Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions
The increasing atmospheric CO2 resulting from human activities over the past two centuries, which is projected to persist, has significant implications for plant physiology. However, our predictive understanding of how elevated CO2 (eCO2) modifies plant tolerance to metal stress remains limited. In...
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Elsevier
2024-12-01
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| Series: | Environment International |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0160412024007360 |
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| author | Lei Wang Sui Wang Haifeng Su Hongguang Cai Yankun Song Xiang Gong Zhihui Sun Jianhua Qu Ying Zhang |
| author_facet | Lei Wang Sui Wang Haifeng Su Hongguang Cai Yankun Song Xiang Gong Zhihui Sun Jianhua Qu Ying Zhang |
| author_sort | Lei Wang |
| collection | DOAJ |
| description | The increasing atmospheric CO2 resulting from human activities over the past two centuries, which is projected to persist, has significant implications for plant physiology. However, our predictive understanding of how elevated CO2 (eCO2) modifies plant tolerance to metal stress remains limited. In this study, we collected roots and rhizosphere soils from Trifolium repens L. subjected to lead (Pb) stress under ambient and elevated CO2 conditions, generating transcriptomic data for roots, microbiota data for rhizospheres, and conducting comprehensive multi-omics analyses. Our findings show that eCO2 reduced the accumulation of Pb-induced reactive oxygen species (ROS) and promoted plant growth by 72% to 402%, as well as increases shoot Pb uptake by 79% compared to ambient CO2. Additionally, eCO2 triggers specific defense response in T. repens, elevating the threshold for stress response. We observed a adaptive reconfiguration of transcriptional network that enhances energy efficiency and optimizes photosynthetic product utilization. Notably, eCO2 induces salicylic acid biosynthesis and activates defense pathways related to redox balance and ROS scavenging processes, thereby enhancing abiotic stress resistance. Through weighted gene co-expression network analysis, our comprehensive investigation reveals a holistic regulatory network encompassing plant traits, gene expression patterns, and bacterial structure potentially linked to metal accumulation as well as tradeoffs between growth and defense in plants under elevated CO2. These insights shed light on the plant stress responses under elevated CO2 and while contributing to a broader comprehension of plant-environment interactions. |
| format | Article |
| id | doaj-art-647ab4122733477b8dedf4f4e564db43 |
| institution | OA Journals |
| issn | 0160-4120 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Environment International |
| spelling | doaj-art-647ab4122733477b8dedf4f4e564db432025-08-20T01:58:08ZengElsevierEnvironment International0160-41202024-12-0119410915010.1016/j.envint.2024.109150Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactionsLei Wang0Sui Wang1Haifeng Su2Hongguang Cai3Yankun Song4Xiang Gong5Zhihui Sun6Jianhua Qu7Ying Zhang8School of Resources and Environment, Northeast Agricultural University, Harbin 150030, ChinaNational Key Laboratory of Smart Farm Technologies and Systems, Northeast Agricultural University, Harbin 150030, ChinaSchool of Resources and Environment, Northeast Agricultural University, Harbin 150030, ChinaJilin Academy of Agricultural Sciences (Northeast Agricultural Research Center of China), Changchun 130033, ChinaSchool of Resources and Environment, Northeast Agricultural University, Harbin 150030, ChinaSchool of Resources and Environment, Northeast Agricultural University, Harbin 150030, ChinaSchool of Resources and Environment, Northeast Agricultural University, Harbin 150030, ChinaSchool of Resources and Environment, Northeast Agricultural University, Harbin 150030, ChinaSchool of Resources and Environment, Northeast Agricultural University, Harbin 150030, China; Corresponding author.The increasing atmospheric CO2 resulting from human activities over the past two centuries, which is projected to persist, has significant implications for plant physiology. However, our predictive understanding of how elevated CO2 (eCO2) modifies plant tolerance to metal stress remains limited. In this study, we collected roots and rhizosphere soils from Trifolium repens L. subjected to lead (Pb) stress under ambient and elevated CO2 conditions, generating transcriptomic data for roots, microbiota data for rhizospheres, and conducting comprehensive multi-omics analyses. Our findings show that eCO2 reduced the accumulation of Pb-induced reactive oxygen species (ROS) and promoted plant growth by 72% to 402%, as well as increases shoot Pb uptake by 79% compared to ambient CO2. Additionally, eCO2 triggers specific defense response in T. repens, elevating the threshold for stress response. We observed a adaptive reconfiguration of transcriptional network that enhances energy efficiency and optimizes photosynthetic product utilization. Notably, eCO2 induces salicylic acid biosynthesis and activates defense pathways related to redox balance and ROS scavenging processes, thereby enhancing abiotic stress resistance. Through weighted gene co-expression network analysis, our comprehensive investigation reveals a holistic regulatory network encompassing plant traits, gene expression patterns, and bacterial structure potentially linked to metal accumulation as well as tradeoffs between growth and defense in plants under elevated CO2. These insights shed light on the plant stress responses under elevated CO2 and while contributing to a broader comprehension of plant-environment interactions.http://www.sciencedirect.com/science/article/pii/S0160412024007360Trifolium repens L.Lead stressElevated CO2Transcriptomic regulationRhizosphere microbes |
| spellingShingle | Lei Wang Sui Wang Haifeng Su Hongguang Cai Yankun Song Xiang Gong Zhihui Sun Jianhua Qu Ying Zhang Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions Environment International Trifolium repens L. Lead stress Elevated CO2 Transcriptomic regulation Rhizosphere microbes |
| title | Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions |
| title_full | Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions |
| title_fullStr | Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions |
| title_full_unstemmed | Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions |
| title_short | Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions |
| title_sort | multi omics profiling reveals elevated co2 enhanced tolerance of trifolium repens l to lead stress through environment plant microbiome interactions |
| topic | Trifolium repens L. Lead stress Elevated CO2 Transcriptomic regulation Rhizosphere microbes |
| url | http://www.sciencedirect.com/science/article/pii/S0160412024007360 |
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