Article Contents
ARTICLE   Open Access     Cite

Leaf senescence as a natural "free radical factory" producing environmentally persistent free radicals

More Information
  • DownLoad: Full size image
    1. Leaf senescence produces environmentally persistent free radicals (EPFRs), a newly identified natural source.

      Cell wall remodeling and lignin accumulation provide phenolic sites for stabilizing EPFRs during senescence.

      Declining antioxidants and elevated oxidative stress drive EPFRs formation in senescent leaves.

      Senesced crop residues contain high levels of EPFRs, potentially impacting soil health and carbon cycling.

      The senescence program itself, not merely water loss, is the key driver of EPFRs generation.

  • Environmentally persistent free radicals (EPFRs) are emerging pollutants of global concern, yet their natural sources remain largely undefined. Here, we identify natural leaf senescence as a major, previously unrecognized source of EPFRs in terrestrial ecosystems. By conducting a cross-species analysis of woody and herbaceous plants, we show that EPFR formation is consistently triggered during senescence, producing markedly elevated electron paramagnetic resonance (EPR) signals compared with mature foliage. Importantly, this radical generation is driven by the senescence process itself—rather than mere water loss. Mechanistic analyses reveal that cell wall remodeling, characterized by lignin accumulation, provides phenolic-rich reaction sites for radical stabilization, while concurrent antioxidant depletion and heightened oxidative stress create a permissive redox environment. Our findings establish plant senescence as a critical biological generator of EPFRs, with implications for understanding radical fluxes in the soil–plant–atmosphere continuum and for re-evaluating the environmental impact of agricultural residue management.
  • 加载中
  • [1] Xu Y. L., Lu X. F., Su G. J., et al. (2023). Scientific and regulatory challenges of environmentally persistent free radicals: From formation theory to risk prevention strategies. J. Hazard. Mater. 456:131674. DOI:10.1016/j.jhazmat.2023.131674

    View in Article CrossRef Google Scholar

    [2] Wang X. Y., Liu H. J., Xue Y. G., et al. (2024). Formation of environmentally persistent free radicals and their risks for human health: A review. Environ. Chem. Lett. 22:1327−1343. DOI:10.1007/s10311-024-01701-x

    View in Article CrossRef Google Scholar

    [3] Xie L. Y., Zhu K. C., Chen N., et al. (2024). A critical review of an environmental risk substance induced by aging microplastics: Insights into environmentally persistent free radicals. Environ. Sci. Technol. 58:22502−22518. DOI:10.1021/acs.est.4c09107

    View in Article CrossRef Google Scholar

    [4] Zhao X. Q., Tang L., Zhang S., et al. (2024). Formation and biotoxicity of environmentally persistent free radicals in steelworks soil under thermal treatment. J. Hazard. Mater. 467:133697.DOI:10.1016/j.jhazmat.2024.133697

    View in Article Google Scholar

    [5] Zhang Y. Q., Huang W. X., Wang H. C., et al. (2025). Environmentally persistent free radical emissions from indoor urning of pelletized biofuels. Environ. Sci. Technol. 59:5661−5671. DOI:10.1021/acs.est.4c14542

    View in Article CrossRef Google Scholar

    [6] Zhao S., Gao P., Miao D., et al. (2019). Formation and evolution of solvent-extracted and nonextractable environmentally persistent free radicals in fly ash of municipal solid waste incinerators. Environ. Sci. Technol. 53:10120−10130. DOI:10.1021/acs.est.9b03453

    View in Article CrossRef Google Scholar

    [7] Hu Y. J., Zhang B. N., Guo Q. Q., et al. (2022). Characterization into environmentally persistent free radicals formed in incineration fly ash and pyrolysis biochar of sewage sludge and biomass. J. Clean. Prod. 373:133666. DOI:10.1016/j.jclepro.2022.133666

    View in Article CrossRef Google Scholar

    [8] Zhao X. Q., Cheng P. F., Borch T., et al. (2022). Humidity induces the formation of radicals and enhances photodegradation of chlorinated-PAHs on Fe(III)-montmorillonite. J. Hazard. Mater. 423:127210. DOI:10.1016/j.jhazmat.2021.127210

    View in Article CrossRef Google Scholar

    [9] Shah S., Chen J., Saleem A. R., et al. (2025). Source-oriented pollution characteristics and decay kinetics of environmentally persistent free radicals in PM2.5 and PM10. J. Hazard. Mater. 495:139074. DOI:10.1016/j.jhazmat.2025.139074

    View in Article Google Scholar

    [10] Ai J., Qin W. H., Chen J., et al. (2023). Pollution characteristics and light-driven evolution of environmentally persistent free radicals in PM2.5 in two typical northern cities of China. J. Hazard. Mater. 454:131466. DOI:10.1016/j.jhazmat.2023.131466

    View in Article Google Scholar

    [11] Li K., Chen Z. L., Hao W. Q., et al. (2024). Differential inhibition of tire wear particles on sludge dewatering by aging modes. J. Hazard. Mater. 480:136214. DOI:10.1016/j.jhazmat.2024.136214

    View in Article CrossRef Google Scholar

    [12] Zhou H. H., Wang X., Sun H., et al. (2025). Soil heterogeneity influences the biotoxicity of photoaged tire wear particles in Eisenia fetida: A comparative assessment. J. Hazard. Mater. 496:139474. DOI:10.1016/j.jhazmat.2025.139474

    View in Article CrossRef Google Scholar

    [13] Vejerano E. P. and Ahn J. (2023). Leaves are a source of biogenic persistent free radicals. Environ. Sci. Technol. Lett. 10:662−667. DOI:10.1021/acs.estlett.3c00277

    View in Article CrossRef Google Scholar

    [14] Sakuraba Y., Jeong J., Kang M. Y., et al. (2014). Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat. Commun. 5:4636. DOI:10.1038/ncomms5636

    View in Article CrossRef Google Scholar

    [15] Kräutler B. (2016). Breakdown of chlorophyll in higher plantsphyllobilins as abundant, yet hardly visible signs of ripening, senescence, and cell eeath. Angew. Chem. Int. 55:4882−4907. DOI:10.1002/anie.201508928

    View in Article CrossRef Google Scholar

    [16] Woo H. R., Masclaux-Daubresse C. and Lim P. O. (2018). Plant senescence: How plants know when and how to die. J. Exp. Bot. 69:715−718. DOI:10.1093/jxb/ery011

    View in Article CrossRef Google Scholar

    [17] Jia M., Liu X. Y., Xue H., et al. (2019). Noncanonical ATG8-ABS3 interaction controls senescence in plants. Nat. Plants. 5:212−224. DOI:10.1038/s41477-018-0348-x

    View in Article CrossRef Google Scholar

    [18] Xue F., Li X., Qin L. X., et al. (2021). Anti-aging properties of phytoconstituents and phyto-nanoemulsions and their application in managing aging-related diseases. Adv Drug Deliver Rev. 176:113886. DOI:10.1016/j.addr.2021.113886

    View in Article CrossRef Google Scholar

    [19] Khachatryan L., McFerrin C. A., Hall R. W., et al. (2014). Environmentally persistent free radicals (EPFRs). 3. Free versus bound hydroxyl radicals in EPFRaqueous solutions. Environ. Sci. Technol. 48:9220-9226. DOI:10.1021/es501158r

    View in Article Google Scholar

    [20] Yang X., Liu F. B., Yang S. Q., et al. (2024). Atmospheric evolution of environmentally persistent free radicals in the rural North China Plain: Effects on water solubility and PM2.5 oxidative potential. Atmos. Chem. Phys. 24:11029-11043. DOI:10.5194/acp-24-11029-2024

    View in Article Google Scholar

    [21] Chen X., Alvarez P. J. J. and Masiello C. A. (2025). Environmentally persistent free radicals in biochar: Environmental context and future research needs. Environ. Sci. Technol. 59:11440−11454. DOI:10.1021/acs.est.4c13603

    View in Article CrossRef Google Scholar

    [22] Yang J., Pignatello J. J., Pan B., et al. (2017). Degradation of p-Nitrophenol by Lignin and cellulose chars: H2O2-Mediated reaction and direct reaction with the char. Environ. Sci. Technol. 51:8972−8980. DOI:10.1021/acs.est.7b01087

    View in Article CrossRef Google Scholar

    [23] Ruan X. X., Liu Y. Y., Wang G. Q., et al. (2018). Transformation of functional groups and environmentally persistent free radicals in hydrothermal carbonisation of lignin. Bioresource Technol. 270:223−229. DOI:10.1016/j.biortech.2018.09.027

    View in Article CrossRef Google Scholar

    [24] Li F. F., Chang Z. F., Khaing K., et al. (2019). Organic matter protection by kaolinite over bio-decomposition as suggested by lignin and solvent-extractable lipid molecular markers. Sci. Total Environ. 647:570−576. DOI:10.1016/j.scitotenv.2018.07.456

    View in Article CrossRef Google Scholar

    [25] Chen S. J., Xia Y. H., Zhang B. L., et al. (2021). Disassembly of lignocellulose into cellulose, hemicellulose, and lignin for preparation of porous carbon materials with enhanced performances. J. Hazard. Mater. 408:124956. DOI:10.1016/j.jhazmat.2020.124956

    View in Article CrossRef Google Scholar

    [26] Chen L., Liu Z., Yang T. H., et al. (2024). Photoaged tire wear particles leading to the oxidative damage on earthworms (eisenia fetida) by disrupting the antioxidant defense system: The definitive role of environmental free radicals. Environ. Sci. Technol. 58:4500−4509. DOI:10.1021/acs.est.3c07878

    View in Article CrossRef Google Scholar

    [27] Ni Z., Zhang C., Ma H. A., et al. (2022). Facet-dependent photo-degradation of nitro polycyclic aromatic hydrocarbons on hematite under visible light: Participation of environmentally persistent free radicals and reactive oxygen/nitrogen species. Appl. Catal. B: Environ. 318:121816. DOI:10.1016/j.apcatb.2022.121816

    View in Article CrossRef Google Scholar

    [28] Sun Y. M., Li Y. R., Wang M., et al. (2018). Redox imbalance contributed differently to membrane damage of cucumber leaves under water stress and Fusarium infection. Plant Science 274:171−180. DOI:10.1016/j.plantsci.2018.05.025

    View in Article CrossRef Google Scholar

    [29] Jezek M., Silva-Alvim F. A. L., Hills A., et al. (2021). Guard cell endomembrane Ca2+-ATPases underpin a 'carbon memory' of photosynthetic assimilation that impacts on water-use efficiency. Nat. Plants. 7:1301−1313. DOI:10.1038/s41477-021-00966-2

    View in Article CrossRef Google Scholar

    [30] Cai J., Peng J., Feng J., et al. (2023). Antioxidant hepatic lipid metabolism can be promoted by orally administered inorganic nanoparticles. Nat. Commun. 14:3643. DOI:10.1038/s41467-023-39423-3

    View in Article CrossRef Google Scholar

    [31] Li T. F., Ma H., Wu S. B., et al. (2020). Effect of highly selective oxypropylation of phenolic hydroxyl groups on subsequent lignin pyrolysis: Toward the lignin valorization. Energy Convers. Manage. 207:112551. DOI:10.1016/j.enconman.2020.112551

    View in Article Google Scholar

    [32] Liu B. W., Qi Y., Qiu X. Q., et al. (2025). Photoelectrocatalytic pathway for the preparation of power-effective aviation fuel precursors from lignin. Adv. Funct. Mater. 35:2421552. DOI:10.1002/adfm.202421552

    View in Article Google Scholar

    [33] Silva C. D. G., Sun P. C., Barrett K., et al. (2024). Polyphenol oxidase activity on guaiacyl and syringyl lignin units. Angew. Chem. Int. 63:e202409324. DOI:10.1002/anie.202409324

    View in Article Google Scholar

    [34] Ding N., Fei Q., Xiao D. D., et al. (2023). Highly efficient and recyclable Z-scheme heterojunction of Ag3PO4/g-C3N4 floating foam for photocatalytic inactivation of harmful algae under visible light. Chemosphere. 317:137773. DOI:10.1016/j.chemosphere.2023.137773

    View in Article CrossRef Google Scholar

    [35] Keylor M. H., Matsuura B. S., Griesser M., et al. (2016). Synthesis of resveratrol tetramers via a stereoconvergent radical equilibrium. Science 354:1260−1265. DOI:10.1126/science.aaj1597

    View in Article CrossRef Google Scholar

    [36] Li Y. J., Qin H. X., Wu D. P., et al. (2026). Natural polyphenol-promoted degradation of emerging contaminants during copper sulfide mineral oxygenation: the synergism of surface-bound radicals and singlet oxygen. Environ. Sci. Technol. 60:6784−6794. DOI:10.1021/acs.est.5c16502

    View in Article CrossRef Google Scholar

    [37] Zhang Z. M., Yang J. R., Zhou Q. L., et al. (2025). The role and mechanism of the cGAS-STING pathway-mediated ROS in apoptosis and ferroptosis induced by manganese exposure. Redox Biology. 85:103761. DOI:10.1016/j.redox.2025.103761

    View in Article CrossRef Google Scholar

    [38] Ma B., Li Y. L., Wang K., et al. (2025). In vitro physiological evaluation of metal bioaccessibility and reactive oxygen species distribution in biomass incineration lightweight mesoporous particulate matter. J. Hazard. Mater. 498:139931. DOI:10.1016/j.jhazmat.2025.139931

    View in Article CrossRef Google Scholar

    [39] Ye J. Y., Zhang Y. H., Gao Y., et al. (2025). Impacts of environmentally persistent free radicals on the denitrification toxicity of photoaged tire wear particles in estuarine sediments. J. Hazard. Mater. 494:138623. DOI:10.1016/j.jhazmat.2025.138623

    View in Article CrossRef Google Scholar

    [40] Xia W. H., Geng Z. X., Meng Z. H., et al. (2026). Photoaging-driven transformation of tire wear particles: unraveling the spatiotemporal dynamics of persistent free radicals and their phytotoxic lmpact. Environ. Sci. Technol. 60:996−1006. DOI:10.1021/acs.est.5c03767

    View in Article CrossRef Google Scholar

  • Cite this article:

    Feng H., Jin X., Ren F., et al. (2026). Leaf senescence as a natural 'free radical factory' producing environmentally persistent free radicals. The Innovation Geoscience 4:100241. https://doi.org/10.59717/j.xinn-geo.2026.100241
    Feng H., Jin X., Ren F., et al. (2026). Leaf senescence as a natural "free radical factory" producing environmentally persistent free radicals. The Innovation Geoscience 4:100241. https://doi.org/10.59717/j.xinn-geo.2026.100241

Welcome!

To request copyright permission to republish or share portions of our works, please visit Copyright Clearance Center's (CCC) Marketplace website at marketplace.copyright.com.

Figures(7)    

Supplementary Information

Share

  • Share the QR code with wechat scanning code to friends and circle of friends.

Article Metrics

Article views(647) PDF downloads(212)

Relative Articles

Cited by

Catalog

    /

    DownLoad:  Full-Size Img  PowerPoint