Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi

BackgroundNardostachys jatamansi, an extremely endangered valuable plant of the alpine Himalayas, can synthesize specific sesquiterpenoids with multiple effective therapies and is widely exploited for the preparation of drugs, cosmetics and even religious functions (e.g., well-known spikenard). Howe...

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Main Authors: Mingkang Feng, Chen Chen, Junzhang Qu-Bie, Axiang Qu-Bie, Xiaoming Bao, Qi Cui, Xinjia Yan, Ying Li, Yuan Liu, Shaoshan Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1041321/full
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author Mingkang Feng
Mingkang Feng
Mingkang Feng
Chen Chen
Chen Chen
Junzhang Qu-Bie
Junzhang Qu-Bie
Junzhang Qu-Bie
Axiang Qu-Bie
Axiang Qu-Bie
Axiang Qu-Bie
Xiaoming Bao
Qi Cui
Qi Cui
Qi Cui
Xinjia Yan
Xinjia Yan
Ying Li
Yuan Liu
Yuan Liu
Shaoshan Zhang
Shaoshan Zhang
author_facet Mingkang Feng
Mingkang Feng
Mingkang Feng
Chen Chen
Chen Chen
Junzhang Qu-Bie
Junzhang Qu-Bie
Junzhang Qu-Bie
Axiang Qu-Bie
Axiang Qu-Bie
Axiang Qu-Bie
Xiaoming Bao
Qi Cui
Qi Cui
Qi Cui
Xinjia Yan
Xinjia Yan
Ying Li
Yuan Liu
Yuan Liu
Shaoshan Zhang
Shaoshan Zhang
author_sort Mingkang Feng
collection DOAJ
description BackgroundNardostachys jatamansi, an extremely endangered valuable plant of the alpine Himalayas, can synthesize specific sesquiterpenoids with multiple effective therapies and is widely exploited for the preparation of drugs, cosmetics and even religious functions (e.g., well-known spikenard). However, how accumulation trend of the sesquiterpenoids in tissues and the molecular mechanisms underlying the production of the active ingredients are not well understood.MethodsThe single-molecule real-time (SMRT) and RNA-seq transcriptome sequencing were combined to analyse the roots, rhizomes, leaves, flowers and anthocaulus of N. jatamansi. The phytochemical analysis was performed by gas chromatography‒mass spectrometry (GC‒MS) and ultrahigh-performance liquid chromatography (UPLC).ResultsA high-quality full-length reference transcriptome with 26,503 unigenes was generated for the first time. For volatile components, a total of sixty-five compounds were successfully identified, including fifty sesquiterpenoids. Their accumulation levels in five tissues were significantly varied, and most of the sesquiterpenoids were mainly enriched in roots and rhizomes. In addition, five aromatic compounds were only detected in flowers, which may help the plant attract insects for pollination. For nonvolatile ingredients, nardosinone-type sesquiterpenoids (nardosinone, kanshone C, and isonardosinone) were detected almost exclusively in roots and rhizomes. The candidate genes associated with sesquiterpenoid biosynthesis were identified by transcriptome analysis. Consistently, it was found that most biosynthesis genes were abundantly expressed in the roots and rhizomes according to the functional enrichment and expression patterns results. There was a positive correlation between the expression profile of genes related to the biosynthesis and the accumulation level of sesquiterpenoids in tissues. Gene family function analysis identified 28 NjTPSs and 43 NjCYPs that may be involved in the biosynthesis of the corresponding sesquiterpenoids. Furthermore, gene family functional analysis and gene coexpression network analysis revealed 28 NjTPSs and 43 NjCYPs associated with nardosinone-type sesquiterpenoid biosynthesis.ConclusionOur research results reveal the framework of sesquiterpenoids accumulation and biosynthesis in plant tissues and provide valuable support for further studies to elucidate the molecular mechanisms of sesquiterpenoid regulation and accumulation in N. jatamansi and will also contribute to the comprehensive utilization of this alpine plant.
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spelling doaj.art-218c916986cb4953b6476872952166ea2022-12-22T02:45:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.10413211041321Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansiMingkang Feng0Mingkang Feng1Mingkang Feng2Chen Chen3Chen Chen4Junzhang Qu-Bie5Junzhang Qu-Bie6Junzhang Qu-Bie7Axiang Qu-Bie8Axiang Qu-Bie9Axiang Qu-Bie10Xiaoming Bao11Qi Cui12Qi Cui13Qi Cui14Xinjia Yan15Xinjia Yan16Ying Li17Yuan Liu18Yuan Liu19Shaoshan Zhang20Shaoshan Zhang21Tibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaCollege of Pharmacy, Southwest Minzu University, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaCollege of Pharmacy, Southwest Minzu University, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaCollege of Pharmacy, Southwest Minzu University, Chengdu, ChinaAnalysis and Application Center, Shimadzu (China) Co., Ltd, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaCollege of Pharmacy, Southwest Minzu University, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaCollege of Pharmacy, Southwest Minzu University, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaTibetan Plateau Ethnic Medicinal Resources Protection and Utilization Key Laboratory of National Ethnic Affairs Commission of the People's Republic of China, Southwest Minzu University, Chengdu, ChinaSichuan Provincial Qiang-Yi Medicinal Resources Protection and Utilization Technology and Engineering Laboratory, Southwest Minzu University, Chengdu, ChinaBackgroundNardostachys jatamansi, an extremely endangered valuable plant of the alpine Himalayas, can synthesize specific sesquiterpenoids with multiple effective therapies and is widely exploited for the preparation of drugs, cosmetics and even religious functions (e.g., well-known spikenard). However, how accumulation trend of the sesquiterpenoids in tissues and the molecular mechanisms underlying the production of the active ingredients are not well understood.MethodsThe single-molecule real-time (SMRT) and RNA-seq transcriptome sequencing were combined to analyse the roots, rhizomes, leaves, flowers and anthocaulus of N. jatamansi. The phytochemical analysis was performed by gas chromatography‒mass spectrometry (GC‒MS) and ultrahigh-performance liquid chromatography (UPLC).ResultsA high-quality full-length reference transcriptome with 26,503 unigenes was generated for the first time. For volatile components, a total of sixty-five compounds were successfully identified, including fifty sesquiterpenoids. Their accumulation levels in five tissues were significantly varied, and most of the sesquiterpenoids were mainly enriched in roots and rhizomes. In addition, five aromatic compounds were only detected in flowers, which may help the plant attract insects for pollination. For nonvolatile ingredients, nardosinone-type sesquiterpenoids (nardosinone, kanshone C, and isonardosinone) were detected almost exclusively in roots and rhizomes. The candidate genes associated with sesquiterpenoid biosynthesis were identified by transcriptome analysis. Consistently, it was found that most biosynthesis genes were abundantly expressed in the roots and rhizomes according to the functional enrichment and expression patterns results. There was a positive correlation between the expression profile of genes related to the biosynthesis and the accumulation level of sesquiterpenoids in tissues. Gene family function analysis identified 28 NjTPSs and 43 NjCYPs that may be involved in the biosynthesis of the corresponding sesquiterpenoids. Furthermore, gene family functional analysis and gene coexpression network analysis revealed 28 NjTPSs and 43 NjCYPs associated with nardosinone-type sesquiterpenoid biosynthesis.ConclusionOur research results reveal the framework of sesquiterpenoids accumulation and biosynthesis in plant tissues and provide valuable support for further studies to elucidate the molecular mechanisms of sesquiterpenoid regulation and accumulation in N. jatamansi and will also contribute to the comprehensive utilization of this alpine plant.https://www.frontiersin.org/articles/10.3389/fpls.2022.1041321/fullNardostachys jatamansisesquiterpenoidtranscriptome sequencingbiosynthesis and accumulationterpene synthasecytochrome P450
spellingShingle Mingkang Feng
Mingkang Feng
Mingkang Feng
Chen Chen
Chen Chen
Junzhang Qu-Bie
Junzhang Qu-Bie
Junzhang Qu-Bie
Axiang Qu-Bie
Axiang Qu-Bie
Axiang Qu-Bie
Xiaoming Bao
Qi Cui
Qi Cui
Qi Cui
Xinjia Yan
Xinjia Yan
Ying Li
Yuan Liu
Yuan Liu
Shaoshan Zhang
Shaoshan Zhang
Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi
Frontiers in Plant Science
Nardostachys jatamansi
sesquiterpenoid
transcriptome sequencing
biosynthesis and accumulation
terpene synthase
cytochrome P450
title Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi
title_full Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi
title_fullStr Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi
title_full_unstemmed Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi
title_short Metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in Nardostachys jatamansi
title_sort metabolome and transcriptome associated analysis of sesquiterpenoid metabolism in nardostachys jatamansi
topic Nardostachys jatamansi
sesquiterpenoid
transcriptome sequencing
biosynthesis and accumulation
terpene synthase
cytochrome P450
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1041321/full
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