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Gene-Metabolite Network Analysis Revealed Tissue-Specific International Journal of Molecular Sciences Article Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in Mallotus japonicus Megha Rai 1,2,† , Amit Rai 1,2,3,† , Tetsuya Mori 3, Ryo Nakabayashi 3, Manami Yamamoto 1, Michimi Nakamura 1, Hideyuki Suzuki 4 , Kazuki Saito 1,2,3 and Mami Yamazaki 1,2,* 1 Graduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, Japan; [email protected] (M.R.); [email protected] (A.R.); [email protected] (M.Y.); [email protected] (M.N.); [email protected] (K.S.) 2 Plant Molecular Science Center, Chiba University, Chiba 260-8675, Japan 3 RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa 230-0045, Japan; [email protected] (T.M.); [email protected] (R.N.) 4 Department of Research and Development, Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; [email protected] * Correspondence: [email protected] † These authors contributed equally. Abstract: Mallotus japonicus is a valuable traditional medicinal plant in East Asia for applications as a gastrointestinal drug. However, the molecular components involved in the biosynthesis of bioactive metabolites have not yet been explored, primarily due to a lack of omics resources. In Citation: Rai, M.; Rai, A.; Mori, T.; this study, we established metabolome and transcriptome resources for M. japonicus to capture the Nakabayashi, R.; Yamamoto, M.; diverse metabolite constituents and active transcripts involved in its biosynthesis and regulation. A Nakamura, M.; Suzuki, H.; Saito, K.; combination of untargeted metabolite profiling with data-dependent metabolite fragmentation and Yamazaki, M. Gene-Metabolite metabolite annotation through manual curation and feature-based molecular networking established Network Analysis Revealed Tissue- an overall metabospace of M. japonicus represented by 2129 metabolite features. M. japonicus de Specific Accumulation of Therapeutic novo transcriptome assembly showed 96.9% transcriptome completeness, representing 226,250 active Metabolites in Mallotus japonicus. transcripts across seven tissues. We identified specialized metabolites biosynthesis in a tissue-specific Int. J. Mol. Sci. 2021, 22, 8835. manner, with a strong correlation between transcripts expression and metabolite accumulations in M. https://doi.org/10.3390/ijms22168835 japonicus. The correlation- and network-based integration of metabolome and transcriptome datasets identified candidate genes involved in the biosynthesis of key specialized metabolites of M. japonicus. Academic Editors: Raffaele Capasso, We further used phylogenetic analysis to identify 13 C-glycosyltransferases and 11 methyltrans- Rafael Cypriano Dutra and Elisabetta Caiazzo ferases coding candidate genes involved in the biosynthesis of medicinally important bergenin. This study provides comprehensive, high-quality multi-omics resources to further investigate biological Received: 19 July 2021 properties of specialized metabolites biosynthesis in M. japonicus. Accepted: 12 August 2021 Published: 17 August 2021 Keywords: Mallotus japonicus; medicinal plants; biosynthesis of specialized metabolites; bergenin; rutin; WCNA; integrative omics; glucosyltransferases; O-methyltransferases Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Mallotus japonicus, also known as “Akamegashiwa” in Japanese, is a well-known medicinal plant from the Euphorbiaceae family and is widely distributed in tropical and temperate parts of East Asia [1–4]. Different tissues of M. japonicus, such as leaves, root, Copyright: © 2021 by the authors. bark, and pericarp, have been shown to be effective in several ailments, including gastric Licensee MDPI, Basel, Switzerland. and duodenal ulcer, hyperacidity, irritable bowel syndrome, hemorrhoids, rheumatism, This article is an open access article diabetes, dermatitis, liver diseases, and neuralgia [1]. The bark of M. japonicus is still distributed under the terms and listed as a stomach tonic for improving appetite in the “17th revision of the Japanese conditions of the Creative Commons Pharmacopoeia”. Bark tissue has been traditionally used to treat stomach disorders and Attribution (CC BY) license (https:// gallstones, as a folk medicine for cancer, and as a crude drug for gastric and duodenal creativecommons.org/licenses/by/ ulcers [5]. 4.0/). Int. J. Mol. Sci. 2021, 22, 8835. https://doi.org/10.3390/ijms22168835 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 8835 2 of 24 The medicinal properties of a given plant are attributed to its metabolic constituents, which include bioactive metabolites, and are often accumulated in a tissue-specific manner. Currently, over 143 compounds have been isolated across different Mallotus species, includ- ing 99 compounds in M. japonicus. These compounds belong to different chemical families such as alkaloids, iridoids, flavonoids, polyphenols, cardenolides, phloroglucinol, tannins, and their derivatives [1,2]. The leaves of M. japonicus, which primarily contains rutin and isoprenoid derivatives, are used to treat boils and swellings [5]. Furthermore, the antiox- idative properties of M. japonicus leaves and their components have been evaluated, and this plant is used as a functional food for human health. Bergenin, a dihydroisocoumarin derivative, possesses anti-inflammatory, antitussive, and hypolipidemic activity; is known for its effectiveness in treating gastritis, gastric ulcer, constipation, and diarrhea [6–10]; and is specifically accumulated in the bark of M. japonicus [11]. Pharmaceuticals such as gas- trointestinal drugs have included M. japonicus as a key ingredient for over 45 years. Despite vast industrial and medicinal applications, including a potential source of new medicines, no comprehensive multi-omics studies have ever been reported for M. japonicus, thus resulting in the lack of genomics and metabolomics resources for this plant species [1,2]. The advancement of high-throughput-omics technologies has facilitated the genera- tion of a wealth of knowledge. The omics datasets for a given species are valuable. When analyzed individually, associations with other omics datasets and comparisons across species provide a holistic view of a biological species [12,13]. Untargeted metabolomics is a “discovery mode” process that gives insight into each metabolite, whether known or unknown, present in the biological entity under study [14]. Additionally, with the rapid development of sequencing technologies, RNA-seq based de novo transcriptome assembly has been established as a powerful tool to study non-model plant species with little or no genomic resources [12,13]. Transcriptome profiling provides an extensive overview of the metabolic pathways and their localization in planta. At the same time, the sequence- similarity approach, together with distinct statistical analyses, assists in the identification of candidate genes involved in the biosynthesis of important metabolites. When combined with phylogenomic, such approaches allow for the identification of potential enzymes involved in the biosynthesis of specialized metabolites. To establish a comprehensive metabolite repository and genomic resources for M. japonicus, we performed untargeted metabolite profiling and deep-sequencing using seven tissues, namely young leaf, mature leaf, young stem, mature stem, bark, central cylinder, and inflorescence (Figure1). Untargeted metabolomics helped us capture the differential accumulation pattern of several specialized metabolite classes present in M. japonicus. WCNA-based network analyses were performed using the expression data of assembled transcripts and intensities of MS2 validated metabolites to classify metabo- lites or genes with similar functionalities into distinct modules. Furthermore, a pairwise correlation between the transcript and metabolite modules was performed to identify gene-to-metabolite associations highlighting the potential candidate genes involved in the biosynthesis of specialized metabolites. Our study identified a distinct transcript module involved in the biosynthesis of rutin in M. japonicus. Furthermore, we performed a gene ontology enrichment analysis to understand the biological significance of the transcript modules having a high correlation with the metabolic modules, which showed the presence of functional modules specific for the type of metabolites accumulated. The metabolome and transcriptome data established in this study will help in understanding the biosynthesis and regulation of specialized metabolites in M. japonicus. Int. J. Mol. Sci. 2021, 22, 8835 3 of 24 Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 3 of 24 Figure 1. TissuesTissues of of MallotusMallotus japonicus japonicus usedused in in this this study study for for the the multi multi-omics-omics analysis analysis:: (a) (ya)oung young leaf leaf,, (b) (mb)ature mature leaf leaf,, (c) young stem, (d) mature stem, (e) bark, (f) central cylinder, and (g) inflorescence. The scale bar represents 1 cm. (c) young stem, (d) mature stem, (e) bark, (f) central cylinder, and (g) inflorescence. The scale bar represents 1 cm. 2. Results and Discussion 2. Results and Discussion 2.1. Mallotus japonicus MetabolomeMetabolome DatabaseDatabase RepresentsRepresents Diverse Diverse Range Range of of Specialized Specialized Metabolites Metabolites In order to achieve holistic insight into the phytochemical composition of M. japonicus, In order to
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