Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress

Abstract Seed propagation is the main method of mulberry expansion in China, an important economic forest species. However, seed germination is the most sensitive stage to various abiotic stresses, especially salinity stress. To reveal the molecular regulatory mechanism of mulberry seed germination...

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Main Authors: Yi Wang, Wei Jiang, Chenlei Li, Zhenjiang Wang, Can Lu, Junsen Cheng, Shanglin Wei, Jiasong Yang, Qiang Yang
Format: Article
Language:English
Published: BMC 2024-02-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-024-04804-3
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author Yi Wang
Wei Jiang
Chenlei Li
Zhenjiang Wang
Can Lu
Junsen Cheng
Shanglin Wei
Jiasong Yang
Qiang Yang
author_facet Yi Wang
Wei Jiang
Chenlei Li
Zhenjiang Wang
Can Lu
Junsen Cheng
Shanglin Wei
Jiasong Yang
Qiang Yang
author_sort Yi Wang
collection DOAJ
description Abstract Seed propagation is the main method of mulberry expansion in China, an important economic forest species. However, seed germination is the most sensitive stage to various abiotic stresses, especially salinity stress. To reveal the molecular regulatory mechanism of mulberry seed germination under salt stress, flavonoid metabolomics and transcriptomics analyses were performed on mulberry seeds germinated under 50 and 100 mmol/L NaCl stress. Analysis of the flavonoid metabolome revealed that a total of 145 differential flavonoid metabolites (DFMs) were classified into 9 groups, 40 flavonols, 32 flavones, 16 chalcones and 14 flavanones. Among them, 61.4% (89) of the DFMs accumulated continuously with increasing salt concentration, reaching the highest level at a 100 mmol/L salt concentration; these DFMs included quercetin-3-O-glucoside (isoquercitrin), kaempferol (3,5,7,4'-tetrahydroxyflavone), quercetin-7-O-glucoside, taxifolin (dihydroquercetin) and apigenin (4',5,7-trihydroxyflavone), indicating that these flavonoids may be key metabolites involved in the response to salt stress. Transcriptional analysis identified a total of 3055 differentially expressed genes (DEGs), most of which were enriched in flavonoid biosynthesis (ko00941), phenylpropanoid biosynthesis (ko00940) and biosynthesis of secondary metabolites (ko01110). Combined analysis of flavonoid metabolomic and transcriptomic data indicated that phenylalanine ammonia-lyase (PAL), 4-coumarate-CoA ligase (4CL), chalcone synthase (CHS), flavonol synthase (FLS), bifunctional dihydroflavonol 4-reductase/flavanone 4-reductase (DFR) and anthocyanidin reductase (ANR) were the key genes involved in flavonoid accumulation during mulberry seed germination under 50 and 100 mmol/L NaCl stress. In addition, three transcription factors, MYB, bHLH and NAC, were involved in the regulation of flavonoid accumulation under salt stress. The results of quantitative real-time PCR (qRT‒PCR) validation showed that the expression levels of 11 DEGs, including 7 genes involved in flavonoid biosynthesis, under different salt concentrations were consistent with the transcriptomic data, and parallel reaction monitoring (PRM) results showed that the expression levels of 6 key enzymes (proteins) involved in flavonoid synthesis were consistent with the accumulation of flavonoids. This study provides a new perspective for investigating the regulatory role of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress at different concentrations.
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spelling doaj.art-04b46dc695a34f4fbf33987ea6805d512024-03-05T18:38:05ZengBMCBMC Plant Biology1471-22292024-02-0124112510.1186/s12870-024-04804-3Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stressYi Wang0Wei Jiang1Chenlei Li2Zhenjiang Wang3Can Lu4Junsen Cheng5Shanglin Wei6Jiasong Yang7Qiang Yang8College of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringSericultural & Agri-Food Research Institute Guangdong Academy of Agricultural SciencesCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringCollege of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and EngineeringAbstract Seed propagation is the main method of mulberry expansion in China, an important economic forest species. However, seed germination is the most sensitive stage to various abiotic stresses, especially salinity stress. To reveal the molecular regulatory mechanism of mulberry seed germination under salt stress, flavonoid metabolomics and transcriptomics analyses were performed on mulberry seeds germinated under 50 and 100 mmol/L NaCl stress. Analysis of the flavonoid metabolome revealed that a total of 145 differential flavonoid metabolites (DFMs) were classified into 9 groups, 40 flavonols, 32 flavones, 16 chalcones and 14 flavanones. Among them, 61.4% (89) of the DFMs accumulated continuously with increasing salt concentration, reaching the highest level at a 100 mmol/L salt concentration; these DFMs included quercetin-3-O-glucoside (isoquercitrin), kaempferol (3,5,7,4'-tetrahydroxyflavone), quercetin-7-O-glucoside, taxifolin (dihydroquercetin) and apigenin (4',5,7-trihydroxyflavone), indicating that these flavonoids may be key metabolites involved in the response to salt stress. Transcriptional analysis identified a total of 3055 differentially expressed genes (DEGs), most of which were enriched in flavonoid biosynthesis (ko00941), phenylpropanoid biosynthesis (ko00940) and biosynthesis of secondary metabolites (ko01110). Combined analysis of flavonoid metabolomic and transcriptomic data indicated that phenylalanine ammonia-lyase (PAL), 4-coumarate-CoA ligase (4CL), chalcone synthase (CHS), flavonol synthase (FLS), bifunctional dihydroflavonol 4-reductase/flavanone 4-reductase (DFR) and anthocyanidin reductase (ANR) were the key genes involved in flavonoid accumulation during mulberry seed germination under 50 and 100 mmol/L NaCl stress. In addition, three transcription factors, MYB, bHLH and NAC, were involved in the regulation of flavonoid accumulation under salt stress. The results of quantitative real-time PCR (qRT‒PCR) validation showed that the expression levels of 11 DEGs, including 7 genes involved in flavonoid biosynthesis, under different salt concentrations were consistent with the transcriptomic data, and parallel reaction monitoring (PRM) results showed that the expression levels of 6 key enzymes (proteins) involved in flavonoid synthesis were consistent with the accumulation of flavonoids. This study provides a new perspective for investigating the regulatory role of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress at different concentrations.https://doi.org/10.1186/s12870-024-04804-3MulberrySalt stressSeed germinationFlavonoidsMetabolomicsTranscriptome
spellingShingle Yi Wang
Wei Jiang
Chenlei Li
Zhenjiang Wang
Can Lu
Junsen Cheng
Shanglin Wei
Jiasong Yang
Qiang Yang
Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
BMC Plant Biology
Mulberry
Salt stress
Seed germination
Flavonoids
Metabolomics
Transcriptome
title Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
title_full Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
title_fullStr Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
title_full_unstemmed Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
title_short Integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
title_sort integrated transcriptomic and metabolomic analyses elucidate the mechanism of flavonoid biosynthesis in the regulation of mulberry seed germination under salt stress
topic Mulberry
Salt stress
Seed germination
Flavonoids
Metabolomics
Transcriptome
url https://doi.org/10.1186/s12870-024-04804-3
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