Multi-omics profiling reveals elevated CO2-enhanced tolerance of Trifolium repens L. to lead stress through environment-plant-microbiome interactions

IF 10.3 1区 环境科学与生态学 Q1 ENVIRONMENTAL SCIENCES Environment International Pub Date : 2024-11-13 DOI:10.1016/j.envint.2024.109150
Lei Wang , Sui Wang , Haifeng Su , Hongguang Cai , Yankun Song , Xiang Gong , Zhihui Sun , Jianhua Qu , Ying Zhang
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Abstract

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.

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多组学分析揭示了通过环境-植物-微生物组的相互作用,二氧化碳升高增强了三叶草(Trifolium repens L.)对铅胁迫的耐受性
过去两个世纪的人类活动导致大气中的二氧化碳不断增加,预计这种情况还将持续,这对植物生理学产生了重大影响。然而,我们对升高的 CO2(eCO2)如何改变植物对金属胁迫的耐受性的预测性了解仍然有限。在本研究中,我们采集了在环境和高二氧化碳条件下受到铅(Pb)胁迫的Trifolium repens L.的根系和根瘤土壤,生成了根系的转录组数据和根瘤的微生物群数据,并进行了全面的多组学分析。我们的研究结果表明,与环境 CO2 相比,eCO2 可减少铅诱导的活性氧(ROS)的积累,促进植物生长 72% 至 402%,并使嫩枝对铅的吸收增加 79%。此外,eCO2 还能触发 T. repens 的特定防御反应,提高应激反应的阈值。我们观察到转录网络进行了适应性重组,从而提高了能量效率并优化了光合产物的利用。值得注意的是,eCO2 会诱导水杨酸的生物合成,并激活与氧化还原平衡和清除 ROS 过程相关的防御途径,从而增强对非生物胁迫的抵抗力。通过加权基因共表达网络分析,我们的综合研究揭示了一个涵盖植物性状、基因表达模式和细菌结构的整体调控网络,它可能与金属积累以及高浓度 CO2 条件下植物生长和防御之间的权衡有关。这些发现揭示了高浓度 CO2 条件下植物的胁迫响应,同时有助于更广泛地理解植物与环境之间的相互作用。
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来源期刊
Environment International
Environment International 环境科学-环境科学
CiteScore
21.90
自引率
3.40%
发文量
734
审稿时长
2.8 months
期刊介绍: Environmental Health publishes manuscripts focusing on critical aspects of environmental and occupational medicine, including studies in toxicology and epidemiology, to illuminate the human health implications of exposure to environmental hazards. The journal adopts an open-access model and practices open peer review. It caters to scientists and practitioners across all environmental science domains, directly or indirectly impacting human health and well-being. With a commitment to enhancing the prevention of environmentally-related health risks, Environmental Health serves as a public health journal for the community and scientists engaged in matters of public health significance concerning the environment.
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