Free Access
Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers
Summary
Terpenoids emitted from snapdragon flowers include three monoterpenes derived from geranyl diphosphate (GPP), myrcene, (E)‐β‐ocimene and linalool, and a sesquiterpene, nerolidol, derived from farnesyl diphosphate (FPP). Using a functional genomics approach, we have isolated and biochemically characterized two nearly identical nerolidol/linalool synthases, AmNES/LIS‐1 and AmNES/LIS‐2, two enzymes responsible for the terpenoid profile of snapdragon scent remaining to be characterized. The AmNES/LIS‐2 protein has an additional 30 amino acids in the N‐terminus, and shares 95% amino acid sequence identity with AmNES/LIS‐1, with only 23 amino acid substitutions distributed across the homologous regions of the proteins. Although these two terpene synthases have very similar catalytic properties, and synthesize linalool and nerolidol as specific products from GPP and FPP, respectively, they are compartmentally segregated. GFP localization studies and analysis of enzyme activities in purified leucoplasts, together with our previous feeding experiments, revealed that AmNES/LIS‐1 is localized in cytosol, and is responsible for nerolidol biosynthesis, whereas AmNES/LIS‐2 is located in plastids, and accounts for linalool formation. Our results show that subcellular localization of bifunctional enzymes, in addition to the availability of substrate, controls the type of product formed. By directing nearly identical bifunctional enzymes to more than one cellular compartment, plants extend the range of available substrates for enzyme utilization, thus increasing the diversity of the metabolites produced.
Citing Literature
Number of times cited: 81
- Guo‐Feng Liu, Jing‐Jing Liu, Zhi‐Rong He, Fu‐Min Wang, Hua Yang, Yi‐Feng Yan, Ming‐Jun Gao, Margaret Y. Gruber, Xiao‐Chun Wan and Shu Wei, Implementation of CsLIS/NES in linalool biosynthesis involves transcript splicing regulation in , Plant, Cell & Environment, 41, 1, (176-186), (2017).
- Wei Liu, Zhiqiang Zhang, Wei Li, Wei Zhu, Zhongying Ren, Zhenyu Wang, Lingli Li, Lin Jia, Shuijin Zhu and Zongbin Ma, Genome-Wide Identification and Comparative Analysis of the 3-Hydroxy-3-methylglutaryl Coenzyme A Reductase (HMGR) Gene Family in Gossypium, Molecules, 23, 2, (193), (2018).
- Abith Vattekkatte, Stefan Garms, Wolfgang Brandt and Wilhelm Boland, Enhanced structural diversity in terpenoid biosynthesis: enzymes, substrates and cofactors, Organic & Biomolecular Chemistry, 16, 3, (348), (2018).
- Man Zhu, Jiajia Lin, Junli Ye, Rui Wang, Chao Yang, Jinli Gong, Yun Liu, Chongling Deng, Ping Liu, Chuanwu Chen, Yunjiang Cheng, Xiuxin Deng and Yunliu Zeng, A comprehensive proteomic analysis of elaioplasts from citrus fruits reveals insights into elaioplast biogenesis and function, Horticulture Research, 5, 1, (2018).
- Sean P. Gordon, Bruno Contreras-Moreira, Daniel P. Woods, David L. Des Marais, Diane Burgess, Shengqiang Shu, Christoph Stritt, Anne C. Roulin, Wendy Schackwitz, Ludmila Tyler, Joel Martin, Anna Lipzen, Niklas Dochy, Jeremy Phillips, Kerrie Barry, Koen Geuten, Hikmet Budak, Thomas E. Juenger, Richard Amasino, Ana L. Caicedo, David Goodstein, Patrick Davidson, Luis A. J. Mur, Melania Figueroa, Michael Freeling, Pilar Catalan and John P. Vogel, Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure, Nature Communications, 8, 1, (2017).
- T. X. Zhang, M. Sun, L. L. Li, Y. H. Guo, X. H. Xie and B. W. Hu, Molecular cloning and expression analysis of a monoterpene synthase gene involved in floral scent production in lily (Lilium ‘Siberia’), Russian Journal of Plant Physiology, 64, 4, (600), (2017).
- Seema Meena, Sarma Rajeev Kumar, Varun Dwivedi, Anup Kumar Singh, Chandan S. Chanotiya, Md. Qussen Akhtar, Krishna Kumar, Ajit Kumar Shasany and Dinesh A. Nagegowda, Transcriptomic insight into terpenoid and carbazole alkaloid biosynthesis, and functional characterization of two terpene synthases in curry tree (Murraya koenigii), Scientific Reports, 7, (44126), (2017).
- Anup Kumar Singh, Sarma Rajeev Kumar, Varun Dwivedi, Avanish Rai, Shaifali Pal, Ajit K. Shasany and Dinesh A. Nagegowda, A WRKY transcription factor from Withania somnifera regulates triterpenoid withanolide accumulation and biotic stress tolerance through modulation of phytosterol and defense pathways, New Phytologist, 215, 3, (1115-1131), (2017).
- Aisha Saleem Khan, Floral Essential Oils, Flowering Plants, (261-286), (2017).
- Guangkai Bian, Yichao Han, Anwei Hou, Yujie Yuan, Xinhua Liu, Zixin Deng and Tiangang Liu, Releasing the potential power of terpene synthases by a robust precursor supply platform, Metabolic Engineering, 42, (1), (2017).
- Ying Zhou, Lanting Zeng, Xiaoyu Liu, Jiadong Gui, Xin Mei, Xiumin Fu, Fang Dong, Jingchi Tang, Lingyun Zhang and Ziyin Yang, Formation of ( E )-nerolidol in tea ( Camellia sinensis ) leaves exposed to multiple stresses during tea manufacturing, Food Chemistry, 231, (78), (2017).
- Farhat Abbas, Yanguo Ke, Rangcai Yu, Yuechong Yue, Sikandar Amanullah, Muhammad Muzammil Jahangir and Yanping Fan, Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering, Planta, 246, 5, (803), (2017).
- Savitha Dhandapani, Jingjing Jin, Vishweshwaran Sridhar, Rajani Sarojam, Nam-Hai Chua and In-Cheol Jang, Integrated metabolome and transcriptome analysis of Magnolia champaca identifies biosynthetic pathways for floral volatile organic compounds, BMC Genomics, 10.1186/s12864-017-3846-8, 18, 1, (2017).
- Mummadireddy Ramya, Oh Keun Kwon, Hye Ryun An, Pil Man Park, Yun Su Baek and Pue Hee Park, Floral scent: Regulation and role of MYB transcription factors, Phytochemistry Letters, 19, (114), (2017).
- William C. Plaxton, Leucoplast Isolation and Subfractionation, Isolation of Plant Organelles and Structures, 10.1007/978-1-4939-6533-5_6, (73-81), (2016).
- Xin Mei, Xiaoyu Liu, Ying Zhou, Xiaoqin Wang, Lanting Zeng, Xiumin Fu, Jianlong Li, Jinchi Tang, Fang Dong and Ziyin Yang, Formation and emission of linalool in tea ( Camellia sinensis ) leaves infested by tea green leafhopper ( Empoasca ( Matsumurasca ) onukii Matsuda), Food Chemistry, 237, (356), (2017).
- Leila Pazouki and Ülo Niinemets, Multi-Substrate Terpene Synthases: Their Occurrence and Physiological Significance, Frontiers in Plant Science, 7, (2016).
- Jose Guedes de Sena Filho, Maureen B. Quin, Daniel J. Spakowicz, Jeffrey J. Shaw, Kaury Kucera, Brian Dunican, Scott A. Strobel and Claudia Schmidt-Dannert, Genome of Diaporthe sp. provides insights into the potential inter-phylum transfer of a fungal sesquiterpenoid biosynthetic pathway, Fungal Biology, 10.1016/j.funbio.2016.04.001, 120, 8, (1050-1063), (2016).
- Chen Xu, Huogen Li, Xiulian Yang, Chunsun Gu, Hongna Mu, Yuanzheng Yue and Lianggui Wang, Cloning and Expression Analysis of MEP Pathway Enzyme-encoding Genes in Osmanthus fragrans, Genes, 7, 12, (78), (2016).
- Xiangling Zeng, Cai Liu, Riru Zheng, Xuan Cai, Jing Luo, Jingjing Zou and Caiyun Wang, Emission and Accumulation of Monoterpene and the Key Terpene Synthase (TPS) Associated with Monoterpene Biosynthesis in Osmanthus fragrans Lour, Frontiers in Plant Science, 6, (2016).
- Pulu Sun, Robert C. Schuurink, Jean-Claude Caissard, Philippe Hugueney and Sylvie Baudino, My Way: Noncanonical Biosynthesis Pathways for Plant Volatiles, Trends in Plant Science, 21, 10, (884), (2016).
- Weng-Keong Chan, Loh Tan, Kok-Gan Chan, Learn-Han Lee and Bey-Hing Goh, Nerolidol: A Sesquiterpene Alcohol with Multi-Faceted Pharmacological and Biological Activities, Molecules, 21, 12, (529), (2016).
- Rafia Rehman, Muhammad Asif Hanif, Zahid Mushtaq and Abdullah Mohammed Al-Sadi, Biosynthesis of essential oils in aromatic plants: A review, Food Reviews International, 10.1080/87559129.2015.1057841, 32, 2, (117-160), (2015).
- Weihua Wu, William Tran, Craig A. Taatjes, Jorge Alonso-Gutierrez, Taek Soon Lee, John M. Gladden and Björn Hamberger, Rapid Discovery and Functional Characterization of Terpene Synthases from Four Endophytic Xylariaceae, PLOS ONE, 11, 2, (e0146983), (2016).
- Paramita Bera, Jhansi Narmada Reddy Kotamreddy, Tanmoy Samanta, Saborni Maiti and Adinpunya Mitra, Inter-specific variation in headspace scent volatiles composition of four commercially cultivated jasmine flowers, Natural Product Research, 29, 14, (1328), (2015).
- Liping Xu and Fangyuan Yu, Corolla structure and fragrance components in Styrax tonkinensis, Trees, 29, 4, (1127), (2015).
- Krishna Kumar, Sarma Rajeev Kumar, Varun Dwivedi, Avanish Rai, Ashutosh K. Shukla, Karuna Shanker and Dinesh A. Nagegowda, Precursor feeding studies and molecular characterization of geraniol synthase establish the limiting role of geraniol in monoterpene indole alkaloid biosynthesis in Catharanthus roseus leaves, Plant Science, 239, (56), (2015).
- Yunzi Luo, Bing-Zhi Li, Duo Liu, Lu Zhang, Yan Chen, Bin Jia, Bo-Xuan Zeng, Huimin Zhao and Ying-Jin Yuan, Engineered biosynthesis of natural products in heterologous hosts, Chemical Society Reviews, 10.1039/C5CS00025D, 44, 15, (5265-5290), (2015).
- Lucian Copolovici and Ülo Niinemets, Temperature dependencies of Henry’s law constants for different plant sesquiterpenes, Chemosphere, 138, (751), (2015).
- Paul C. Chikezie, Chiedozie O. Ibegbulem and Ferdinand N. Mbagwu, Bioactive Principles from Medicinal Plants, Research Journal of Phytochemistry, 10.3923/rjphyto.2015.88.115, 9, 3, (88-115), (2015).
- Yuechong Yue, Rangcai Yu and Yanping Fan, Transcriptome profiling provides new insights into the formation of floral scent in Hedychium coronarium, BMC Genomics, 16, 1, (470), (2015).
- Joshua R. Widhalm, Rohit Jaini, John A. Morgan and Natalia Dudareva, Rethinking how volatiles are released from plant cells, Trends in Plant Science, 20, 9, (545), (2015).
- Yan-Liang Lin, Yi-Ru Lee, Wen-Ke Huang, Shang-Tzen Chang and Fang-Hua Chu, Characterization of S-(+)-linalool synthase from several provenances of Cinnamomum osmophloeum, Tree Genetics & Genomes, 10.1007/s11295-013-0665-1, 10, 1, (75-86), (2013).
- Yuechong Yue, Rangcai Yu and Yanping Fan, Characterization of two monoterpene synthases involved in floral scent formation in Hedychium coronarium, Planta, 240, 4, (745), (2014).
- Masato Tsuro and Satoshi Asada, Differential expression of limonene synthase gene affects production and composition of essential oils in leaf and floret of transgenic lavandin (Lavandula × intermedia Emeric ex Loisel.), Plant Biotechnology Reports, 8, 2, (193), (2014).
- Alberto González, Marlen Gutiérrez-Cutiño and Alejandra Moenne, Oligo-Carrageenan Kappa-Induced Reducing Redox Status and Increase in TRR/TRX Activities Promote Activation and Reprogramming of Terpenoid Metabolism in Eucalyptus Trees, Molecules, 19, 12, (7356), (2014).
- Xin-Yue Li, Shao-Yuan Zheng, Rang-Cai Yu and Yan-Ping Fan, Promoters of HcTPS1 and HcTPS2 Genes from Hedychium coronarium Direct Floral-Specific, Developmental-Regulated and Stress-Inducible Gene Expression in Transgenic Tobacco, Plant Molecular Biology Reporter, 32, 4, (864), (2014).
- Gerard Farré‐Armengol, Iolanda Filella, Joan Llusià, Ülo Niinemets and Josep Peñuelas, Changes in floral bouquets from compound‐specific responses to increasing temperatures, Global Change Biology, 20, 12, (3660-3669), (2014).
- Ying Cao, Shanglian Hu, Qilin Dai and Yongsheng Liu, Tomato terpene synthases TPS5 and TPS39 account for a monoterpene linalool production in tomato fruits, Biotechnology Letters, 36, 8, (1717), (2014).
- Nelson Kibinge, Shun Ikeda, Naoaki Ono, Md. Altaf-Ul-Amin and Shigehiko Kanaya, Integration of Residue Attributes for Sequence Diversity Characterization of Terpenoid Enzymes, BioMed Research International, 2014, (1), (2014).
- JOËLLE K. MUHLEMANN, ANTJE KLEMPIEN and NATALIA DUDAREVA, Floral volatiles: from biosynthesis to function, Plant, Cell & Environment, 37, 8, (1936-1949), (2014).
- Frédéric Jullien, Sandrine Moja, Aurélie Bony, Sylvain Legrand, Cécile Petit, Tarek Benabdelkader, Kévin Poirot, Sébastien Fiorucci, Yann Guitton, Florence Nicolè, Sylvie Baudino and Jean-Louis Magnard, Isolation and functional characterization of a τ-cadinol synthase, a new sesquiterpene synthase from Lavandula angustifolia, Plant Molecular Biology, 84, 1-2, (227), (2014).
- Takehiko Shimada, Tomoko Endo, Hiroshi Fujii, Ana Rodríguez, Leandro Peña and Mitsuo Omura, Characterization of three linalool synthase genes from Citrus unshiu Marc. and analysis of linalool-mediated resistance against Xanthomonas citri subsp. citri and Penicilium italicum in citrus leaves and fruits, Plant Science, 229, (154), (2014).
- Bao-Qing Zhu, Jian Cai, Zhi-Qun Wang, Xiao-Qing Xu, Chang-Qing Duan and Qiu-Hong Pan, Identification of a Plastid-Localized Bifunctional Nerolidol/Linalool Synthase in Relation to Linalool Biosynthesis in Young Grape Berries, International Journal of Molecular Sciences, 15, 12, (21992), (2014).
- Natalia Dudareva, Antje Klempien, Joëlle K. Muhlemann and Ian Kaplan, Biosynthesis, function and metabolic engineering of plant volatile organic compounds, New Phytologist, 198, 1, (16-32), (2013).
- Avanish Rai, Shachi S. Smita, Anup Kumar Singh, Karuna Shanker and Dinesh A. Nagegowda, Heteromeric and Homomeric Geranyl Diphosphate Synthases from Catharanthus roseus and Their Role in Monoterpene Indole Alkaloid Biosynthesis, Molecular Plant, 10.1093/mp/sst058, 6, 5, (1531-1549), (2013).
- Arti Rani, Puja Ravikumar, Manjunatha Damodara Reddy and Anil Kush, Molecular regulation of santalol biosynthesis in Santalum album L., Gene, 527, 2, (642), (2013).
- Iban Eduardo, Giorgiana Chietera, Raul Pirona, Igor Pacheco, Michela Troggio, Elisa Banchi, Daniele Bassi, Laura Rossini, Alberto Vecchietti and Carlo Pozzi, Genetic dissection of aroma volatile compounds from the essential oil of peach fruit: QTL analysis and identification of candidate genes using dense SNP maps, Tree Genetics & Genomes, 9, 1, (189), (2013).
- Shun Ikeda, Takashi Abe, Yukiko Nakamura, Nelson Kibinge, Aki Hirai Morita, Atsushi Nakatani, Naoaki Ono, Toshimichi Ikemura, Kensuke Nakamura, Md. Altaf-Ul-Amin and Shigehiko Kanaya, Systematization of the Protein Sequence Diversity in Enzymes Related to Secondary Metabolic Pathways in Plants, in the Context of Big Data Biology Inspired by the KNApSAcK Motorcycle Database, Plant and Cell Physiology, 10.1093/pcp/pct041, 54, 5, (711-727), (2013).
- Shubhra Rastogi, Ritesh Kumar, Chandan S. Chanotiya, Karuna Shanker, Madan M. Gupta, Dinesh A. Nagegowda and Ajit K. Shasany, 4-Coumarate: CoA Ligase Partitions Metabolites for Eugenol Biosynthesis, Plant and Cell Physiology, 54, 8, (1238), (2013).
- Andrew J. Simkin, Karel Miettinen, Patricia Claudel, Vincent Burlat, Grégory Guirimand, Vincent Courdavault, Nicolas Papon, Sophie Meyer, Stéphanie Godet, Benoit St-Pierre, Nathalie Giglioli-Guivarc’h, Marc J.C. Fischer, Johan Memelink and Marc Clastre, Characterization of the plastidial geraniol synthase from Madagascar periwinkle which initiates the monoterpenoid branch of the alkaloid pathway in internal phloem associated parenchyma, Phytochemistry, 85, (36), (2013).
- Alok K Gupta, Tariq A Akhtar, Alex Widmer, Eran Pichersky and Florian P Schiestl, Identification of white campion (Silene latifolia) guaiacol O-methyltransferase involved in the biosynthesis of veratrole, a key volatile for pollinator attraction, BMC Plant Biology, 12, 1, (158), (2012).
- Danilo Aros, Veronica Gonzalez, Rudolf K. Allemann, Carsten T. Müller, Carlo Rosati and Hilary J. Rogers, Volatile emissions of scented Alstroemeria genotypes are dominated by terpenes, and a myrcene synthase gene is highly expressed in scented Alstroemeria flowers, Journal of Experimental Botany, 63, 7, (2739), (2012).
- Sol A. Green, Xiuyin Chen and Adam J. Matich, In Planta Transient Expression Analysis of Monoterpene Synthases, Natural Product Biosynthesis by Microorganisms and Plants, Part A, 10.1016/B978-0-12-394290-6.00003-3, (43-61), (2012).
- Sol A. Green, Xiuyin Chen, Niels J. Nieuwenhuizen, Adam J. Matich, Mindy Y. Wang, Barry J. Bunn, Yar-Khing Yauk and Ross G. Atkinson, Identification, functional characterization, and regulation of the enzyme responsible for floral (E)-nerolidol biosynthesis in kiwifruit (Actinidia chinensis), Journal of Experimental Botany, 63, 5, (1951), (2012).
- Zerihun A. Demissie, Monica A. Cella, Lukman S. Sarker, Travis J. Thompson, Mark R. Rheault and Soheil S. Mahmoud, Cloning, functional characterization and genomic organization of 1,8-cineole synthases from Lavandula, Plant Molecular Biology, 79, 4-5, (393), (2012).
- Diane M. Martin, Angela Chiang, Steven T. Lund and Jörg Bohlmann, Biosynthesis of wine aroma: transcript profiles of hydroxymethylbutenyl diphosphate reductase, geranyl diphosphate synthase, and linalool/nerolidol synthase parallel monoterpenol glycoside accumulation in Gewürztraminer grapes, Planta, 236, 3, (919), (2012).
- Joëlle K. Muhlemann, Hiroshi Maeda, Ching-Yun Chang, Phillip San Miguel, Ivan Baxter, Bruce Cooper, M. Ann Perera, Basil J. Nikolau, Olga Vitek, John A. Morgan, Natalia Dudareva and Gustavo Bonaventure, Developmental Changes in the Metabolic Network of Snapdragon Flowers, PLoS ONE, 7, 7, (e40381), (2012).
- Lucian Copolovici, Astrid Kännaste, Leila Pazouki and Ülo Niinemets, Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments, Journal of Plant Physiology, 169, 7, (664), (2012).
- Feng Chen, Dorothea Tholl, Jörg Bohlmann and Eran Pichersky, The family of terpene synthases in plants: a mid‐size family of genes for specialized metabolism that is highly diversified throughout the kingdom, The Plant Journal, 66, 1, (212-229), (2011).
- Tsutomu Sato, Hiroko Hoshino, Satoru Yoshida, Mami Nakajima and Tsutomu Hoshino, Bifunctional Triterpene/Sesquarterpene Cyclase: Tetraprenyl-β-curcumene Cyclase Is Also Squalene Cyclase in Bacillus megaterium, Journal of the American Chemical Society, 10.1021/ja2060319, 133, 44, (17540-17543), (2011).
- Anke Fähnrich, Katrin Krause and Birgit Piechulla, Product Variability of the ‘Cineole Cassette’ Monoterpene Synthases of Related Nicotiana Species, Molecular Plant, 4, 6, (965), (2011).
- Zerihun A. Demissie, Lukman S. Sarker and Soheil S. Mahmoud, Cloning and functional characterization of β-phellandrene synthase from Lavandula angustifolia, Planta, 233, 4, (685), (2011).
- Ab. Rahim Mohd-Hairul, Parameswari Namasivayam, Janna Ong Abdullah and Gwendoline Ee Cheng Lian, Screening, isolation, and molecular characterization of putative fragrance-related transcripts from Vanda Mimi Palmer, Acta Physiologiae Plantarum, 33, 5, (1651), (2011).
- Chiaki Nakano, Hyo-Kyoung Kim and Yasuo Ohnishi, Identification and Characterization of the Linalool/Nerolidol Synthase from Streptomyces clavuligerus, ChemBioChem, 12, 16, (2403), (2011).
- Petra M. Bleeker, Eleni A. Spyropoulou, Paul J. Diergaarde, Hanne Volpin, Michiel T. J. De Both, Philipp Zerbe, Joerg Bohlmann, Vasiliki Falara, Yuki Matsuba, Eran Pichersky, Michel A. Haring and Robert C. Schuurink, RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes, Plant Molecular Biology, 77, 4-5, (323), (2011).
- Dorothea Tholl, Reza Sohrabi, Jung-Hyun Huh and Sungbeom Lee, The biochemistry of homoterpenes – Common constituents of floral and herbivore-induced plant volatile bouquets, Phytochemistry, 10.1016/j.phytochem.2011.01.019, 72, 13, (1635-1646), (2011).
- Norihiko Misawa, Pathway engineering for functional isoprenoids, Current Opinion in Biotechnology, 22, 5, (627), (2011).
- Yann Guitton, Florence Nicolè, Sandrine Moja, Nadine Valot, Sylvain Legrand, Frédéric Jullien and Laurent Legendre, Differential accumulation of volatile terpene and terpene synthase mRNAs during lavender (Lavandula angustifolia and L. x intermedia) inflorescence development, Physiologia Plantarum, 138, 2, (150-163), (2009).
- Dinesh A. Nagegowda, Plant volatile terpenoid metabolism: Biosynthetic genes, transcriptional regulation and subcellular compartmentation, FEBS Letters, 584, 14, (2965-2973), (2010).
- Joe Chappell and Robert M. Coates, Sesquiterpenes, Comprehensive Natural Products II, 10.1016/B978-008045382-8.00005-8, (609-641), (2010).
- Andras Keszei, Curt L. Brubaker, Richard Carter, Tobias Köllner, Jörg Degenhardt and William J. Foley, Functional and evolutionary relationships between terpene synthases from Australian Myrtaceae, Phytochemistry, 71, 8-9, (844), (2010).
- Dinesh A. Nagegowda, The small subunit of geranyl diphosphate synthase: a tool to improve aroma and flavour by metabolic engineering, Journal of Biosciences, 35, 2, (167), (2010).
- Xiuyin Chen, Yar-Khing Yauk, Niels J. Nieuwenhuizen, Adam J. Matich, Mindy Y. Wang, Ramon Lopez Perez, Ross G. Atkinson and Lesley L. Beuning, Characterisation of an (S)-linalool synthase from kiwifruit (Actinidia arguta) that catalyses the first committed step in the production of floral lilac compounds, Functional Plant Biology, 37, 3, (232), (2010).
- Ab. Rahim Mohd-Hairul, Parameswari Namasivayam, Gwendoline Ee Cheng Lian and Janna Ong Abdullah, Terpenoid, Benzenoid, and Phenylpropanoid Compounds in the Floral Scent of Vanda Mimi Palmer, Journal of Plant Biology, 53, 5, (358), (2010).
- Niels J. Nieuwenhuizen, Sol Green and Ross G. Atkinson, Floral sesquiterpenes and their synthesis in dioecious kiwifruit, Plant Signaling & Behavior, 5, 1, (61), (2010).
- Michael C. Long, Dinesh A. Nagegowda, Yasuhisa Kaminaga, Kwok Ki Ho, Christine M. Kish, Jennifer Schnepp, Debra Sherman, Henry Weiner, David Rhodes and Natalia Dudareva, Involvement of snapdragon benzaldehyde dehydrogenase in benzoic acid biosynthesis, The Plant Journal, 59, 2, (256-265), (2009).
- Jörg Degenhardt, Tobias G. Köllner and Jonathan Gershenzon, Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants, Phytochemistry, 70, 15-16, (1621), (2009).
- N. J. Nieuwenhuizen, M. Y. Wang, A. J. Matich, S. A. Green, X. Chen, Y.-K. Yauk, L. L. Beuning, D. A. Nagegowda, N. Dudareva and R. G. Atkinson, Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa), Journal of Experimental Botany, 60, 11, (3203), (2009).
- Linda M. Mascavage, Serge Jasmin, Philip E. Sonnet, Michael Wilson and David R. Dalton, Alkaloids, Ullmann's Encyclopedia of Industrial Chemistry, (2010).
- Yang Sun, Xinzheng Huang, Yuese Ning, Weixia Jing, Toby J. A. Bruce, Fangjun Qi, Qixia Xu, Kongming Wu, Yongjun Zhang and Yuyuan Guo, TPS46, a Rice Terpene Synthase Conferring Natural Resistance to Bird Cherry-Oat Aphid, Rhopalosiphum padi (Linnaeus), Frontiers in Plant Science, 10.3389/fpls.2017.00110, 08, (2017).
