Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong

Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong (N. scrophulariiflora) is an important wild medicinal plant that belongs to the Plantaginaceae family. Its main active ingredients, picroside I (P-I) and picroside II (P-II), possess anti-inflammatory, anticancer, and antibacterial properties. Due t...

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Main Authors: Ke Rao, Siyu Liu, Xiaohui Tang, Guofu Jia, Shaohua Yang, Chaoxiang Ren, Jin Pei
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1527477/full
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author Ke Rao
Ke Rao
Siyu Liu
Siyu Liu
Xiaohui Tang
Guofu Jia
Shaohua Yang
Chaoxiang Ren
Chaoxiang Ren
Jin Pei
Jin Pei
author_facet Ke Rao
Ke Rao
Siyu Liu
Siyu Liu
Xiaohui Tang
Guofu Jia
Shaohua Yang
Chaoxiang Ren
Chaoxiang Ren
Jin Pei
Jin Pei
author_sort Ke Rao
collection DOAJ
description Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong (N. scrophulariiflora) is an important wild medicinal plant that belongs to the Plantaginaceae family. Its main active ingredients, picroside I (P-I) and picroside II (P-II), possess anti-inflammatory, anticancer, and antibacterial properties. Due to overharvesting, N. scrophulariiflora resources are facing the risk of depletion, urgently requiring resource protection and rational utilization. However, the biosynthetic pathways and related genes of active compounds in N. scrophulariiflora have not been fully investigated. In this study, widely targeted metabolomics and RNA-seq technology were employed to perform a joint analysis of the metabolome and transcriptome in different tissues of N. scrophulariiflora, including the roots, stems, and leaves. A total of 196 flavonoids and 63 terpenoids were identified. Among the 158,254 annotated genes, 74 were annotated as related to iridoid synthesis. Using bioinformatics methods such as clustering analysis, phylogenetic tree construction, and weighted gene co-expression network analysis (WGCNA), 43 candidate genes were identified that may be involved in the biosynthesis of picroside-I and picroside-II, of which 26 genes were significantly correlated with the synthesis of picrosides and their intermediates. Transcriptome analysis revealed the expression patterns of differentially expressed genes, and metabolomic analysis revealed the distribution characteristics of metabolites in different tissues of N. scrophulariiflora. Through qRT-PCR validation, we found that three NsF3H/NsF3D genes, four NsUGD/NsUPD genes, one Ns2HFD gene, and three NsSQM genes may participate in the iridoid biosynthesis pathway. These findings provide important genetic and metabolomic information for an in-depth understanding of the biosynthetic mechanisms of iridoids and lay the foundation for the protection and sustainable utilization of N. scrophulariiflora.
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spelling doaj-art-ab9bdf86b473470d91db25e06b2e70932025-02-03T06:33:43ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-02-011610.3389/fpls.2025.15274771527477Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.HongKe Rao0Ke Rao1Siyu Liu2Siyu Liu3Xiaohui Tang4Guofu Jia5Shaohua Yang6Chaoxiang Ren7Chaoxiang Ren8Jin Pei9Jin Pei10State Key Laboratory of Southwestern Chinese Medicine Resources, Chengdu, Sichuan, ChinaCollege of Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, ChinaState Key Laboratory of Southwestern Chinese Medicine Resources, Chengdu, Sichuan, ChinaCollege of Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, ChinaSichuan Academy of Grassland Sciences, Chengdu, ChinaSichuan Academy of Grassland Sciences, Chengdu, ChinaYunnan Provincial Academy of Agricultural Sciences of Alpine Economic Plant Research Institute, Yunnan, ChinaState Key Laboratory of Southwestern Chinese Medicine Resources, Chengdu, Sichuan, ChinaCollege of Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, ChinaState Key Laboratory of Southwestern Chinese Medicine Resources, Chengdu, Sichuan, ChinaCollege of Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, ChinaNeopicrorhiza scrophulariiflora (Pennell) D.Y.Hong (N. scrophulariiflora) is an important wild medicinal plant that belongs to the Plantaginaceae family. Its main active ingredients, picroside I (P-I) and picroside II (P-II), possess anti-inflammatory, anticancer, and antibacterial properties. Due to overharvesting, N. scrophulariiflora resources are facing the risk of depletion, urgently requiring resource protection and rational utilization. However, the biosynthetic pathways and related genes of active compounds in N. scrophulariiflora have not been fully investigated. In this study, widely targeted metabolomics and RNA-seq technology were employed to perform a joint analysis of the metabolome and transcriptome in different tissues of N. scrophulariiflora, including the roots, stems, and leaves. A total of 196 flavonoids and 63 terpenoids were identified. Among the 158,254 annotated genes, 74 were annotated as related to iridoid synthesis. Using bioinformatics methods such as clustering analysis, phylogenetic tree construction, and weighted gene co-expression network analysis (WGCNA), 43 candidate genes were identified that may be involved in the biosynthesis of picroside-I and picroside-II, of which 26 genes were significantly correlated with the synthesis of picrosides and their intermediates. Transcriptome analysis revealed the expression patterns of differentially expressed genes, and metabolomic analysis revealed the distribution characteristics of metabolites in different tissues of N. scrophulariiflora. Through qRT-PCR validation, we found that three NsF3H/NsF3D genes, four NsUGD/NsUPD genes, one Ns2HFD gene, and three NsSQM genes may participate in the iridoid biosynthesis pathway. These findings provide important genetic and metabolomic information for an in-depth understanding of the biosynthetic mechanisms of iridoids and lay the foundation for the protection and sustainable utilization of N. scrophulariiflora.https://www.frontiersin.org/articles/10.3389/fpls.2025.1527477/fullN. scrophulariiflorapicroside-Itranscriptomemetabolitesbiosynthetic pathway
spellingShingle Ke Rao
Ke Rao
Siyu Liu
Siyu Liu
Xiaohui Tang
Guofu Jia
Shaohua Yang
Chaoxiang Ren
Chaoxiang Ren
Jin Pei
Jin Pei
Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong
Frontiers in Plant Science
N. scrophulariiflora
picroside-I
transcriptome
metabolites
biosynthetic pathway
title Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong
title_full Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong
title_fullStr Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong
title_full_unstemmed Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong
title_short Integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in Neopicrorhiza scrophulariiflora (Pennell) D.Y.Hong
title_sort integrative analysis of metabolite and transcriptome reveals the biosynthetic pathway and candidate genes for iridoid glycoside biosynthesis in neopicrorhiza scrophulariiflora pennell d y hong
topic N. scrophulariiflora
picroside-I
transcriptome
metabolites
biosynthetic pathway
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1527477/full
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