Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea

Tanshinones found in Salvia species are the main active compounds for the treatment of cardiovascular and cerebrovascular diseases, but their contents are hugely different in different species. For example, tanshinone IIA content in Salvia castanea Diels f. tomentosa Stib. is about 49 times higher t...

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Main Authors: Yue Chen, Yanting Wang, Juan Guo, Jian Yang, Xiaodan Zhang, Zixuan Wang, Ying Cheng, Zewei Du, Zhechen Qi, Yanbo Huang, Mans Dennis, Yukun Wei, Dongfeng Yang, Luqi Huang, Zongsuo Liang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.820582/full
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author Yue Chen
Yanting Wang
Juan Guo
Jian Yang
Xiaodan Zhang
Zixuan Wang
Ying Cheng
Zewei Du
Zhechen Qi
Yanbo Huang
Mans Dennis
Yukun Wei
Dongfeng Yang
Luqi Huang
Zongsuo Liang
author_facet Yue Chen
Yanting Wang
Juan Guo
Jian Yang
Xiaodan Zhang
Zixuan Wang
Ying Cheng
Zewei Du
Zhechen Qi
Yanbo Huang
Mans Dennis
Yukun Wei
Dongfeng Yang
Luqi Huang
Zongsuo Liang
author_sort Yue Chen
collection DOAJ
description Tanshinones found in Salvia species are the main active compounds for the treatment of cardiovascular and cerebrovascular diseases, but their contents are hugely different in different species. For example, tanshinone IIA content in Salvia castanea Diels f. tomentosa Stib. is about 49 times higher than that in Salvia miltiorrhiza Bunge. The molecular mechanism responsible for this phenomenon remains largely unknown. To address this, we performed comparative transcriptomic and proteomic analyses of S. miltiorrhiza and S. castanea. A total of 296 genes in S. castanea and 125 genes in S. miltiorrhiza were highly expressed at both the transcriptional and proteome levels, including hormone signal regulation, fungus response genes, transcription factors, and CYP450. Among these differentially expressed genes, the expression of SmWRKY61 was particularly high in S. castanea. Overexpression of SmWRKY61 in S. miltiorrhiza could significantly increase the content of tanshinone I and tanshinone IIA, which were 11.09 and 33.37 times of the control, respectively. Moreover, SmWRKY61 had a strong regulatory effect, elevating the expression levels of tanshinone pathway genes such as DXS2, CMK, HMGS2, 1, KSL1, KSL2, CYP76AH1, and CYP76AK3. For the WRKY family, 79 SmWRKYs were originally obtained and classified into three main groups. Collinearity analysis indicated a more specific extension of WRKY gene family in Salvia genus. In 55 Salvia species, only 37 species contained the WRKY61 sequence, and high SmWRKY61 expression in some Salvia L. species was often accompanied by high tanshinone accumulation. The above results suggest that SmWRKY61 is a highly effective regulator of tanshinone accumulation and may be a key factor resulting in high tanshinone accumulation in S. castanea.
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spelling doaj.art-ca0736eb3d864ccb8d1daf5c6915c64a2022-12-22T01:40:24ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-03-011210.3389/fpls.2021.820582820582Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castaneaYue Chen0Yanting Wang1Juan Guo2Jian Yang3Xiaodan Zhang4Zixuan Wang5Ying Cheng6Zewei Du7Zhechen Qi8Yanbo Huang9Mans Dennis10Yukun Wei11Dongfeng Yang12Luqi Huang13Zongsuo Liang14College of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaState Key Laboratory of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, ChinaState Key Laboratory of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaEastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, ChinaFaculty of Medical Sciences, Anton de Kom University of Suriname, Paramaribo, SurinameEastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaState Key Laboratory of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, ChinaCollege of Life Sciences and Medicine, Key Laboratory of Plant Secondary Metabolism and Regulation in Zhejiang Province, Zhejiang Sci-Tech University, Hangzhou, ChinaTanshinones found in Salvia species are the main active compounds for the treatment of cardiovascular and cerebrovascular diseases, but their contents are hugely different in different species. For example, tanshinone IIA content in Salvia castanea Diels f. tomentosa Stib. is about 49 times higher than that in Salvia miltiorrhiza Bunge. The molecular mechanism responsible for this phenomenon remains largely unknown. To address this, we performed comparative transcriptomic and proteomic analyses of S. miltiorrhiza and S. castanea. A total of 296 genes in S. castanea and 125 genes in S. miltiorrhiza were highly expressed at both the transcriptional and proteome levels, including hormone signal regulation, fungus response genes, transcription factors, and CYP450. Among these differentially expressed genes, the expression of SmWRKY61 was particularly high in S. castanea. Overexpression of SmWRKY61 in S. miltiorrhiza could significantly increase the content of tanshinone I and tanshinone IIA, which were 11.09 and 33.37 times of the control, respectively. Moreover, SmWRKY61 had a strong regulatory effect, elevating the expression levels of tanshinone pathway genes such as DXS2, CMK, HMGS2, 1, KSL1, KSL2, CYP76AH1, and CYP76AK3. For the WRKY family, 79 SmWRKYs were originally obtained and classified into three main groups. Collinearity analysis indicated a more specific extension of WRKY gene family in Salvia genus. In 55 Salvia species, only 37 species contained the WRKY61 sequence, and high SmWRKY61 expression in some Salvia L. species was often accompanied by high tanshinone accumulation. The above results suggest that SmWRKY61 is a highly effective regulator of tanshinone accumulation and may be a key factor resulting in high tanshinone accumulation in S. castanea.https://www.frontiersin.org/articles/10.3389/fpls.2021.820582/fullsecondary metabolismSalvia miltiorrhizaSalvia LinnproteometranscriptomeWRKYs
spellingShingle Yue Chen
Yanting Wang
Juan Guo
Jian Yang
Xiaodan Zhang
Zixuan Wang
Ying Cheng
Zewei Du
Zhechen Qi
Yanbo Huang
Mans Dennis
Yukun Wei
Dongfeng Yang
Luqi Huang
Zongsuo Liang
Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea
Frontiers in Plant Science
secondary metabolism
Salvia miltiorrhiza
Salvia Linn
proteome
transcriptome
WRKYs
title Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea
title_full Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea
title_fullStr Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea
title_full_unstemmed Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea
title_short Integrated Transcriptomics and Proteomics to Reveal Regulation Mechanism and Evolution of SmWRKY61 on Tanshinone Biosynthesis in Salvia miltiorrhiza and Salvia castanea
title_sort integrated transcriptomics and proteomics to reveal regulation mechanism and evolution of smwrky61 on tanshinone biosynthesis in salvia miltiorrhiza and salvia castanea
topic secondary metabolism
Salvia miltiorrhiza
Salvia Linn
proteome
transcriptome
WRKYs
url https://www.frontiersin.org/articles/10.3389/fpls.2021.820582/full
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