toby J. A. Bruce and Lan‐Qin Xia, Molecular characterization of two isoforms of a farnesyl pyrophosphate synthase gene in wheat and their roles in sesquiterpene synthesis and inducible defence against aphid infestation, New Phytologist, 206, 3, (1101-1115), (2015).
- M. E. Poulson and T. Thai, Effect of high light intensity on photoinhibition, oxyradicals and artemisinin content in Artemisia annua L., Photosynthetica, 53, 3, (403), (2015).
- N. Kusaira B. K. Ikram, Xin Zhan, Xi-Wu Pan, Brian C. King and Henrik T. Simonsen, Stable heterologous expression of biologically active terpenoids in green plant cells, Frontiers in Plant Science, 6, (2015).
- Yu-Jun Zhao, Xin Chen, Meng Zhang, Ping Su, Yu-Jia Liu, Yu-Ru Tong, Xiu-Juan Wang, Lu-Qi Huang, Wei Gao and Timothy P Devarenne, Molecular Cloning and Characterisation of Farnesyl Pyrophosphate Synthase from Tripterygium wilfordii, PLOS ONE, 10, 5, (e0125415), (2015).
- Shirin Sultana, Hao Hu, Liping Gao, Jing Mao, Jing Luo, Maarten A. Jongsma and Caiyun Wang, Molecular cloning and characterization of the trichome specific chrysanthemyl diphosphate/chrysanthemol synthase promoter from Tanacetum cinerariifolium, Scientia Horticulturae, 185, (193), (2015).
- Malik Zainul Abdin and Pravej Alam, Genetic engineering of artemisinin biosynthesis: prospects to improve its production, Acta Physiologiae Plantarum, 10.1007/s11738-015-1771-5, 37, 2, (2015).
- Junli Han, Hongzhen Wang, Anneli Lundgren and Peter E. Brodelius, Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants, Phytochemistry, 102, (89), (2014).
- Naivy Pérez-Alonso, Borys Chong-Pérez, Alina Capote, Anabel Pérez, Yovanny Izquierdo, Geert Angenon and Elio Jiménez, Agrobacterium tumefaciens-mediated genetic transformation of Digitalis purpurea L., Plant Biotechnology Reports, 8, 5, (387), (2014).
- Yunpeng Ji, Jingwei Xiao, Yalin Shen, Dongming Ma, Zhenqiu Li, Gaobin Pu, Xing Li, Lili Huang, Benye Liu, Hechun Ye and Hong Wang, Cloning and Characterization of AabHLH1, a bHLH Transcription Factor that Positively Regulates Artemisinin Biosynthesis in Artemisia annua, Plant and Cell Physiology, 55, 9, (1592), (2014).
- Kexuan Tang, Qian Shen, Tingxiang Yan and Xueqing Fu, Transgenic approach to increase artemisinin content in Artemisia annua L., Plant Cell Reports, 33, 4, (605), (2014).
- B. Markus Lange and Amirhossein Ahkami, Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities, Plant Biotechnology Journal, 11, 2, (169-196), (2012).
- Arti Rani, Puja Ravikumar, Manjunatha Damodara Reddy and Anil Kush, Molecular regulation of santalol biosynthesis in Santalum album L., Gene, 527, 2, (642), (2013).
- Yunfei Chen, Qian Shen, Yueyue Wang, Tao Wang, Shaoyan Wu, Ling Zhang, Xu Lu, Fangyuan Zhang, Weimin Jiang, Bo Qiu, Erdi Gao, Xiaofen Sun and Kexuan Tang, The stacked over-expression of FPS, CYP71AV1 and CPR genes leads to the increase of artemisinin level in Artemisia annua L., Plant Biotechnology Reports, 7, 3, (287), (2013).
- Jong Moon Yoon, Le Zhao and Jacqueline V. Shanks, Metabolic Engineering with Plants for a Sustainable Biobased Economy, Annual Review of Chemical and Biomolecular Engineering, 10.1146/annurev-chembioeng-061312-103320, 4, 1, (211-237), (2013).
- Hongzhen Wang, Junli Han, Selvaraju Kanagarajan, Anneli Lundgren and Peter E. Brodelius, Trichome-specific expression of the amorpha-4,11-diene 12-hydroxylase (cyp71av1) gene, encoding a key enzyme of artemisinin biosynthesis in Artemisia annua, as reported by a promoter-GUS fusion, Plant Molecular Biology, 81, 1-2, (119), (2013).
- Alain Tissier, Glandular trichomes: what comes after expressed sequence tags?, The Plant Journal, 70, 1, (51-68), (2012).
- Oktavia Hendrawati, Herman J. Woerdenbag, Jacques Hille and Oliver Kayser, Metabolic Engineering of Medicinal Plants and Microorganisms for the Production of Natural Products, Pharmaceutical Biotechnology, (491-526), (2012).
- Q. Shen, Y.F. Chen, T. Wang, S.Y. Wu, X. Lu, L. Zhang, F.Y. Zhang, W.M. Jiang and G.F. Wang and K.X. Tang, Overexpression of the cytochrome P450 monooxygenase (cyp71av1) and cytochrome P450 reductase (cpr) genes increased artemisinin content in Artemisia annua (Asteraceae), Genetics and Molecular Research, 11, 3, (3298), (2012).
- Wenping Hua, Jie Song, Cuiqin Li and Zhezhi Wang, Molecular cloning and characterization of the promoter of SmGGPPs and its expression pattern in Salvia miltiorrhiza, Molecular Biology Reports, 39, 5, (5775), (2012).
- Benye Liu, Hong Wang, Zhigao Du, Guofeng Li and Hechun Ye, Metabolic engineering of artemisinin biosynthesis in Artemisia annua L., Plant Cell Reports, 30, 5, (689), (2011).
- Tazyeen Nafis, Mohd. Akmal, Mauji Ram, Pravej Alam, Seema Ahlawat, Anis Mohd and Malik Zainul Abdin, Enhancement of artemisinin content by constitutive expression of the HMG-CoA reductase gene in high-yielding strain of Artemisia annua L., Plant Biotechnology Reports, 5, 1, (53), (2011).
- Pravej Alam and M. Z. Abdin, Over-expression of HMG-CoA reductase and amorpha-4,11-diene synthase genes in Artemisia annua L. and its influence on artemisinin content, Plant Cell Reports, 30, 10, (1919), (2011).
- Xinkai Xie, Kangjian Qiao and Yi Tang, Metabolic Engineering of Natural Product Biosynthesis, Bioactive Compounds from Natural Sources, Second Edition, 10.1201/b11196-4, (65-96), (2012).
- Hongzhen Wang, Linda Olofsson, Anneli Lundgren and Peter E. Brodelius, Trichome-Specific Expression of Amorpha-4,11-Diene Synthase, a Key Enzyme of Artemisinin Biosynthesis in <i>Artemisia annua</i> L., as Reported by a Promoter-GUS Fusion, American Journal of Plant Sciences, 02, 04, (619), (2011).
- Caiyan Lei, Dongming Ma, Gaobin Pu, Xiaofang Qiu, Zhigao Du, Hong Wang, Guofeng Li, Hechun Ye and Benye Liu, Foliar application of chitosan activates artemisinin biosynthesis in Artemisia annua L., Industrial Crops and Products, 33, 1, (176), (2011).
- Linda Olofsson, Alexander Engström, Anneli Lundgren and Peter E Brodelius, Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L, BMC Plant Biology, 11, 1, (45), (2011).
- Khanhvan T. Nguyen, Patrick R. Arsenault and Pamela J. Weathers, Trichomes + roots + ROS = artemisinin: regulating artemisinin biosynthesis in Artemisia annua L., In Vitro Cellular & Developmental Biology - Plant, 47, 3, (329), (2011).
- Rafael Zárate, Plant Secondary Metabolism Engineering: Methods, Strategies, Advances, and Omics, Comprehensive Natural Products II, 10.1016/B978-008045382-8.00068-X, (629-668), (2010).
- Ying Li and Yu-Lin Wu, A golden phoenix arising from the herbal nest — A review and reflection on the study of antimalarial drug Qinghaosu, Frontiers of Chemistry in China, 10.1007/s11458-010-0214-5, 5, 4, (357-422), (2010).
- Huahong Wang, Chenfei Ma, Zhenqiu Li, Lanqing Ma, Hong Wang, Hechun Ye, Guowang Xu and Benye Liu, Effects of exogenous methyl jasmonate on artemisinin biosynthesis and secondary metabolites in Artemisia annua L., Industrial Crops and Products, 31, 2, (214), (2010).
- Lin Xiang, Kaige Zhao and Longqing Chen, Molecular cloning and expression of Chimonanthus praecox farnesyl pyrophosphate synthase gene and its possible involvement in the biosynthesis of floral volatile sesquiterpenoids, Plant Physiology and Biochemistry, 48, 10-11, (845), (2010).
- Waleerat Banyai, Chalermpol Kirdmanee, Masahiro Mii and Kanyaratt Supaibulwatana, Overexpression of farnesyl pyrophosphate synthase (FPS) gene affected artemisinin content and growth of Artemisia annua L., Plant Cell, Tissue and Organ Culture (PCTOC), 103, 2, (255), (2010).
- Su-Ping He, Gui-Yu Tan, Gang Li, Wei-Ming Tan, Tie-Gui Nan, Bao-Min Wang, Zhao-Hu Li and Qing X. Li, Development of a sensitive monoclonalantibody-based enzyme-linked immunosorbent assay for the antimalaria active ingredient artemisinin in the Chinese herb Artemisia annua L., Analytical and Bioanalytical Chemistry, 393, 4, (1297), (2009).
- Dongming Ma, Gaobin Pu, Caiyan Lei, Lanqing Ma, Huahong Wang, Yanwu Guo, Jianlin Chen, Zhigao Du, Hong Wang, Guofeng Li, Hechun Ye and Benye Liu, Isolation and Characterization of AaWRKY1, an Artemisia annua Transcription Factor that Regulates the Amorpha-4,11-diene Synthase Gene, a Key Gene of Artemisinin Biosynthesis, Plant and Cell Physiology, 50, 12, (2146), (2009).
- Chenfei Ma, Huahong Wang, Xin Lu, Hong Wang, Guowang Xu and Benye Liu, Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry, Metabolomics, 5, 4, (497), (2009).
- Kazuki Saito, Toshiya Muranaka, Hiroshi Sudo and Mareshige Kojoma, Medicinal Plants, Compendium of Transgenic Crop Plants, (141-156), (2009).
- Chenfei Ma, Huahong Wang, Xin Lu, Guowang Xu and Benye Liu, Metabolic fingerprinting investigation of Artemisia annua L. in different stages of development by gas chromatography and gas chromatography–mass spectrometry, Journal of Chromatography A, 1186, 1-2, (412), (2008).
- Rafael Zárate, Nabil El Jaber-Vazdekis, Elena Cequier-Sánchez, Fátima Gutierrez-Nicolás and Ángel G. Ravelo, Biotechnology for the production of plant natural products, Bioactive Natural Products (Part N), 10.1016/S1572-5995(08)80030-0, (309-392), (2008).
- Ying Li, Jing‐Lei Shuang, Wei‐Wei Yuan, Wu‐Yang Huang and Ren‐Xiang Tan, Verticase: a Fibrinolytic Enzyme Produced by Verticillium sp. Tj33, an Endophyte of Trachelospermum jasminoides, Journal of Integrative Plant Biology, 49, 11, (1548-1554), (2007).
- Sonia Gómez-Galera, Ana M. Pelacho, Anna Gené, Teresa Capell and Paul Christou, The genetic manipulation of medicinal and aromatic plants, Plant Cell Reports, 10.1007/s00299-007-0384-x, 26, 10, (1689-1715), (2007).
- Axel Schmidt and Jonathan Gershenzon, Cloning and characterization of isoprenyl diphosphate synthases with farnesyl diphosphate and geranylgeranyl diphosphate synthase activity from Norway spruce (Picea abies) and their relation to induced oleoresin formation, Phytochemistry, 68, 21, (2649), (2007).
- Braulio M. Fraga, Natural sesquiterpenoids, Natural Product Reports, 10.1039/b706427f, 24, 6, (1350), (2007).
