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Metabolomics and Complementary Techniques to Investigate the Plant

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Metabolomics and Complementary Techniques to Investigate the Plant Natural Product Reports View Article Online REVIEW View Journal Metabolomics and complementary techniques to investigate the plant phytochemical cosmos† Cite this: DOI: 10.1039/d1np00014d Hiroshi Tsugawa, *abcd Amit Rai, ae Kazuki Saito ae and Ryo Nakabayashi *a Covering: up to 2021 Plants and their associated microbial communities are known to produce millions of metabolites, a majority of which are still not characterized and are speculated to possess novel bioactive properties. In addition to their role in plant physiology, these metabolites are also relevant as existing and next-generation medicine candidates. Elucidation of the plant metabolite diversity is thus valuable for the successful exploitation of natural resources for humankind. Herein, we present a comprehensive review on recent metabolomics approaches to illuminate molecular networks in plants, including chemical isolation and enzymatic Creative Commons Attribution 3.0 Unported Licence. production as well as the modern metabolomics approaches such as stable isotope labeling, ultrahigh- resolution mass spectrometry, metabolome imaging (spatial metabolomics), single-cell analysis, cheminformatics, and computational mass spectrometry. Mass spectrometry-based strategies to characterize plant metabolomes through metabolite identification and annotation are described in detail. Received 3rd March 2021 We also highlight the use of phytochemical genomics to mine genes associated with specialized DOI: 10.1039/d1np00014d metabolites' biosynthesis. Understanding the metabolic diversity through biotechnological advances is rsc.li/npr fundamental to elucidate the functions of the plant-derived specialized metabolome. This article is licensed under a 1. Introduction 3. Cutting-edge technologies to identify unknown 2. Grand challenges in metabolomics: general approaches metabolites to natural product chemistry 3.1. Technological advances in biology, chemistry, and 2.1. Annotation in untargeted metabolomics instrumentation Open Access Article. Published on 20 August 2021. Downloaded 9/27/2021 2:08:22 AM. 2.2. Motivation to analyze authentic standards in untargeted 3.1.1. SIL-based metabolomics metabolomics 3.1.2. UHRMS-based metabolomics 2.3. Compound isolation from plants to identify novel 3.1.3. IMS metabolomics metabolites 3.1.4. Single cell metabolomics 2.4. Enzymatic approaches to obtain natural compounds of 3.2. Cheminformatics and CompMS interest 3.2.1. Generalist, well maintained, and widely used soware 2.5. Purposes of metabolite annotation in MSI level 2, 3, and programs in metabolomics 4 condences 3.2.2. Mass spectral databases for annotation 3.2.3. Fragment ion curations to accelerate the substructure annotations 3.2.4. Fragment feature-centric metabolite annotations aRIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, 3.2.5. Integrated CompMS and cheminformatics approach to Yokohama, Kanagawa 230-0045, Japan. E-mail: [email protected]; roy. metabolomics [email protected] 4. Phytochemical genomics in a supporting role to explore bRIKEN Center for Integrative Medical Sciences, 1-7-22 Suehiro-cho, Tsurumi-ku, the metabolite cosmos Yokohama, Kanagawa 230-0045, Japan cDepartment of Biotechnology and Life Science, Tokyo University of Agriculture and 4.1. Importance of genome mining for plant natural product Technology, 2-24-16 Nakamachi, Koganei, Tokyo 184-8588, Japan discovery dGraduate School of Medical Life Science, Yokohama City University, 1-7-22 Suehiro- 4.2. Near-isogenic lines (NILs), recombinant inbred lines cho, Tsurumi-ku, Yokohama 230-0045, Japan (RILs), and chromosome segment substitution lines ePlant Molecular Science Center, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba (CSSLs) for metabolome-assisted functional genomics 260-8675, Japan 4.3. Natural variants for metabolome-assisted functional † Electronic supplementary information (ESI) available. See DOI: genomics 10.1039/d1np00014d This journal is © The Royal Society of Chemistry 2021 Nat. Prod. Rep. View Article Online Natural Product Reports Review 4.4. Comparative genomics and phylogenetic approaches to 8. Conicts of interest elucidate the metabolites' diversity and role in speciation 9. Acknowledgements 4.5. Gene cluster analysis to link the genome architect with 10. Notes and references the metabolome 4.6. Machine learning and genomics to explore cellular 1. Introduction components involved in specialized metabolism 5. Prospects of metabolomics Plants are predominantly photosynthetic eukaryotes with over 5.1. Structure elucidation using other mass fragmentation 391 000 known species across the planet.1 One of the fasci- technologies nating characteristics of plants is their unique metabolic system 5.2. Spatial metabolomics with ion mobility (IM) spectrom- (metabolism), which produces highly complex and bioactive etry and toward spatial multi-omics molecules that modulate the cellular activity, microbiome, and 5.3. Plant kingdom-wide annotation phenotype in human health and diseases.2,3 Each plant species 5.4. Virtual platform-based annotation produces secondary (specialized) metabolites. According to 5.5. Articial intelligence for mass spectrometry data (AIMS) Afendi et al., the plant metabolite diversity exceeds 1 million, research with each plant producing nearly 4.7 structurally unique 6. Conclusion molecules;4 of these, only 300 000 structures have been cata- 7. Author contributions loged in the Dictionary of Natural Products (DNP). Moreover, Hiroshi Tsugawa got his PhD Kazuki Saito is a Professor from Osaka University in 2012, Emeritus at Chiba University Japan. His major is systems aer retiring as a professor of Creative Commons Attribution 3.0 Unported Licence. biology through computational the Graduate School of Phar- mass spectrometry (CompMS) to maceutical Sciences. Since April deepen the understanding of 2020, he has been appointed as metabolisms in living organ- the Director of RIKEN Center for isms. Employing CompMS, he Sustainable Resource Science. could develop a data processing His research is focused on pipeline for complex MS data metabolomics, functional geno- and identify unknown metabo- mics, and biotechnology of This article is licensed under a lites using computational anal- plant-specialized metabolism. ysis of mass fragmentation. The He is also fond of music (classic awards he received are RIKEN BAIHO Award (2020), Top 40 Under and jazz), movies, history, and hiking. 40 of “The Analytical Science” (2018), and RIKEN Incentive Open Access Article. Published on 20 August 2021. Downloaded 9/27/2021 2:08:22 AM. Research Award (2016). Since 2021, he is working as an associate professor at the Department of Biotechnology and Life Science, Tokyo University of Agriculture and Technology. Amit Rai got his PhD in 2013 Ryo Nakabayashi received his from the National University of PhD from Chiba University in Singapore. He is currently 2009, Japan. His expertise is working as a Research Scientist natural product chemistry, at the Metabolomics research analytical chemistry, and group, CSRS, RIKEN, and as metabolomics. As a research a guest lecturer at Chiba scientist, he has joined the University. His research interest Metabolomics Research Group includes functional genomics for (Principal Investigator: Dr plant natural products using Kazuki Saito), RIKEN CSRS, and comparative genomics, metab- has developed metabolomics olomics, integrative multi- approaches using LC-MS/MS, omics, and systems biology MALDI-MS, FTICR-MS, and approach. He has been awarded the Young Scientist award at the IMS for identifying specialized metabolites and their functions in National University of Singapore (Nov. 2014), best research poster plants. He has received the RIKEN Incentive Award in 2017 and the at “The 4th International Conference on Plant Metabolism”, JSPCMB Award for Young Scientists in 2020. Dalian, China (2017), and the best original research by The Japanese Society of Pharmacognosy (2018). Nat. Prod. Rep. This journal is © The Royal Society of Chemistry 2021 View Article Online Review Natural Product Reports this diversity may be further expanded when human microbial and (4) availability of comprehensive metabolite MS/MS spec- metabolism is considered, where the structure of natural tral libraries (>850 000 unique molecular standards).19 More- products is modied in the microbiome.5 In fact, the modied over, the methodologies of obtaining the retention index using molecule oen has higher bioactivity than that of the original a series of fatty acid-derived chemicals, as used in gas chro- form. For instance, 40,7-dihydroxyisoavan (equol), catalyzed in matography (GC)-MS, facilitate systematic annotation in the microbiome from the plant metabolite 40,7-dihydroxyiso- reverse-phase and hydrophilic interaction chromatography.20,21 avone (daidzein), acts as a superior ligand for estrogen Furthermore, recent advances in ion mobility (IM) and related receptors.6 informatics tools provide robust and reliable annotation criteria As many metabolites in plants (phytochemicals) possess based on the collision cross-section (CCS) values of 12 million biologically active sites for mammalian proteins, nearly half of compounds,22 thus increasing the coverage of metabolic the commercially available drugs released during 1940–2014 proling by separating isobars in a dri tube.23,24 However, were of plant origin.7 According to the MarketsandMarkets despite the remarkable advances in MS techniques, databases, analysis,8 plant extracts as a commercial commodity in indus- and informatics
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