Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia

Nepeta tenuifolia is a medicinal plant rich in terpenoids and flavonoids with antiviral, immunoregulatory, and anti-inflammatory activities. The peltate glandular trichome (PGT) is a multicellular structure considered to be the primary storage organ for monoterpenes; it may serve as an ideal model f...

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Main Authors: Peina Zhou, Jingjie Dang, Zunrui Shi, Yongfang Shao, Mengru Sang, Shilin Dai, Wei Yue, Chanchan Liu, Qinan Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.936244/full
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author Peina Zhou
Peina Zhou
Jingjie Dang
Jingjie Dang
Zunrui Shi
Zunrui Shi
Yongfang Shao
Yongfang Shao
Mengru Sang
Mengru Sang
Shilin Dai
Shilin Dai
Wei Yue
Wei Yue
Chanchan Liu
Chanchan Liu
Chanchan Liu
Qinan Wu
Qinan Wu
Qinan Wu
author_facet Peina Zhou
Peina Zhou
Jingjie Dang
Jingjie Dang
Zunrui Shi
Zunrui Shi
Yongfang Shao
Yongfang Shao
Mengru Sang
Mengru Sang
Shilin Dai
Shilin Dai
Wei Yue
Wei Yue
Chanchan Liu
Chanchan Liu
Chanchan Liu
Qinan Wu
Qinan Wu
Qinan Wu
author_sort Peina Zhou
collection DOAJ
description Nepeta tenuifolia is a medicinal plant rich in terpenoids and flavonoids with antiviral, immunoregulatory, and anti-inflammatory activities. The peltate glandular trichome (PGT) is a multicellular structure considered to be the primary storage organ for monoterpenes; it may serve as an ideal model for studying cell differentiation and the development of glandular trichomes (GTs). The genes that regulate the development of GTs have not yet been well studied. In this study, we identified NtMIXTA1, a GT development-associated gene from the R2R3 MYB SBG9 family. NtMIXTA1 overexpression in tobacco resulted in the production of longer and denser GTs. Virus-induced gene silencing of NtMIXTA1 resulted in lower PGT density, a significant reduction in monoterpene concentration, and the decreased expression of genes related to monoterpene biosynthesis. Comparative transcriptome and widely targeted metabolic analyses revealed that silencing NtMIXTA1 significantly influenced the expression of genes, and the production of metabolites involved in the biosynthesis of terpenoids, flavonoids, and lipids. This study provides a solid foundation describing a mechanism underlying the regulation of GT development. In addition, this study further deepens our understanding of the regulatory networks involved in GT development and GT development-associated metabolite flux, as well as provides valuable reference data for studying plants with a high medicinal value without genetic transformation.
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spelling doaj.art-dd4573c094fe47cc896a784afa48daa02022-12-22T03:40:16ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-07-011310.3389/fpls.2022.936244936244Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifoliaPeina Zhou0Peina Zhou1Jingjie Dang2Jingjie Dang3Zunrui Shi4Zunrui Shi5Yongfang Shao6Yongfang Shao7Mengru Sang8Mengru Sang9Shilin Dai10Shilin Dai11Wei Yue12Wei Yue13Chanchan Liu14Chanchan Liu15Chanchan Liu16Qinan Wu17Qinan Wu18Qinan Wu19College of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaNational and Local Collaborative Engineering Center of Chinese Medicinal Resources Industrialization and Formulae Innovative Medicine, Nanjing, ChinaCollege of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center of Chinese Medicinal Resources Industrialization, Nanjing, ChinaNational and Local Collaborative Engineering Center of Chinese Medicinal Resources Industrialization and Formulae Innovative Medicine, Nanjing, ChinaNepeta tenuifolia is a medicinal plant rich in terpenoids and flavonoids with antiviral, immunoregulatory, and anti-inflammatory activities. The peltate glandular trichome (PGT) is a multicellular structure considered to be the primary storage organ for monoterpenes; it may serve as an ideal model for studying cell differentiation and the development of glandular trichomes (GTs). The genes that regulate the development of GTs have not yet been well studied. In this study, we identified NtMIXTA1, a GT development-associated gene from the R2R3 MYB SBG9 family. NtMIXTA1 overexpression in tobacco resulted in the production of longer and denser GTs. Virus-induced gene silencing of NtMIXTA1 resulted in lower PGT density, a significant reduction in monoterpene concentration, and the decreased expression of genes related to monoterpene biosynthesis. Comparative transcriptome and widely targeted metabolic analyses revealed that silencing NtMIXTA1 significantly influenced the expression of genes, and the production of metabolites involved in the biosynthesis of terpenoids, flavonoids, and lipids. This study provides a solid foundation describing a mechanism underlying the regulation of GT development. In addition, this study further deepens our understanding of the regulatory networks involved in GT development and GT development-associated metabolite flux, as well as provides valuable reference data for studying plants with a high medicinal value without genetic transformation.https://www.frontiersin.org/articles/10.3389/fpls.2022.936244/fullglandular trichome developmentNepeta tenuifoliaVIGStranscriptomic (RNA-seq)metabolome
spellingShingle Peina Zhou
Peina Zhou
Jingjie Dang
Jingjie Dang
Zunrui Shi
Zunrui Shi
Yongfang Shao
Yongfang Shao
Mengru Sang
Mengru Sang
Shilin Dai
Shilin Dai
Wei Yue
Wei Yue
Chanchan Liu
Chanchan Liu
Chanchan Liu
Qinan Wu
Qinan Wu
Qinan Wu
Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia
Frontiers in Plant Science
glandular trichome development
Nepeta tenuifolia
VIGS
transcriptomic (RNA-seq)
metabolome
title Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia
title_full Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia
title_fullStr Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia
title_full_unstemmed Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia
title_short Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia
title_sort identification and characterization of a novel gene involved in glandular trichome development in nepeta tenuifolia
topic glandular trichome development
Nepeta tenuifolia
VIGS
transcriptomic (RNA-seq)
metabolome
url https://www.frontiersin.org/articles/10.3389/fpls.2022.936244/full
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