Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla

Abstract Gentiana macrophylla is one of Chinese herbal medicines in which 4 kinds of iridoids or secoiridoids, such as loganic acid, sweroside, swertiamarin, and gentiopicroside, are identified as the dominant medicinal secondary metabolites. WRKY, as a large family of transcription factors (TFs), p...

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Main Authors: Yangyang Yin, Huanhuan Fu, Fakai Mi, Ye Yang, Yaomin Wang, Zhe Li, Yihan He, Zhenggang Yue
Format: Article
Language:English
Published: BMC 2024-01-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-024-04727-z
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author Yangyang Yin
Huanhuan Fu
Fakai Mi
Ye Yang
Yaomin Wang
Zhe Li
Yihan He
Zhenggang Yue
author_facet Yangyang Yin
Huanhuan Fu
Fakai Mi
Ye Yang
Yaomin Wang
Zhe Li
Yihan He
Zhenggang Yue
author_sort Yangyang Yin
collection DOAJ
description Abstract Gentiana macrophylla is one of Chinese herbal medicines in which 4 kinds of iridoids or secoiridoids, such as loganic acid, sweroside, swertiamarin, and gentiopicroside, are identified as the dominant medicinal secondary metabolites. WRKY, as a large family of transcription factors (TFs), plays an important role in the synthesis of secondary metabolites in plants. Therefore, WRKY genes involved in the biosynthesis of secoiridoids in G. macrophylla were systematically studied. First, a comprehensive genome-wide analysis was performed, and 42 GmWRKY genes were identified, which were unevenly distributed in 12 chromosomes. Accordingly, gene structure, collinearity, sequence alignment, phylogenetic, conserved motif and promoter analyses were performed, and the GmWRKY proteins were divided into three subfamilies based on phylogenetic and multiple sequence alignment analyses. Moreover, the enzyme-encoding genes of the secoiridoid biosynthesis pathway and their promoters were then analysed, and the contents of the four secoiridoids were determined in different tissues. Accordingly, correlation analysis was performed using Pearson′s correlation coefficient to construct WRKY gene-enzyme-encoding genes and WRKY gene–metabolite networks. Meanwhile, G. macrophylla seedlings were treated with methyl jasmonate (MeJA) to detect the dynamic change trend of GmWRKYs, biosynthetic genes, and medicinal ingredient accumulation. Thus, a total of 12 GmWRKYs were identified to be involved in the biosynthesis of secoiridoids, of which 8 (GmWRKY1, 6, 12, 17, 33, 34, 38 and 39) were found to regulate the synthesis of gentiopicroside, and 4 (GmWRKY7, 14, 26 and 41) were found to regulate the synthesis of loganic acid. Taken together, this study systematically identified WRKY transcription factors related to the biosynthesis of secoiridoids in G. macrophylla, which could be used as a cue for further investigation of WRKY gene functions in secondary metabolite accumulation.
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spelling doaj.art-5837cda0e03e4fd8aec3eda1f704525e2024-03-05T16:24:48ZengBMCBMC Plant Biology1471-22292024-01-0124112010.1186/s12870-024-04727-zGenomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophyllaYangyang Yin0Huanhuan Fu1Fakai Mi2Ye Yang3Yaomin Wang4Zhe Li5Yihan He6Zhenggang Yue7State Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineState Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineCollege of Life Science, Qinghai Normal UniversityState Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineState Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineState Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineState Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineState Key Laboratory of Research & Development of Characteristic Qin Medicine Resources (Cultivation), Coconstruction Collaborative Innovation Center for Chinese Medicinal Resources Industrialization By Shaanxi & Education Ministry, Shaanxi Innovative Drug Research Center, School of Pharmacy, Shaanxi University of Chinese MedicineAbstract Gentiana macrophylla is one of Chinese herbal medicines in which 4 kinds of iridoids or secoiridoids, such as loganic acid, sweroside, swertiamarin, and gentiopicroside, are identified as the dominant medicinal secondary metabolites. WRKY, as a large family of transcription factors (TFs), plays an important role in the synthesis of secondary metabolites in plants. Therefore, WRKY genes involved in the biosynthesis of secoiridoids in G. macrophylla were systematically studied. First, a comprehensive genome-wide analysis was performed, and 42 GmWRKY genes were identified, which were unevenly distributed in 12 chromosomes. Accordingly, gene structure, collinearity, sequence alignment, phylogenetic, conserved motif and promoter analyses were performed, and the GmWRKY proteins were divided into three subfamilies based on phylogenetic and multiple sequence alignment analyses. Moreover, the enzyme-encoding genes of the secoiridoid biosynthesis pathway and their promoters were then analysed, and the contents of the four secoiridoids were determined in different tissues. Accordingly, correlation analysis was performed using Pearson′s correlation coefficient to construct WRKY gene-enzyme-encoding genes and WRKY gene–metabolite networks. Meanwhile, G. macrophylla seedlings were treated with methyl jasmonate (MeJA) to detect the dynamic change trend of GmWRKYs, biosynthetic genes, and medicinal ingredient accumulation. Thus, a total of 12 GmWRKYs were identified to be involved in the biosynthesis of secoiridoids, of which 8 (GmWRKY1, 6, 12, 17, 33, 34, 38 and 39) were found to regulate the synthesis of gentiopicroside, and 4 (GmWRKY7, 14, 26 and 41) were found to regulate the synthesis of loganic acid. Taken together, this study systematically identified WRKY transcription factors related to the biosynthesis of secoiridoids in G. macrophylla, which could be used as a cue for further investigation of WRKY gene functions in secondary metabolite accumulation.https://doi.org/10.1186/s12870-024-04727-zGentiana macrophyllaWRKY transcription factorsSecoiridoid biosynthesisCorrelation analysisMethyl jasmonate treatment
spellingShingle Yangyang Yin
Huanhuan Fu
Fakai Mi
Ye Yang
Yaomin Wang
Zhe Li
Yihan He
Zhenggang Yue
Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla
BMC Plant Biology
Gentiana macrophylla
WRKY transcription factors
Secoiridoid biosynthesis
Correlation analysis
Methyl jasmonate treatment
title Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla
title_full Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla
title_fullStr Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla
title_full_unstemmed Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla
title_short Genomic characterization of WRKY transcription factors related to secoiridoid biosynthesis in Gentiana macrophylla
title_sort genomic characterization of wrky transcription factors related to secoiridoid biosynthesis in gentiana macrophylla
topic Gentiana macrophylla
WRKY transcription factors
Secoiridoid biosynthesis
Correlation analysis
Methyl jasmonate treatment
url https://doi.org/10.1186/s12870-024-04727-z
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