Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban

Centella asiatica (L.) Urban is a well-known medicinal plant which has multiple pharmacological properties. Notably, the leaves of C. asiatica contain large amounts of triterpenoid saponins. However, there have only been a few studies systematically elucidating the metabolic dynamics and transcripti...

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Main Authors: Lingyun Wan, Qiulan Huang, Cui Li, Haixia Yu, Guiyu Tan, Shugen Wei, Ahmed H. El-Sappah, Suren Sooranna, Kun Zhang, Limei Pan, Zhanjiang Zhang, Ming Lei
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1295186/full
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author Lingyun Wan
Lingyun Wan
Lingyun Wan
Qiulan Huang
Cui Li
Cui Li
Haixia Yu
Haixia Yu
Haixia Yu
Guiyu Tan
Guiyu Tan
Guiyu Tan
Shugen Wei
Shugen Wei
Shugen Wei
Ahmed H. El-Sappah
Ahmed H. El-Sappah
Suren Sooranna
Suren Sooranna
Kun Zhang
Kun Zhang
Kun Zhang
Limei Pan
Limei Pan
Limei Pan
Zhanjiang Zhang
Zhanjiang Zhang
Zhanjiang Zhang
Ming Lei
Ming Lei
author_facet Lingyun Wan
Lingyun Wan
Lingyun Wan
Qiulan Huang
Cui Li
Cui Li
Haixia Yu
Haixia Yu
Haixia Yu
Guiyu Tan
Guiyu Tan
Guiyu Tan
Shugen Wei
Shugen Wei
Shugen Wei
Ahmed H. El-Sappah
Ahmed H. El-Sappah
Suren Sooranna
Suren Sooranna
Kun Zhang
Kun Zhang
Kun Zhang
Limei Pan
Limei Pan
Limei Pan
Zhanjiang Zhang
Zhanjiang Zhang
Zhanjiang Zhang
Ming Lei
Ming Lei
author_sort Lingyun Wan
collection DOAJ
description Centella asiatica (L.) Urban is a well-known medicinal plant which has multiple pharmacological properties. Notably, the leaves of C. asiatica contain large amounts of triterpenoid saponins. However, there have only been a few studies systematically elucidating the metabolic dynamics and transcriptional differences regarding triterpenoid saponin biosynthesis during the leaf development stages of C. asiatica. Here, we performed a comprehensive analysis of the metabolome and transcriptome to reveal the dynamic patterns of triterpenoid saponin accumulation and identified the key candidate genes associated with their biosynthesis in C. asiatica leaves. In this study, we found that the key precursors in the synthesis of terpenoids, including DMAPP, IPP and β-amyrin, as well as 22 triterpenes and eight triterpenoid saponins were considered as differentially accumulated metabolites. The concentrations of DMAPP, IPP and β-amyrin showed significant increases during the entire stage of leaf development. The levels of 12 triterpenes decreased only during the later stages of leaf development, but five triterpenoid saponins rapidly accumulated at the early stages, and later decreased to a constant level. Furthermore, 48 genes involved in the MVA, MEP and 2, 3-oxidosqualene biosynthetic pathways were selected following gene annotation. Then, 17 CYP450s and 26 UGTs, which are respectively responsible for backbone modifications, were used for phylogenetic-tree construction and time-specific expression analysis. From these data, by integrating metabolomics and transcriptomics analyses, we identified CaHDR1 and CaIDI2 as the candidate genes associated with DMAPP and IPP synthesis, respectively, and CaβAS1 as the one regulating β-amyrin synthesis. Two genes from the CYP716 family were confirmed as CaCYP716A83 and CaCYP716C11. We also selected two UGT73 families as candidate genes, associated with glycosylation of the terpenoid backbone at C-3 in C. asiatica. These findings will pave the way for further research on the molecular mechanisms associated with triterpenoid saponin biosynthesis in C. asiatica.
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spelling doaj.art-1b1a4f1ba21e4accb572e4ad1274ad102024-01-12T04:30:33ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-01-011410.3389/fpls.2023.12951861295186Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) UrbanLingyun Wan0Lingyun Wan1Lingyun Wan2Qiulan Huang3Cui Li4Cui Li5Haixia Yu6Haixia Yu7Haixia Yu8Guiyu Tan9Guiyu Tan10Guiyu Tan11Shugen Wei12Shugen Wei13Shugen Wei14Ahmed H. El-Sappah15Ahmed H. El-Sappah16Suren Sooranna17Suren Sooranna18Kun Zhang19Kun Zhang20Kun Zhang21Limei Pan22Limei Pan23Limei Pan24Zhanjiang Zhang25Zhanjiang Zhang26Zhanjiang Zhang27Ming Lei28Ming Lei29Guangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaFaculty of Agriculture, Forestry and Food Engineering, Yibin University, Yibin, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaGuangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaGuangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaGuangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaFaculty of Agriculture, Forestry and Food Engineering, Yibin University, Yibin, ChinaGenetics Department, Faculty of Agriculture, Zagazig University, Zagazig, EgyptNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaDepartment of Metabolism, Digestion and Reproduction, Imperial College London, London, United KingdomGuangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaGuangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaGuangxi Key Laboratory for High-Quality Formation and Utilization of Dao-Di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Center for Traditional Chinese Medicine (TCM) Inheritance and Innovation, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaNational Engineering Research Center for the Development of Southwestern Endangered Medicinal Materials, Guangxi Botanical Garden of Medicinal Plants, Nanning, ChinaCentella asiatica (L.) Urban is a well-known medicinal plant which has multiple pharmacological properties. Notably, the leaves of C. asiatica contain large amounts of triterpenoid saponins. However, there have only been a few studies systematically elucidating the metabolic dynamics and transcriptional differences regarding triterpenoid saponin biosynthesis during the leaf development stages of C. asiatica. Here, we performed a comprehensive analysis of the metabolome and transcriptome to reveal the dynamic patterns of triterpenoid saponin accumulation and identified the key candidate genes associated with their biosynthesis in C. asiatica leaves. In this study, we found that the key precursors in the synthesis of terpenoids, including DMAPP, IPP and β-amyrin, as well as 22 triterpenes and eight triterpenoid saponins were considered as differentially accumulated metabolites. The concentrations of DMAPP, IPP and β-amyrin showed significant increases during the entire stage of leaf development. The levels of 12 triterpenes decreased only during the later stages of leaf development, but five triterpenoid saponins rapidly accumulated at the early stages, and later decreased to a constant level. Furthermore, 48 genes involved in the MVA, MEP and 2, 3-oxidosqualene biosynthetic pathways were selected following gene annotation. Then, 17 CYP450s and 26 UGTs, which are respectively responsible for backbone modifications, were used for phylogenetic-tree construction and time-specific expression analysis. From these data, by integrating metabolomics and transcriptomics analyses, we identified CaHDR1 and CaIDI2 as the candidate genes associated with DMAPP and IPP synthesis, respectively, and CaβAS1 as the one regulating β-amyrin synthesis. Two genes from the CYP716 family were confirmed as CaCYP716A83 and CaCYP716C11. We also selected two UGT73 families as candidate genes, associated with glycosylation of the terpenoid backbone at C-3 in C. asiatica. These findings will pave the way for further research on the molecular mechanisms associated with triterpenoid saponin biosynthesis in C. asiatica.https://www.frontiersin.org/articles/10.3389/fpls.2023.1295186/fullCentella asiaticatranscriptomemetabolometriterpenoid saponincandidate gene
spellingShingle Lingyun Wan
Lingyun Wan
Lingyun Wan
Qiulan Huang
Cui Li
Cui Li
Haixia Yu
Haixia Yu
Haixia Yu
Guiyu Tan
Guiyu Tan
Guiyu Tan
Shugen Wei
Shugen Wei
Shugen Wei
Ahmed H. El-Sappah
Ahmed H. El-Sappah
Suren Sooranna
Suren Sooranna
Kun Zhang
Kun Zhang
Kun Zhang
Limei Pan
Limei Pan
Limei Pan
Zhanjiang Zhang
Zhanjiang Zhang
Zhanjiang Zhang
Ming Lei
Ming Lei
Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban
Frontiers in Plant Science
Centella asiatica
transcriptome
metabolome
triterpenoid saponin
candidate gene
title Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban
title_full Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban
title_fullStr Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban
title_full_unstemmed Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban
title_short Integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of Centella asiatica (L.) Urban
title_sort integrated metabolome and transcriptome analysis identifies candidate genes involved in triterpenoid saponin biosynthesis in leaves of centella asiatica l urban
topic Centella asiatica
transcriptome
metabolome
triterpenoid saponin
candidate gene
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1295186/full
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