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Phenanthrene metabolism in Panicum miliaceum: anatomical adaptations, degradation pathway, and computational analysis of a dioxygenase enzyme

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Abstract

Polycyclic aromatic compounds (PAHs) are persistent organic pollutants of environmental concern due to their potential impacts on food chain, with plants being particularly vulnerable. While plants can uptake, transport, and transform PAHs, the precise mechanisms underlying their localization and degradation are not fully understood. Here, a cultivation experiment conducted with Panicum miliaceum exposed different concentrations of phenanthrene (PHE). Intermediate PHE degradation compounds were identified via GC–MS analysis, leading to the proposal of a phytodegradation pathway featuring three significant benzene ring cleavage steps. Our results showed that P. miliaceum exhibited the ability to effectively degrade high levels of PHE, resulting in the production of various intermediate products through several chemical changes. Examination of the localization and anatomical characteristics revealed structural alterations linked to PHE stress, with an observed enhancement in PHE accumulation density in both roots and shoots as treatment levels increased. Following a 2-week aging period, a decrease in the amount of PHE accumulation was observed, along with a change in its localization. Bioinformatics analysis of the P. miliaceum 2-oxoglutarate–dependent dioxygenase (2-ODD) DAO-like protein revealed a 299 amino acid structure with two highly conserved domains, namely 2OG-FeII_Oxy and DIOX_N. Molecular docking analysis aligned with experimental results, strongly affirming the potential link and direct action of 2-ODD DAO-like protein with PHE. Our study highlights P. miliaceum capacity for PAHs degradation and elucidates the mechanisms behind enhanced degradation efficiency. By integrating experimental evidence with bioinformatics analysis, we offer valuable insights into the potential applications of plant-based remediation strategies for PAHs-contaminated environments.

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The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This research was supported by the research grant (number SAD/243-1401/01/30) of the University of Tabriz. The entirety of this study, encompassing all laboratory work, was principally conducted within the facilities of the University of Tabriz. The authors express their profound gratitude for the extensive support extended by the institution.

Furthermore, the authors wish to convey their sincere appreciation to Southern Federal University for facilitating computational analysis essential for bioinformatics investigations. This assistance has been made possible through financial support from the Ministry of Science and Higher Education of the Russian Federation, agreement no. 075-15-2023-587.

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ST: conceptualization; investigation; methodology; original draft; software; review and editing. RM: funding acquisition; project administration; supervision; validation. EMK: data curation; formal analysis; methodology; review and editing. MK: data curation; software; review and editing. SYSL: data curation; investigation; visualization. SS: data curation; formal analysis; validation. TM: funding acquisition; review and editing; supervision.

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Correspondence to Rouhollah Motafakkerazad.

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Responsible Editor: Gangrong Shi

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Tarigholizadeh, S., Motafakkerazad, R., Mohajel Kazemi, E. et al. Phenanthrene metabolism in Panicum miliaceum: anatomical adaptations, degradation pathway, and computational analysis of a dioxygenase enzyme. Environ Sci Pollut Res 31, 37532–37551 (2024). https://doi.org/10.1007/s11356-024-33737-5

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  • DOI: https://doi.org/10.1007/s11356-024-33737-5

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