Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots

Previous research has shown that fluoranthene (Flu) exhibits dual uptake behavior in ryegrass. At low concentrations (1–10 mg/L), Flu uptake is higher, whereas at higher concentrations (20–40 mg/L), uptake appears to decrease. Furthermore, indole-3-acetic acid (IAA) content and antioxidant enzyme ac...

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Main Authors: Yuanzhou Xu, Yunyun Li, Xinyue Zhang, Zhuoliang Xiao, Jiaguo Jiao, Huijuan Zhang, Huixin Li, Feng Hu, Li Xu
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325001769
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author Yuanzhou Xu
Yunyun Li
Xinyue Zhang
Zhuoliang Xiao
Jiaguo Jiao
Huijuan Zhang
Huixin Li
Feng Hu
Li Xu
author_facet Yuanzhou Xu
Yunyun Li
Xinyue Zhang
Zhuoliang Xiao
Jiaguo Jiao
Huijuan Zhang
Huixin Li
Feng Hu
Li Xu
author_sort Yuanzhou Xu
collection DOAJ
description Previous research has shown that fluoranthene (Flu) exhibits dual uptake behavior in ryegrass. At low concentrations (1–10 mg/L), Flu uptake is higher, whereas at higher concentrations (20–40 mg/L), uptake appears to decrease. Furthermore, indole-3-acetic acid (IAA) content and antioxidant enzyme activity play distinct roles in this process. However, the molecular mechanisms underlying these behaviors remain unclear. To address this, we exposed ryegrass to different Flu concentrations (0, 5, and 20 mg/L) and conducted a combined transcriptomic and physiological analysis of the root system to elucidate the specific mechanisms of Flu uptake. Our results revealed that under 5 mg/L Flu treatment, ryegrass has a higher bioconcentration factor (BCF). The genes involved in IAA synthesis (TAA1, ALDH, and AAO1/2) were upregulated, which led to an increase in IAA content. Elevated IAA levels, in turn, promoted the expression of genes encoding H+-ATPase (ATP5A1, ATP5B, ATP5H, and ATP6E) and the ABC transporter protein (ABCB1), resulting in enhanced H+-ATPase activity, and facilitated the active transport of Flu. In contrast, the 20 mg/L Flu treatment resulted in a lower BCF. The downregulation of IAA synthesis genes (amiE and YUCCA) decreased IAA content. The downregulation of the H+-ATPase gene (ATP6C) and the ABC transporter protein gene (ABCG2), resulting in decreased H+-ATPase activity and inhibited Flu transport. Moreover, the promoted expression of redox-related genes (POD1, SOD1 and SOD2) further reduced Flu uptake. Elucidating the molecular mechanisms underlying Flu uptake in ryegrass may provide a theoretical foundation for developing strategies to regulate Flu accumulation in plants.
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spelling doaj-art-59afd945a39d49a19e06a884eb5e85b72025-02-07T04:46:36ZengElsevierEcotoxicology and Environmental Safety0147-65132025-02-01291117840Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass rootsYuanzhou Xu0Yunyun Li1Xinyue Zhang2Zhuoliang Xiao3Jiaguo Jiao4Huijuan Zhang5Huixin Li6Feng Hu7Li Xu8Soil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR China; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing 210014, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR China; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing 210014, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR China; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing 210014, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR China; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing 210014, PR ChinaSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR China; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing 210014, PR China; Sanya Institute of Nanjing Agricultural University, Sanya, China; Correspondence to: Nanjing Agricultural University, Weigang No.1, Nanjing, Jiangsu 210095, PR China.Previous research has shown that fluoranthene (Flu) exhibits dual uptake behavior in ryegrass. At low concentrations (1–10 mg/L), Flu uptake is higher, whereas at higher concentrations (20–40 mg/L), uptake appears to decrease. Furthermore, indole-3-acetic acid (IAA) content and antioxidant enzyme activity play distinct roles in this process. However, the molecular mechanisms underlying these behaviors remain unclear. To address this, we exposed ryegrass to different Flu concentrations (0, 5, and 20 mg/L) and conducted a combined transcriptomic and physiological analysis of the root system to elucidate the specific mechanisms of Flu uptake. Our results revealed that under 5 mg/L Flu treatment, ryegrass has a higher bioconcentration factor (BCF). The genes involved in IAA synthesis (TAA1, ALDH, and AAO1/2) were upregulated, which led to an increase in IAA content. Elevated IAA levels, in turn, promoted the expression of genes encoding H+-ATPase (ATP5A1, ATP5B, ATP5H, and ATP6E) and the ABC transporter protein (ABCB1), resulting in enhanced H+-ATPase activity, and facilitated the active transport of Flu. In contrast, the 20 mg/L Flu treatment resulted in a lower BCF. The downregulation of IAA synthesis genes (amiE and YUCCA) decreased IAA content. The downregulation of the H+-ATPase gene (ATP6C) and the ABC transporter protein gene (ABCG2), resulting in decreased H+-ATPase activity and inhibited Flu transport. Moreover, the promoted expression of redox-related genes (POD1, SOD1 and SOD2) further reduced Flu uptake. Elucidating the molecular mechanisms underlying Flu uptake in ryegrass may provide a theoretical foundation for developing strategies to regulate Flu accumulation in plants.http://www.sciencedirect.com/science/article/pii/S0147651325001769Bioconcentration factorH+-ATPase activityAntioxidant enzyme activityIndole-3-acetic acid
spellingShingle Yuanzhou Xu
Yunyun Li
Xinyue Zhang
Zhuoliang Xiao
Jiaguo Jiao
Huijuan Zhang
Huixin Li
Feng Hu
Li Xu
Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
Ecotoxicology and Environmental Safety
Bioconcentration factor
H+-ATPase activity
Antioxidant enzyme activity
Indole-3-acetic acid
title Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
title_full Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
title_fullStr Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
title_full_unstemmed Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
title_short Auxin signaling related to H+-ATPase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
title_sort auxin signaling related to h atpase synthesis and antioxidant enzyme activities regulates fluoranthene uptake by ryegrass roots
topic Bioconcentration factor
H+-ATPase activity
Antioxidant enzyme activity
Indole-3-acetic acid
url http://www.sciencedirect.com/science/article/pii/S0147651325001769
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