Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>

<i>Mallotus japonicus</i> 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...

Full description

Bibliographic Details
Main Authors: Megha Rai, Amit Rai, Tetsuya Mori, Ryo Nakabayashi, Manami Yamamoto, Michimi Nakamura, Hideyuki Suzuki, Kazuki Saito, Mami Yamazaki
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/16/8835
_version_ 1797523583274057728
author Megha Rai
Amit Rai
Tetsuya Mori
Ryo Nakabayashi
Manami Yamamoto
Michimi Nakamura
Hideyuki Suzuki
Kazuki Saito
Mami Yamazaki
author_facet Megha Rai
Amit Rai
Tetsuya Mori
Ryo Nakabayashi
Manami Yamamoto
Michimi Nakamura
Hideyuki Suzuki
Kazuki Saito
Mami Yamazaki
author_sort Megha Rai
collection DOAJ
description <i>Mallotus japonicus</i> 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 this study, we established metabolome and transcriptome resources for <i>M. japonicus</i> to capture the diverse metabolite constituents and active transcripts involved in its biosynthesis and regulation. A combination of untargeted metabolite profiling with data-dependent metabolite fragmentation and metabolite annotation through manual curation and feature-based molecular networking established an overall metabospace of <i>M. japonicus</i> represented by 2129 metabolite features. <i>M. japonicus</i> de novo transcriptome assembly showed 96.9% transcriptome completeness, representing 226,250 active transcripts across seven tissues. We identified specialized metabolites biosynthesis in a tissue-specific manner, with a strong correlation between transcripts expression and metabolite accumulations in <i>M. japonicus</i>. The correlation- and network-based integration of metabolome and transcriptome datasets identified candidate genes involved in the biosynthesis of key specialized metabolites of <i>M. japonicus</i>. We further used phylogenetic analysis to identify 13 C-glycosyltransferases and 11 methyltransferases coding candidate genes involved in the biosynthesis of medicinally important bergenin. This study provides comprehensive, high-quality multi-omics resources to further investigate biological properties of specialized metabolites biosynthesis in <i>M. japonicus</i>.
first_indexed 2024-03-10T08:45:01Z
format Article
id doaj.art-a718b8749a0547b3868f481dc3568d0a
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-10T08:45:01Z
publishDate 2021-08-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-a718b8749a0547b3868f481dc3568d0a2023-11-22T08:01:19ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-08-012216883510.3390/ijms22168835Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>Megha Rai0Amit Rai1Tetsuya Mori2Ryo Nakabayashi3Manami Yamamoto4Michimi Nakamura5Hideyuki Suzuki6Kazuki Saito7Mami Yamazaki8Graduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, JapanGraduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, JapanRIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa 230-0045, JapanRIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa 230-0045, JapanGraduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, JapanGraduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, JapanDepartment of Research and Development, Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, JapanGraduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, JapanGraduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, Japan<i>Mallotus japonicus</i> 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 this study, we established metabolome and transcriptome resources for <i>M. japonicus</i> to capture the diverse metabolite constituents and active transcripts involved in its biosynthesis and regulation. A combination of untargeted metabolite profiling with data-dependent metabolite fragmentation and metabolite annotation through manual curation and feature-based molecular networking established an overall metabospace of <i>M. japonicus</i> represented by 2129 metabolite features. <i>M. japonicus</i> de novo transcriptome assembly showed 96.9% transcriptome completeness, representing 226,250 active transcripts across seven tissues. We identified specialized metabolites biosynthesis in a tissue-specific manner, with a strong correlation between transcripts expression and metabolite accumulations in <i>M. japonicus</i>. The correlation- and network-based integration of metabolome and transcriptome datasets identified candidate genes involved in the biosynthesis of key specialized metabolites of <i>M. japonicus</i>. We further used phylogenetic analysis to identify 13 C-glycosyltransferases and 11 methyltransferases coding candidate genes involved in the biosynthesis of medicinally important bergenin. This study provides comprehensive, high-quality multi-omics resources to further investigate biological properties of specialized metabolites biosynthesis in <i>M. japonicus</i>.https://www.mdpi.com/1422-0067/22/16/8835<i>Mallotus japonicus</i>medicinal plantsbiosynthesis of specialized metabolitesbergeninrutinWCNA
spellingShingle Megha Rai
Amit Rai
Tetsuya Mori
Ryo Nakabayashi
Manami Yamamoto
Michimi Nakamura
Hideyuki Suzuki
Kazuki Saito
Mami Yamazaki
Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>
International Journal of Molecular Sciences
<i>Mallotus japonicus</i>
medicinal plants
biosynthesis of specialized metabolites
bergenin
rutin
WCNA
title Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>
title_full Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>
title_fullStr Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>
title_full_unstemmed Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>
title_short Gene-Metabolite Network Analysis Revealed Tissue-Specific Accumulation of Therapeutic Metabolites in <i>Mallotus japonicus</i>
title_sort gene metabolite network analysis revealed tissue specific accumulation of therapeutic metabolites in i mallotus japonicus i
topic <i>Mallotus japonicus</i>
medicinal plants
biosynthesis of specialized metabolites
bergenin
rutin
WCNA
url https://www.mdpi.com/1422-0067/22/16/8835
work_keys_str_mv AT megharai genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT amitrai genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT tetsuyamori genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT ryonakabayashi genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT manamiyamamoto genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT michiminakamura genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT hideyukisuzuki genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT kazukisaito genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi
AT mamiyamazaki genemetabolitenetworkanalysisrevealedtissuespecificaccumulationoftherapeuticmetabolitesinimallotusjaponicusi