Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum

Proteomics provides an essential means of explaining the mechanisms underlying gene expression regulation. The proteomic mechanisms by which heavy metal hyperaccumulators respond to lead (Pb) stress remain largely unclear. To this end, we examined Pogonatherum crinitum (Thunb.) Kunth and employed pr...

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Main Authors: Weicai Meng, Xiaolong Hou, Cuiting Cai, Shuyi Cao, Linghua Liu, Xiaoyu Wang, Shihong Guo, Xinyi Jiang, Yijie Li, Yuqi Yuan
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324015148
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author Weicai Meng
Xiaolong Hou
Cuiting Cai
Shuyi Cao
Linghua Liu
Xiaoyu Wang
Shihong Guo
Xinyi Jiang
Yijie Li
Yuqi Yuan
author_facet Weicai Meng
Xiaolong Hou
Cuiting Cai
Shuyi Cao
Linghua Liu
Xiaoyu Wang
Shihong Guo
Xinyi Jiang
Yijie Li
Yuqi Yuan
author_sort Weicai Meng
collection DOAJ
description Proteomics provides an essential means of explaining the mechanisms underlying gene expression regulation. The proteomic mechanisms by which heavy metal hyperaccumulators respond to lead (Pb) stress remain largely unclear. To this end, we examined Pogonatherum crinitum (Thunb.) Kunth and employed proteomic sequencing technology to screen for differential proteins that respond to Pb stress. The connection between Pb-tolerant proteins in metabolic pathways and their functions were analyzed. Differences in the downstream molecules of Pb-resistant proteins in P. crinitum were also assessed. Furthermore, we utilized Parallel Reaction Monitoring (PRM) technology to validate the selected Pb-tolerant differential proteins across various stress concentration gradients. A total of 5275 protein families were identified, and 118 DEPs were observed between the stressed and control groups, including 76 upregulated and 42 downregulated proteins. Functional annotation analysis using Gene Ontology and the Kyoto Encyclopedia of Genes and Genomes revealed that Pb stress led to the upregulation of 16 proteins within P. crinitum leaves. These proteins were primarily involved in the metabolic processes of energy and carbohydrate metabolism (PcCht1, PcSPS5, PcGME-1, and PcPEP4) as well as protein translation and oxidative stress (PcHSP26.7, PcHSP18, PcCAT3, and PcCAT1). Bioinformatic analysis indicated that DEPs responding to Pb stress were primarily related to the MAPK signaling pathway, amino sugar and nucleotide sugar metabolism, and starch and sucrose metabolism. Pathway analysis revealed maltose, acetylcholine, N-acetylglucosamine, and oxalic acid as the downstream products. Moreover, the levels of these indicators all increased with increasing Pb concentrations. PRM of the 16 DEPs revealed that nine proteins were upregulated under different Pb concentrations. PRM and data-independent acquisition results for the upregulation of these nine DEPs were identical, suggesting the reliability of our analytical outcomes. In conclusion, the upregulation of specific proteins in P. crinitum enables the regulation of glucose metabolism and antioxidant balance within the plant and represents a mechanism underlying its Pb stress response.
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spelling doaj-art-e7f7d96e9a224ad5be53bf38d8bb4db22024-12-07T08:24:45ZengElsevierEcotoxicology and Environmental Safety0147-65132024-12-01288117438Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitumWeicai Meng0Xiaolong Hou1Cuiting Cai2Shuyi Cao3Linghua Liu4Xiaoyu Wang5Shihong Guo6Xinyi Jiang7Yijie Li8Yuqi Yuan9College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China; Key Laboratory of Soil and Water Conservation of Southern Red Soil Region, State Forestry and Grassland Administration, Fuzhou 350002, China; National Positioning Observation and Research Station of Red Soil Hilly Ecosystem, Longyan, Changting 364000, China; Co-Innovation Center for Soil and Water Conservation in Red Soil Region of the Cross-Strait, Fuzhou 350002, China; Corresponding author at: College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China.College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaFujian Provincial Academy of Environmental Sciences, Fuzhou 350003, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaProteomics provides an essential means of explaining the mechanisms underlying gene expression regulation. The proteomic mechanisms by which heavy metal hyperaccumulators respond to lead (Pb) stress remain largely unclear. To this end, we examined Pogonatherum crinitum (Thunb.) Kunth and employed proteomic sequencing technology to screen for differential proteins that respond to Pb stress. The connection between Pb-tolerant proteins in metabolic pathways and their functions were analyzed. Differences in the downstream molecules of Pb-resistant proteins in P. crinitum were also assessed. Furthermore, we utilized Parallel Reaction Monitoring (PRM) technology to validate the selected Pb-tolerant differential proteins across various stress concentration gradients. A total of 5275 protein families were identified, and 118 DEPs were observed between the stressed and control groups, including 76 upregulated and 42 downregulated proteins. Functional annotation analysis using Gene Ontology and the Kyoto Encyclopedia of Genes and Genomes revealed that Pb stress led to the upregulation of 16 proteins within P. crinitum leaves. These proteins were primarily involved in the metabolic processes of energy and carbohydrate metabolism (PcCht1, PcSPS5, PcGME-1, and PcPEP4) as well as protein translation and oxidative stress (PcHSP26.7, PcHSP18, PcCAT3, and PcCAT1). Bioinformatic analysis indicated that DEPs responding to Pb stress were primarily related to the MAPK signaling pathway, amino sugar and nucleotide sugar metabolism, and starch and sucrose metabolism. Pathway analysis revealed maltose, acetylcholine, N-acetylglucosamine, and oxalic acid as the downstream products. Moreover, the levels of these indicators all increased with increasing Pb concentrations. PRM of the 16 DEPs revealed that nine proteins were upregulated under different Pb concentrations. PRM and data-independent acquisition results for the upregulation of these nine DEPs were identical, suggesting the reliability of our analytical outcomes. In conclusion, the upregulation of specific proteins in P. crinitum enables the regulation of glucose metabolism and antioxidant balance within the plant and represents a mechanism underlying its Pb stress response.http://www.sciencedirect.com/science/article/pii/S0147651324015148Pogonatherum crinitum (Thunb.) KunthLead stressProteomicsParallel reaction monitoringMetabolic pathways
spellingShingle Weicai Meng
Xiaolong Hou
Cuiting Cai
Shuyi Cao
Linghua Liu
Xiaoyu Wang
Shihong Guo
Xinyi Jiang
Yijie Li
Yuqi Yuan
Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum
Ecotoxicology and Environmental Safety
Pogonatherum crinitum (Thunb.) Kunth
Lead stress
Proteomics
Parallel reaction monitoring
Metabolic pathways
title Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum
title_full Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum
title_fullStr Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum
title_full_unstemmed Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum
title_short Analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of Pogonatherum crinitum
title_sort analysis of differentially expressed proteins and related metabolic pathways in response to lead stress in the leaves of pogonatherum crinitum
topic Pogonatherum crinitum (Thunb.) Kunth
Lead stress
Proteomics
Parallel reaction monitoring
Metabolic pathways
url http://www.sciencedirect.com/science/article/pii/S0147651324015148
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