Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)

Cadmium (Cd) and polycyclic aromatic hydrocarbons (PAHs) are prominent soil contaminants found in industrial sites, and their combined effects on plants are not yet fully understood. To investigate the mechanisms underlying the co-exposure of Cd and PAHs and identify key biomarkers for their co-effe...

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Main Authors: Cheng Li, Yiming Yao, Xiaosong Liu, Hao Chen, Xiaoxiao Li, Maosen Zhao, Hongzhi Zhao, Yu Wang, Zhipeng Cheng, Lei Wang, Jiemin Cheng, Hongwen Sun
Format: Article
Language:English
Published: Elsevier 2023-08-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412023003781
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author Cheng Li
Yiming Yao
Xiaosong Liu
Hao Chen
Xiaoxiao Li
Maosen Zhao
Hongzhi Zhao
Yu Wang
Zhipeng Cheng
Lei Wang
Jiemin Cheng
Hongwen Sun
author_facet Cheng Li
Yiming Yao
Xiaosong Liu
Hao Chen
Xiaoxiao Li
Maosen Zhao
Hongzhi Zhao
Yu Wang
Zhipeng Cheng
Lei Wang
Jiemin Cheng
Hongwen Sun
author_sort Cheng Li
collection DOAJ
description Cadmium (Cd) and polycyclic aromatic hydrocarbons (PAHs) are prominent soil contaminants found in industrial sites, and their combined effects on plants are not yet fully understood. To investigate the mechanisms underlying the co-exposure of Cd and PAHs and identify key biomarkers for their co-effects, an integrated analysis of metabolomics, transcriptomics, and proteomics was conducted on ryegrass leaves cultivated in soil. In nontarget metabolomics analysis, nine differentially expressed metabolites that were specifically induced by the compound exposure were identified. When combined with the analysis of differentially expressed genes and proteins, it was determined that the major pathways involved in the response to the co-stress of Cd and PAHs were linoleic acid metabolism and phenylpropanoid biosynthesis. The upregulation of 12,13-dihydroxy-9Z-octadecenoic acid and the downregulation of sinapyl alcohol were identified as typical biomarkers, respectively. Compared to scenarios of single exposures, the compound exposure to Cd and PAHs disrupted the oxidation of linoleic acid, leading to alterations in the profiles of linoleate metabolites. Additionally, it intensified hydroxylation, carboxylation, and methylation processes, and interfered with reactions involving coenzyme A, thus inhibiting lignin production. As a result, oxidative stress was elevated, and the cell wall defense system in ryegrass was weakened. The findings of this study highlight the ecological risks associated with unique biological responses in plants co-exposed to Cd and PAHs in polluted soils.
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spelling doaj.art-cb317870f1824433986e124d47d038cd2023-08-16T04:26:26ZengElsevierEnvironment International0160-41202023-08-01178108105Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)Cheng Li0Yiming Yao1Xiaosong Liu2Hao Chen3Xiaoxiao Li4Maosen Zhao5Hongzhi Zhao6Yu Wang7Zhipeng Cheng8Lei Wang9Jiemin Cheng10Hongwen Sun11MOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, China; College of Geography and Environment, Shandong Normal University, Jinan 250358, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, China; Corresponding author.MOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaCollege of Geography and Environment, Shandong Normal University, Jinan 250358, ChinaMOE Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University, Tianjin 300071, ChinaCadmium (Cd) and polycyclic aromatic hydrocarbons (PAHs) are prominent soil contaminants found in industrial sites, and their combined effects on plants are not yet fully understood. To investigate the mechanisms underlying the co-exposure of Cd and PAHs and identify key biomarkers for their co-effects, an integrated analysis of metabolomics, transcriptomics, and proteomics was conducted on ryegrass leaves cultivated in soil. In nontarget metabolomics analysis, nine differentially expressed metabolites that were specifically induced by the compound exposure were identified. When combined with the analysis of differentially expressed genes and proteins, it was determined that the major pathways involved in the response to the co-stress of Cd and PAHs were linoleic acid metabolism and phenylpropanoid biosynthesis. The upregulation of 12,13-dihydroxy-9Z-octadecenoic acid and the downregulation of sinapyl alcohol were identified as typical biomarkers, respectively. Compared to scenarios of single exposures, the compound exposure to Cd and PAHs disrupted the oxidation of linoleic acid, leading to alterations in the profiles of linoleate metabolites. Additionally, it intensified hydroxylation, carboxylation, and methylation processes, and interfered with reactions involving coenzyme A, thus inhibiting lignin production. As a result, oxidative stress was elevated, and the cell wall defense system in ryegrass was weakened. The findings of this study highlight the ecological risks associated with unique biological responses in plants co-exposed to Cd and PAHs in polluted soils.http://www.sciencedirect.com/science/article/pii/S0160412023003781Heavy metalOrganic pollutantCompound exposurePlant biological effectMultiomicsIndustry
spellingShingle Cheng Li
Yiming Yao
Xiaosong Liu
Hao Chen
Xiaoxiao Li
Maosen Zhao
Hongzhi Zhao
Yu Wang
Zhipeng Cheng
Lei Wang
Jiemin Cheng
Hongwen Sun
Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)
Environment International
Heavy metal
Organic pollutant
Compound exposure
Plant biological effect
Multiomics
Industry
title Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)
title_full Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)
title_fullStr Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)
title_full_unstemmed Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)
title_short Integrated metabolomics, transcriptomics, and proteomics analyses reveal co-exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass (Lolium perenne L.)
title_sort integrated metabolomics transcriptomics and proteomics analyses reveal co exposure effects of polycyclic aromatic hydrocarbons and cadmium on ryegrass lolium perenne l
topic Heavy metal
Organic pollutant
Compound exposure
Plant biological effect
Multiomics
Industry
url http://www.sciencedirect.com/science/article/pii/S0160412023003781
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