Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis

As a high-value active component in Salvia miltiorrhiza (Danshen), the accumulation of tanshinones is under the influence of various environmental factors, yet it is unknown whether light, as an essential environmental factor for plant growth, regulates the biosynthesis of tanshinones. In this study...

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Main Authors: Han Zheng, Xueqing Fu, Muyao Yu, Qi Liu, Chenyi Li, Ling Li, Shuyi Qian, Kang Chen, Shuncang Zhang, Kexuan Tang, Luqi Huang
Format: Article
Language:English
Published: Maximum Academic Press 2024-01-01
Series:Medicinal Plant Biology
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Online Access:https://www.maxapress.com/article/doi/10.48130/mpb-0024-0006
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author Han Zheng
Xueqing Fu
Muyao Yu
Qi Liu
Chenyi Li
Ling Li
Shuyi Qian
Kang Chen
Shuncang Zhang
Kexuan Tang
Luqi Huang
author_facet Han Zheng
Xueqing Fu
Muyao Yu
Qi Liu
Chenyi Li
Ling Li
Shuyi Qian
Kang Chen
Shuncang Zhang
Kexuan Tang
Luqi Huang
author_sort Han Zheng
collection DOAJ
description As a high-value active component in Salvia miltiorrhiza (Danshen), the accumulation of tanshinones is under the influence of various environmental factors, yet it is unknown whether light, as an essential environmental factor for plant growth, regulates the biosynthesis of tanshinones. In this study, we first measured the temporal accumulation of jasmonates (JAs) and tanshinones under dark-to-light transition, and found that the accumulation of JA, JA-Ile and tanshinones is light-dependent. Transcriptome analysis revealed that SmAOS and SmAOC involved in JA biosynthesis responded rapidly under dark-to-light transition, followed by the accumulation of JA and JA-Ile. A light-responsive transcription factor SmHY5 was filtered indicating a potential regulatory relationship with tanshinone-related genes. Co-expression analysis identified multiple classes of transcription factors highly correlated with JAs and tanshinone biosynthetic genes, among which SmHY5 was confirmed to interact with SmBBX21 through Y2H-seq. Further confirmation of the interaction between SmHY5 and the IV subfamily of SmBBXs, including SmBBX20-24, was obtained through Y2H experiments. Specifically, SmBBX20 and SmBBX21 showed tissue-specific expression in aboveground and underground tissues, consistent with the accumulation sites of JAs and tanshinones. Taken together, this study contributes to the understanding of light and JA signaling in tanshinone biosynthesis in Danshen. We propose a crosstalk between light and JA signaling which regulates tanshinone biosynthesis through the SmHY5-SmBBXs complex and thus provide a basis for improving tanshinone production through the combination of light and JA.
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spelling doaj-art-a0e61c357d2b486b8b86e8d8ce7d457c2025-08-20T02:12:25ZengMaximum Academic PressMedicinal Plant Biology2835-69692024-01-013111010.48130/mpb-0024-0006mpb-0024-0006Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesisHan Zheng0Xueqing Fu1Muyao Yu2Qi Liu3Chenyi Li4Ling Li5Shuyi Qian6Kang Chen7Shuncang Zhang8Kexuan Tang9Luqi Huang10State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaFrontiers Science Center for Transformative Molecules, Joint International Research Laboratory of Metabolic & Developmental Sciences, Plant Biotechnology Research Center, Fudan-SJTU-Nottingham Plant Biotechnology R & D Center, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaState Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaState Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaDepartment of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200438, ChinaFrontiers Science Center for Transformative Molecules, Joint International Research Laboratory of Metabolic & Developmental Sciences, Plant Biotechnology Research Center, Fudan-SJTU-Nottingham Plant Biotechnology R & D Center, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaFrontiers Science Center for Transformative Molecules, Joint International Research Laboratory of Metabolic & Developmental Sciences, Plant Biotechnology Research Center, Fudan-SJTU-Nottingham Plant Biotechnology R & D Center, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaState Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaCollege of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, ChinaFrontiers Science Center for Transformative Molecules, Joint International Research Laboratory of Metabolic & Developmental Sciences, Plant Biotechnology Research Center, Fudan-SJTU-Nottingham Plant Biotechnology R & D Center, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaState Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, ChinaAs a high-value active component in Salvia miltiorrhiza (Danshen), the accumulation of tanshinones is under the influence of various environmental factors, yet it is unknown whether light, as an essential environmental factor for plant growth, regulates the biosynthesis of tanshinones. In this study, we first measured the temporal accumulation of jasmonates (JAs) and tanshinones under dark-to-light transition, and found that the accumulation of JA, JA-Ile and tanshinones is light-dependent. Transcriptome analysis revealed that SmAOS and SmAOC involved in JA biosynthesis responded rapidly under dark-to-light transition, followed by the accumulation of JA and JA-Ile. A light-responsive transcription factor SmHY5 was filtered indicating a potential regulatory relationship with tanshinone-related genes. Co-expression analysis identified multiple classes of transcription factors highly correlated with JAs and tanshinone biosynthetic genes, among which SmHY5 was confirmed to interact with SmBBX21 through Y2H-seq. Further confirmation of the interaction between SmHY5 and the IV subfamily of SmBBXs, including SmBBX20-24, was obtained through Y2H experiments. Specifically, SmBBX20 and SmBBX21 showed tissue-specific expression in aboveground and underground tissues, consistent with the accumulation sites of JAs and tanshinones. Taken together, this study contributes to the understanding of light and JA signaling in tanshinone biosynthesis in Danshen. We propose a crosstalk between light and JA signaling which regulates tanshinone biosynthesis through the SmHY5-SmBBXs complex and thus provide a basis for improving tanshinone production through the combination of light and JA.https://www.maxapress.com/article/doi/10.48130/mpb-0024-0006salvia miltiorrhizalightjasmonateshy5bbxstanshinones
spellingShingle Han Zheng
Xueqing Fu
Muyao Yu
Qi Liu
Chenyi Li
Ling Li
Shuyi Qian
Kang Chen
Shuncang Zhang
Kexuan Tang
Luqi Huang
Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
Medicinal Plant Biology
salvia miltiorrhiza
light
jasmonates
hy5
bbxs
tanshinones
title Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
title_full Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
title_fullStr Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
title_full_unstemmed Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
title_short Transcriptome and yeast two-hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
title_sort transcriptome and yeast two hybrid sequencing shed light on the crosstalk between light and jasmonate signaling in regulating tanshinone biosynthesis
topic salvia miltiorrhiza
light
jasmonates
hy5
bbxs
tanshinones
url https://www.maxapress.com/article/doi/10.48130/mpb-0024-0006
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