<p><i>Triticum aestivum</i> (common wheat) was grown hydroponically in the presence of perfluorooctanoic acid (PFOA), and the plant’s ability to cope with this stressor was assessed through several analytical methods. The tolerance index showed that wheat tolerated PFOA treatment without growth inhibition. The roots and stems of <i>T. aestivum</i> accumulated 75.82% and 24.18% of total PFOA, respectively. Root proteome analysis using a label-free shotgun proteomics approach, revealed a total of 1885 non-redundant proteins, with 215 uniquely to PFOA-treated plants. Although PFOA did not significantly affect plant growth, it had a substantial impact on the proteome. PFOA exposure reprogrammed root metabolism by altering redox balance, phosphate and hormone homeostasis, and redirecting carbohydrate and lipid pathways toward energy mobilization. Numerous lysine methylations in proteins from PFOA-treated plants highlight the plant’s metabolic plasticity in response to chemical stress, indicating that various cellular processes in the root, such as antioxidative defense, xenobiotics removal, and stress tolerance, could be regulated by methylation. Several plant lipid transfer proteins were identified in the roots of <i>T. aestivum,</i> which may be involved in the deposition of lipophilic PFOA. Decreased lipase and increased peroxidase activity indicate oxidative damage primarily affecting membrane lipids, triggering antioxidant compensation mechanisms. Integrated physiological and proteomic findings indicate that glutathione S-transferases, peroxidases and lipid transfer proteins hold the most promise for enhancing plant resilience to chemicals.</p> Graphical Abstract <p></p> <p>Hydroponically grown <i>Triticum aestivum</i> exposed to perfluorooctanoic acid (PFOA) exhibited high tolerance, with no significant inhibition of plant growth despite substantial contaminant uptake. PFOA predominantly accumulated in the roots (75.82%), with limited translocation to the shoots (24.18%), indicating restricted upward mobility within the plant. Although physiological parameters such as biomass and vegetation indices showed only minor changes, proteomic analysis revealed extensive remodeling of the root proteome, including 215 proteins uniquely identified in PFOA-treated plants. These alterations reflect a profound metabolic reprogramming involving redox homeostasis, energy production, and hormone-related signaling pathways. Adaptive responses included activation of detoxification mechanisms (e.g., glutathione S-transferases and cytochrome P450), modulation of mitochondrial function, shifts toward carbohydrate and lipid catabolism, and structural modifications of the cell wall. Enhanced protein methylation further suggests fine regulation of stress-response pathways. Overall, the results demonstrate that wheat can maintain stable growth under PFOA stress through complex molecular adaptations, highlighting proteomic responses as sensitive indicators of environmental contamination and potential targets for improving crop resilience.</p>

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Integrated Physiological and Proteomic Insights into PFOA Responses in Wheat Roots

  • Ana Medić,
  • Marija Lješević,
  • Kristina Joksimović,
  • Kristina Kasalica,
  • Abdullah Khraibah,
  • Yingxi Li,
  • Nikoleta Lugonja,
  • Branka Lončarević,
  • Hideyuki Inui,
  • Lidija Izrael Živković,
  • Jelena Radulović,
  • Itana Nuša Bubanja,
  • Ljubodrag Vujisić,
  • Maxim Berezovski,
  • Zoran Minić,
  • Ivanka Karadžić,
  • Vladimir P. Beškoski

摘要

Triticum aestivum (common wheat) was grown hydroponically in the presence of perfluorooctanoic acid (PFOA), and the plant’s ability to cope with this stressor was assessed through several analytical methods. The tolerance index showed that wheat tolerated PFOA treatment without growth inhibition. The roots and stems of T. aestivum accumulated 75.82% and 24.18% of total PFOA, respectively. Root proteome analysis using a label-free shotgun proteomics approach, revealed a total of 1885 non-redundant proteins, with 215 uniquely to PFOA-treated plants. Although PFOA did not significantly affect plant growth, it had a substantial impact on the proteome. PFOA exposure reprogrammed root metabolism by altering redox balance, phosphate and hormone homeostasis, and redirecting carbohydrate and lipid pathways toward energy mobilization. Numerous lysine methylations in proteins from PFOA-treated plants highlight the plant’s metabolic plasticity in response to chemical stress, indicating that various cellular processes in the root, such as antioxidative defense, xenobiotics removal, and stress tolerance, could be regulated by methylation. Several plant lipid transfer proteins were identified in the roots of T. aestivum, which may be involved in the deposition of lipophilic PFOA. Decreased lipase and increased peroxidase activity indicate oxidative damage primarily affecting membrane lipids, triggering antioxidant compensation mechanisms. Integrated physiological and proteomic findings indicate that glutathione S-transferases, peroxidases and lipid transfer proteins hold the most promise for enhancing plant resilience to chemicals.

Graphical Abstract

Hydroponically grown Triticum aestivum exposed to perfluorooctanoic acid (PFOA) exhibited high tolerance, with no significant inhibition of plant growth despite substantial contaminant uptake. PFOA predominantly accumulated in the roots (75.82%), with limited translocation to the shoots (24.18%), indicating restricted upward mobility within the plant. Although physiological parameters such as biomass and vegetation indices showed only minor changes, proteomic analysis revealed extensive remodeling of the root proteome, including 215 proteins uniquely identified in PFOA-treated plants. These alterations reflect a profound metabolic reprogramming involving redox homeostasis, energy production, and hormone-related signaling pathways. Adaptive responses included activation of detoxification mechanisms (e.g., glutathione S-transferases and cytochrome P450), modulation of mitochondrial function, shifts toward carbohydrate and lipid catabolism, and structural modifications of the cell wall. Enhanced protein methylation further suggests fine regulation of stress-response pathways. Overall, the results demonstrate that wheat can maintain stable growth under PFOA stress through complex molecular adaptations, highlighting proteomic responses as sensitive indicators of environmental contamination and potential targets for improving crop resilience.