Plant Soil Environ., 2025, 71(9):650-665 | DOI: 10.17221/246/2025-PSE
Physiological and biochemical bases of AMF-mediated antimony stress tolerance in Linum usitatissimum: enhancing growth, phytochemical production, and oxidative damage resilienceOriginal Paper
- 1 Laboratory of Engineering Processes and Industrial Systems, Chemical Engineering Department, National School of Engineers of Gabes, University of Gabes, Gabes, Tunisia
- 2 Faculty of Sciences of Gabes, University of Gabes, Gabes, Tunisia
- 3 Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia
- 4 Botany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
- 5 Higher Institute of Management of Gabes and Higher Institute of Management of Tunis, GEF2A-Lab, Tunis, Tunisia
- 6 Public Health Department, College of Health Sciences, Saudi Electronic University, Riyadh, Saudi Arabia
- 7 Department of Biology, College of Science, Kingdom of Saudi Arabia; Imam Mohammad Ibn Saud Islamic University (IMSIU), Riyadh, Kingdom of Saudi Arabia
- 8 Department of Integrative Agriculture, College of Agriculture and Veterinary Medicine, United Arab Emirates University, Al Ain, Abu Dhabi, United Arab Emirates
- 9 Centro de Investigaciones Biotecnológicas del Ecuador (CIBE), Escuela Superior Politécnica del Litoral, ESPOL, Campus Gustavo Galindo, Guayaquil, Ecuador
- 10 College of Science, Arar, Department of Biological Science, Northern Border University, Arar, Saudi Arabia
Antimony (Sb) pollution from industrial activities poses a severe global threat, particularly impacting valuable medicinal crops like linseed, which are highly sensitive to heavy metals. This study reveals the remarkable potential of arbuscular mycorrhizal fungi (AMF) as a sustainable solution to this challenge. Our research demonstrates that while Sb stress significantly impairs linseed growth and photosynthesis, it also triggers oxidative damage. AMF improved photosynthetic performance and water status, and notably enhanced the biosynthesis of crucial phytochemicals like phenolics, flavonoids, and citric acid. These compounds are vital for both plant defence and human health. Furthermore, AMF promoted the accumulation of essential detoxifying agents, leading to a better redox balance and significantly reducing Sb uptake and translocation by 47%. This dual action not only bolsters the plant’s tolerance to Sb but also enhances its medicinal value by boosting health-promoting bioactive metabolites. These promising findings underscore AMF’s dual role: a powerful tool for phytoremediation and a natural enhancer of phytochemical quality. Arbuscular mycorrhizal fungi provide a sustainable, nature-inspired approach to safely cultivate medicinal plants in environments contaminated with heavy metals, underscoring the vital role of plant-microbe interactions in alleviating environmental stresses.
Keywords: medicinal plants; symbiosis; heavy metal; redox homeostasis; detoxification; physiological parameters
Received: June 4, 2025; Revised: August 1, 2025; Accepted: August 4, 2025; Prepublished online: September 12, 2025; Published: September 26, 2025 Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- AbdElgawad H., El-Sawah A.M., Mohammed A.E., Beemster G.T.S., Sheteiwy M.S. (2022): Increasing atmospheric CO2 differentially supports arsenite stress mitigating impact of arbuscular mycorrhizal fungi in wheat and soybean plants. Chemosphere, 296: 134044.
Go to original source...
Go to PubMed...
- Adeyemi J.O., Onwudiwe D.C. (2020): Chemistry and some biological potential of bismuth and antimony dithiocarbamate complexes. Molecules, 25: 305.
Go to original source...
Go to PubMed...
- Adorian T.J., Pianesso D., Bender A.B.B., Speroni C.S., Mombach P.I., Kowalski É.A., da Silva L.P. (2022): Fractionation of linseed and obtaining ingredients rich in protein and fibers: alternatives for animal feed. Journal of the Science of Food and Agriculture, 102: 1514-1521.
Go to original source...
Go to PubMed...
- Alam M.Z., Choudhury T.R., Mridha M.A.U. (2023): Arbuscular mycorrhizal fungi enhance biomass growth, mineral content, and antioxidant activity in tomato plants under drought stress. Journal of Food Quality, 2023: 2581608.
Go to original source...
- Albqmi M., Selim S., Al-sanea M.M., Alnusaire T.S. (2023): Interactive effect of arbuscular mycorrhizal fungi (AMF) and olive solid waste on wheat under arsenite toxicity. Plants, 12: 1100.
Go to original source...
Go to PubMed...
- Albqmi M., Selim S., Bouqellah N.A., Alnusaire T.S., Almuhayawi M.S., Al Jaouni S.K., AbdElgawad H. (2024): Improving plant adaptation to soil antimony contamination: the synergistic contribution of arbuscular mycorrhizal fungus and olive mill waste. BMC Plant Biology, 24: 1-12.
Go to original source...
Go to PubMed...
- Alotaibi M.O., Saleh A.M., Sobrinho R.L., Mohammed A.E., Abdelgawad H. (2021): Arbuscular mycorrhizae mitigate aluminum toxicity and regulate proline metabolism in plants grown in acidic soil. Journal of Fungi, 7: 531.
Go to original source...
Go to PubMed...
- Al-Raddadi T.M., Al-khateeb L.A., Sadaka M.W., Bahaffi S.O. (2025): Trace element speciation and nutrient distribution in Boerhavia elegans: evaluation and toxic metal concentration across plant tissues. Toxics, 13: 14.
Go to original source...
Go to PubMed...
- Alsherif E.A., Al-shaikh T.M., Abdelgawad H. (2022): Heavy metal effects on biodiversity and stress responses of plants inhabiting contaminated soil in Khulais, Saudi Arabia. Biology, 11: 164.
Go to original source...
Go to PubMed...
- Andrade G., Mihara K.L., Linderman R.G., Bethlenfalvay G.J. (1997): Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant and Soil, 192: 71-79.
Go to original source...
- Cai F., Ren J., Tao S., Wang X. (2016): Uptake, translocation and transformation of antimony in rice (Oryza sativa L.) seedlings. Environmental Pollution, 209: 169-176.
Go to original source...
Go to PubMed...
- Chakraborty K., Bishi S.K., Goswami N., Singh A.L., Zala P.V. (2016): Differential fine-regulation of enzyme driven ROS detoxification network imparts salt tolerance in contrasting peanut genotypes. Environmental and Experimental Botany, 128: 79-90.
Go to original source...
- De Souza Buzo F., Garé L.M., Garcia N.F.S., de Andrade Silva M.S.R., Martins J.T., da Silva P.H.G., Arf O. (2023): Effect of mycorrhizae on phosphate fertilisation efficiency and maize growth under field conditions. Scientific Reports, 13: 1-12.
Go to original source...
Go to PubMed...
- Dhindsa R.S., Plumb-Dhindsa P., Thorpe T.A. (1981): Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany, 32: 93-101.
Go to original source...
- Duan R., Lin Y., Yang L., Zhang Y., Hu W., Du Y., Huang M. (2023): Effects of antimony stress on growth, structure, enzyme activity and metabolism of Nipponbare rice (Oryza sativa L.) roots. Ecotoxicology and Environmental Safety, 249: 114409.
Go to original source...
Go to PubMed...
- El-Sawah A.M., Abdel-Fattah G.G., Holford P., Ali B., Sheteiwy M.S. (2023): Funneliformis constrictum modulates polyamine metabolism to enhance tolerance of Zea mays L. to salinity. Microbiological Research, 266: 127254.
Go to original source...
Go to PubMed...
- Espinosa-Vellarino F.L., Garrido I., Ortega A., Casimiro I., Espinosa F. (2020): Effects of antimony on reactive oxygen and nitrogen species (ROS and RNS) and antioxidant mechanisms in tomato plants. Frontiers in Plant Science, 11: 674.
Go to original source...
Go to PubMed...
- Espinosa-Vellarino F.L., Garrido I., Ortega A., Casimiro I., Espinosa F. (2021): Response to antimony toxicity in Dittrichia viscosa plants: ROS, NO, H2S, and the antioxidant system. Antioxidants, 10: 1698.
Go to original source...
Go to PubMed...
- Faizan M., Alam P., Hussain A., Karabulut F., Haque S., Hui S., Hayat S. (2024): Plant stress phytochelatins: key regulator against heavy metal toxicity in plants. Plant Stress, 11: 100355.
Go to original source...
- Feng R., Wei C., Tu S., Wu F., Yang L. (2009): Antimony accumulation and antioxidative responses in four fern plants. Plant and Soil, 317: 93-101.
Go to original source...
- Filella M., Belzile N., Chen Y.W. (2002): Antimony in the environment: a review focused on natural waters I. Occurence. Earth-Science Reviews, 57: 125-176.
Go to original source...
- Gao Y., Li Q., Ling W., Zhu X. (2011): Arbuscular mycorrhizal phytoremediation of soils contaminated with phenanthrene and pyrene. Journal of Hazardous Materials, 185: 703-709.
Go to original source...
Go to PubMed...
- Garrido I., Ortega A., Hernández M., Fernández-Pozo L., Cabezas J., Espinosa F. (2021): Effect of antimony in soils of an Sb mine on the photo-synthetic pigments and antioxidant system of Dittrichia viscosa leaves. Environmental Geochemistry and Health, 43: 1367-1383.
Go to original source...
Go to PubMed...
- Gupta S., Thokchom S.D., Kapoor R. (2021): Arbuscular mycorrhiza improves photosynthesis and restores alteration in sugar metabolism in Triticum aestivum L. grown in arsenic contaminated soil. Frontiers in Plant Science, 12: 640379.
Go to original source...
Go to PubMed...
- Hadwan M.H. (2018): Simple spectrophotometric assay for measuring catalase activity in biological tissues. BMC Biochemistry, 19: 1-8.
Go to original source...
Go to PubMed...
- Haider F.U., Zulfiqar U., ul Ain N., Mehmood T., Ali U., Aguila L.C.R., Li Y., Siddique K.H., Farooq M. (2024): Managing antimony pollution: insights into soil-plant system dynamics and remediation strategies. Chemosphere, 362: 142694.
Go to original source...
Go to PubMed...
- Hozzein W.N., Abuelsoud W., Wadaan M.A.M., Al Jaouni S., Abd-Elgawad H. (2019): Exploring the potential of actinomycetes in improving soil fertility and grain quality of economically important cereals. Science of the Total Environment, 651: 2787-2798.
Go to original source...
Go to PubMed...
- Hu S., Hu B., Chen Z., Vosátka M., Vymazal J. (2020): Antioxidant response in arbuscular mycorrhizal fungi inoculated wetland plant under Cr stress. Environmental Research, 191: 110203.
Go to original source...
Go to PubMed...
- Jańczak-Pieniażek M., Cichoński J. (2023): Effect of heavy metal stress on phenolic compounds accumulation in winter wheat plants. Molecules, 28: 241.
Go to original source...
Go to PubMed...
- Jiang X., Yu W., Wu S., Tang L., Zhong G., Wan F., Huang R. (2021): Arsenic(III) and/or antimony(III) induced disruption of calcium homeostasis and endoplasmic reticulum stress resulting in apoptosis in the mouse heart. Ecotoxicology and Environmental Safety, 220: 112394.
Go to original source...
Go to PubMed...
- Kaur P., Waghmare R., Kumar V., Rasane P., Kaur S., Gat Y. (2018): Recent advances in utilisation of flaxseed as a potential source for value addition. OCL - Oilseeds and Fats, Crops and Lipids, 220: 112394.
Go to original source...
- Kiryluk A., Kostecka J. (2020): Pro-environmental and health-promoting grounds for restitution of flax (Linum usitatissimum L.) cultivation. Journal of Ecological Engineering, 21: 99-107.
Go to original source...
- Lenoir I., Fontaine J., Lounès-Hadj Sahraoui A. (2016): Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry, 123: 4-15.
Go to original source...
Go to PubMed...
- Li H., Wang H., Zhao J., Zhang L., Li Y., Wang H., Yuan Z. (2022): Physio-biochemical and transcriptomic features of arbuscular mycorrhizal fungi relieving cadmium stress in wheat. Antioxidants, 11: 2390.
Go to original source...
Go to PubMed...
- Luo W.T., He L., Li F., Li J.K. (2021): Exogenous salicylic acid alleviates the antimony (Sb) toxicity in rice (Oryza sativa L.) seedlings. Journal of Plant Growth Regulation, 40: 1327-1340.
Go to original source...
- Mi Y., Xu C., Li X., Zhou M., Cao K., Dong C., Wei Y. (2023): Arbuscular mycorrhizal fungi community analysis revealed the significant impact of arsenic in antimony- and arsenic-contaminated soil in three Guizhou regions. Frontiers in Microbiology, 14: 1-15.
Go to original source...
Go to PubMed...
- Mohammed A.E., Pawelzik E., Nour M.M., Alotaibi M.O., Abdelgawad H., Saleh A.M. (2023): Mycorrhized wheat and bean plants tolerate bis-muth contaminated soil via improved metal detoxification and antioxidant defense systems. Plant Physiology and Biochemistry, 205: 108148.
Go to original source...
Go to PubMed...
- Naudts K., Van den Berge J., Farfan E., Asard H., Nijs I. (2013): Future climate alleviates stress impact on grassland productivity through altered antioxidant capacity. Environmental and Experimental Botany, 99: 150-158.
Go to original source...
- Neetu N., Aggarwal A., Tanwar A., Alpa A. (2012): Influence of arbuscular mycorrhizal fungi and Pseudomonas fluorescens at different superphosphate levels on linseed (Linum usitatissimum L.) growth response. Chilean Journal of Agricultural Research, 72: 237-243.
Go to original source...
- Nishad P.A., Bhaskarapillai A. (2021): Antimony, a pollutant of emerging concern: a review on industrial sources and remediation technologies. Chemosphere, 277: 130252.
Go to original source...
Go to PubMed...
- Novitskaya L., Trevanion S.J., Driscoll S., Foyer C.H., Noctor G. (2002): How does photorespiration modulate leaf amino acid contents? A dual approach through modelling and metabolite analysis. Plant, Cell and Environment, 25: 821-835.
Go to original source...
- Ortega A., Garrido I., Casimiro I., Espinosa F. (2017): Effects of antimony on redox activities and antioxidant defence systems in sunflower (Helianthus annuus L.) plants. PLoS One, 12: 1-21.
Go to original source...
Go to PubMed...
- Pasricha S., Mathur V., Garg A., Lenka S., Verma K. (2021): Molecular mechanisms underlying heavy metal uptake, translocation and tolerance in hyperaccumulators - an analysis. Environmental Challenges, 4: 100197.
Go to original source...
- Periferakis A., Caruntu A., Periferakis A.T., Scheau A.E., Badarau I.A., Caruntu C., Scheau C. (2022): Availability, toxicology and medical significance of antimony. International Journal of Environmental Research and Public Health, 9: 4669.
Go to original source...
Go to PubMed...
- Peško M., Molnárová M., Fargašová A. (2016): Response of tomato plants (Solanum lycopersicum) to stress induced by Sb(III). Acta Environmen-talica Universitatis Comenianae, 24: 42-47.
Go to original source...
- Poimenova I.A., Sozarukova M.M., Ratova D.M.V., Nikitina V.N., Khabibullin V.R., Mikheev I.V., Proskurnin M.A. (2024): Analytical methods for assessing thiol antioxidants in biological fluids: a review. Molecules, 29: 4433.
Go to original source...
Go to PubMed...
- Rahman M., Asaeda T., Fukahori K., Imamura F., Nohara A., Matsubayashi M. (2023): Hydrogen peroxide measurement can be used to monitor plant oxidative stress rapidly using modified ferrous oxidation xylenol orange and titanium sulfate assay correlation. International Journal of Plant Biology, 14: 546-557.
Go to original source...
- Schwab A.P., He Y., Banks M.K. (2005): The influence of organic ligands on the retention of lead in soil. Chemosphere, 61: 856-866.
Go to original source...
Go to PubMed...
- Singh V.P., Singh S., Kumar J., Prasad S.M. (2015): Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged Luffa seedlings. Protoplasma, 252: 1217-1229.
Go to original source...
Go to PubMed...
- Sreekanth T.V.M., Nagajyothi P.C., Lee K.D., Prasad T.N.V.K.V. (2013): Occurrence, physiological responses and toxicity of nickel in plants. Environmental Science and Technology, 10: 1129-1140.
Go to original source...
- Srivastava R.K., Pandey P., Rajpoot R., Rani A., Dubey R.S. (2014): Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma, 251: 1047-1065.
Go to original source...
Go to PubMed...
- Stavropoulos P., Mavroeidis A., Papadopoulos G., Roussis I., Bilalis D., Kakabouki I. (2023): On the Path towards a "Greener" EU: a mini review on flax (Linum usitatissimum L.) as a case study. Plants, 12: 1102.
Go to original source...
Go to PubMed...
- Talaat N.B. (2014): Plant physiology and biochemistry effective microorganisms enhance the scavenging capacity of the ascorbate-glutathione cycle in common bean (Phaseolus vulgaris L.) plants grown in salty soils. Plant Physiology and Biochemistry, 80: 136-143.
Go to original source...
Go to PubMed...
- Taulavuori E., Hellström E.K., Taulavuori K., Laine K. (2001): Comparison of two methods used to analyse lipid peroxidation from Vaccinium myrtillus (L.) during snow removal, reacclimation and cold acclimation. Journal of Experimental Botany, 52: 2375-2380.
Go to original source...
Go to PubMed...
- Tzamos E., Gamaletsos P.N., Grieco G., Bussolesi M., Xenidis A., Zouboulis A., Godelitsas A. (2020): New insights into the mineralogy and geochemistry of Sb ores from Greece. Minerals, 10: 236.
Go to original source...
- Vardhan K.H., Kumar P.S., Panda R.C. (2019): A review on heavy metal pollution, toxicity and remedial measures: current trends and future perspectives. Journal of Molecular Liquids, 290: 111197.
Go to original source...
- Versieren L., Evers S., AbdElgawad H., Asard H., Smolders E. (2017): Mixture toxicity of copper, cadmium, and zinc to barley seedlings is not explained by antioxidant and oxidative stress biomarkers. Environmental Toxicology and Chemistry, 36: 220-230.
Go to original source...
Go to PubMed...
- Wei Y., Su Q., Sun Z.J., Shen Y.Q., Li J.N., Zhu X.L., Wu F.C. (2016): The role of arbuscular mycorrhizal fungi in plant uptake, fractions, and speciation of antimony. Applied Soil Ecology, 107: 244-250.
Go to original source...
- Wellburn A.R. (1994): The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology, 144: 307-313.
Go to original source...
- Yong W.A., Mubark H., Mirza N. (2017): Physiological characteristics of Ficus tikoua under antimony stress. Transactions of Nonferrous Metals Society of China, 27: 939-945.
Go to original source...
- Zainab N., Din B.U., Javed M.T., Afridi M.S., Mukhtar T., Kamran M.A., Khan A.A., Ali J., Jatoi W.N., Munis M.F.H., Chaudhary H.J. (2020): Deciphering metal toxicity responses of flax (Linum usitatissimum L.) with exopolysaccharide and ACC-deaminase producing bacteria in industrially contaminated soils. Plant Physiology and Biochemistry, 152: 90-99.
Go to original source...
Go to PubMed...
- Zhang J., Jia W., Yang J., Ismail A.M. (2006): Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research, 97: 111-119.
Go to original source...
- Zhou M., Li X., Liu X., Mi Y., Fu Z., Zhang R., Wang F. (2022): Effects of antimony on rice growth and its existing forms in rice under arbuscular mycorrhizal fungi environment. Frontiers in Microbiology, 13: 1-11.
Go to original source...
Go to PubMed...
- Zhou X., Sun C., Zhu P., Liu F. (2018): Effects of antimony stress on photosynthesis and growth of Acorus calamus. Frontiers in Plant Science, 9: 579.
Go to original source...
Go to PubMed...
- Zinta G., Khan A., AbdElgawad H., Verma V., Srivastava A.K. (2016): Unveiling the redox control of plant reproductive development during abiotic stress. Frontiers in Plant Science, 7: 700.
Go to original source...
Go to PubMed...
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.