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Integrated Metabolome and Transcriptome Analysis of Magnolia

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Integrated Metabolome and Transcriptome Analysis of Magnolia Dhandapani et al. BMC Genomics (2017) 18:463 DOI 10.1186/s12864-017-3846-8 RESEARCH ARTICLE Open Access Integrated metabolome and transcriptome analysis of Magnolia champaca identifies biosynthetic pathways for floral volatile organic compounds Savitha Dhandapani1,2, Jingjing Jin1, Vishweshwaran Sridhar1, Rajani Sarojam1, Nam-Hai Chua3 and In-Cheol Jang1,2* Abstract Background: Magnolia champaca, commonly known as champak is a well-known tree due to its highly fragrant flowers. Champak floral scent is attributed to a complex mix of volatile organic compounds (VOCs). These aromatic flowers are widely used in flavors and fragrances industry. Despite its commercial importance, the VOC biosynthesis pathways in these flowers are largely unknown. Here, we combine metabolite and RNA sequencing (RNA-seq) analyses of fully opened champak flowers to discover the active VOC biosynthesis pathways as well as floral scent-related genes. Results: Volatile collection by headspace method and analysis by gas chromatography-mass spectrometry (GC-MS) identified a total of 43 VOCs from fully opened champak flowers, of which 46.9% were terpenoids, 38.9% were volatile esters and 5.2% belonged to phenylpropanoids/benzenoids. Sequencing and de novo assembly of champak flower transcriptome yielded 47,688 non-redundant unigenes. Transcriptome assembly was validated using standard polymerase chain reaction (PCR) based approach for randomly selected unigenes. The detailed profiles of VOCs led to the discovery of pathways and genes involved in floral scent biosynthesis from RNA-seq data. Analysis of expression levels of many floral-scent biosynthesis-related unigenes in flowers and leaves showed that most of them were expressed higher in flowers than in leaf tissues. Moreover, our metabolite-guided transcriptomics, in vitro and in vivo enzyme assays and transgenic studies identified (R)-linalool synthase that is essential for the production of major VOCs of champak flowers, (R)-linalool and linalool oxides. Conclusion: As our study is the first report on transcriptome analysis of Magnolia champaca, this transcriptome dataset that serves as an important public information for functional genomics will not only facilitate better understanding of ecological functions of champak floral VOCs, but also provide biotechnological targets for sustainable production of champak floral scent. Keywords: Magnolia champaca, Metabolome, Transcriptome, Floral volatile organic, Compounds, Biosynthetic pathways, Terpene synthase, Volatile esters, (R)-linalool * Correspondence: [email protected] 1Temasek Life Sciences Laboratory, 1 Research Link, National University of Singapore, Singapore 117604, Singapore 2Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Dhandapani et al. BMC Genomics (2017) 18:463 Page 2 of 18 Background esterification of the aldehydes, acids and alcohols formed Flowers emit a large group of volatile organic com- by the above-mentioned processes by a class of enzymes pounds (VOCs) that play crucial roles in interactions called alcohol acyl transferases (AAT) [12]. with other organisms. In general, floral VOCs are con- The initial substrate for the biosynthesis of phenylpro- sidered not only to serve to attract pollinators to ensure panoids and benzenoids is phenylalanine, which is successful reproduction, but also to act as defense agents provided by the shikimate pathway [13]. Production and against microbes and herbivores [1]. Most of floral emission of phenylpropanoids/benzenoids are highly VOCs that are synthesized on the petals of the flowers regulated both temporally and spatially [14]. Many fall into three classes of VOCs namely terpenoids, phenylpropanoids/benzenoids biosynthetic enzymes have phenylpropanoids/benzenoids and volatile esters [2]. been identified and functionally characterized [14, 15]. The quality and quantity of floral VOCs emitted deter- However, the regulatory mechanisms involved in their mine floral scents and are also vital in determining the production are relatively unknown as compared to economic value of flowering plants as well as its usage terpenoids biosynthesis. in the flavors and fragrances industry. Magnolia champaca, commonly known as champak is Terpenoids, the largest class of VOCs, are produced a tall evergreen aromatic tree of the Magnoliaceae fam- and emitted by a number of floral species such as ily. Since various tissues of champak have been reported snapdragon and ylang ylang [3, 4]. In plants, biosynthesis to possess a broad range of medicinal properties, they of terpenoids involves three steps: (1) production of C5 are traditionally used in the treatment of various dis- isoprenoid precursors isopentenyl diphosphate (IPP) and eases such as cephalalgia, ophthalmia, gout, rheumatism dimethylallyl diphosphate (DMAPP) by two compart- and microbial infections [16]. In addition, the tree has mentally separated pathways: the methylerythritol 4- commercial value for its strongly diffusive fragrant phosphate (MEP) pathway in plastids and the mevalo- flowers which are widely used in cosmetic industries for nate (MVA) pathway in the cytosol, (2) condensation of the production of perfumes and essential oils due to the IPP and DMAPP into geranyl diphosphate (GPP, C10), high amounts of VOCs [17]. The composition of cham- farnesyl diphosphate (FPP, C15), and geranylgeranyl pak essential oil has been investigated previously show- diphosphate (GGPP, C20), the precursors for the produc- ing that it varied widely due to various factors including tion of mono-, sesqui- and diterpenes, respectively and extraction method and flower maturity [18–20]. Al- (3) generation of diverse terpene structures by the final though the reported percentages of the compounds were cyclization and oxidation steps carried out by the different, champak flowers mainly produced linalool and terpene synthases (TPS) and cytochrome P450s linalool oxides, 2-phenyl ethanol, methyl anthranilate, (CYP450) [5]. A large number of TPSs involved in floral indole and methyl linoleate [18–20]. scent production have been characterized in a variety of Despite the overall popularity of the champak, to our plants [1]. knowledge very little DNA sequences are available on Volatile esters are also known to contribute to the GenBank for this species. The availability of DNA aroma of many fruits and flowers. For instance, volatile sequences may provide an opportunity to identify genes esters such as methyl hexanoate, ethyl hexanoate, methyl involved in biosynthesis of floral VOCs. Identifying and jasmonate and methyl tiglate contribute profoundly to investigating the regulatory mechanisms behind floral the total floral scent composition of many plant species VOCs biosynthesis is essential to understand their roles [2] whereas hexyl acetate, ethyl 2-methylbutanoate and in plants and to improve VOC production through methyl 3-methylvalerate have been reported to be key metabolic engineering. Here, we present the chemical flavor constituents of many fruits including apple [6] composition and the transcriptome data from fully and strawberry [7]. They can be derived from fatty acids opened champak flowers, which were comprehensive or from branched-chain and aromatic amino acids [8, 9]. enough to discover and analyze major secondary metab- Conversion of fatty acids to volatile esters occur via olite pathways associated with floral scent production. In three processes: α-oxidation, β-oxidation and lipoxygen- addition, we identified the genes encoding the first and ase (LOX) pathway [10]. On the other hand, the first the last enzymes of the MEP pathway, DXS and HDR step in the conversion of amino acids to volatile esters is along with the (R)-linalool synthase, which makes a deamination step catalyzed by aminotransferases substantial contribution to the fragrance of champak resulting in α-ketoacids. α-ketoacids can be converted essential oil. into (1) carboxylic acids via oxidative decarboxylation, (2) aldehydes via decarboxylation and (3) α-hydroxyacids Results via reduction by a multi-subunit complex of enzymes Chemical composition profile of champak flowers named as α-ketoacid dehydrogenase complex [11]. The A previous report on the floral VOCs of Michelia alba, last step in the formation of volatile esters is the one of the species in Magnoliaceae family, showed the Dhandapani et al. BMC Genomics (2017) 18:463 Page 3 of 18 characteristic M. alba fragrance to be intense from half The pleasant fragrance of flowers such as Wisteria, bloom flowers to fully opened flowers [19]. To investi- orchids and lilies is often due to the presence of a gate the VOCs profile of fully opened champak flowers particular volatile ester or a mixture of several volatile grown in Singapore, we analyzed the headspace volatiles esters [2]. We found volatile esters as the second major emitted
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