Academic Journal
Sustainable Mitigation of Tungsten Nanoparticle Contamination via Chitosan-Driven Regulation of Photosynthesis and Lignin Metabolism in Chickpea.
| Τίτλος: | Sustainable Mitigation of Tungsten Nanoparticle Contamination via Chitosan-Driven Regulation of Photosynthesis and Lignin Metabolism in Chickpea. |
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| Συγγραφείς: | Aloufi FA; Department of Environment, Faculty of Environmental Sciences, King Abdulaziz University, Jeddah, Saudi Arabia., Halawani RF; Department of Environment, Faculty of Environmental Sciences, King Abdulaziz University, Jeddah, Saudi Arabia. |
| Πηγή: | Physiologia plantarum [Physiol Plant] 2026 May-Jun; Vol. 178 (3), pp. e70928. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: Scandinavian Society For Plant Physiology Country of Publication: Denmark NLM ID: 1256322 Publication Model: Print Cited Medium: Internet ISSN: 1399-3054 (Electronic) Linking ISSN: 00319317 NLM ISO Abbreviation: Physiol Plant Subsets: MEDLINE |
| Imprint Name(s): | Publication: Copenhagen : Scandinavian Society For Plant Physiology Original Publication: Lund, Sweden [etc.] |
| Ιατρικοί όροι (MeSH): | Photosynthesis*/drug effects , Chitosan*/pharmacology , Lignin*/metabolism , Cicer*/drug effects , Cicer*/metabolism , Cicer*/physiology , Metal Nanoparticles*/toxicity, Oxidative Stress/drug effects ; Plant Roots/drug effects ; Plant Roots/metabolism ; Nanoparticles |
| Περίληψη: | Tungsten nanoparticles (WNPs) impose severe phytotoxicity, highlighting the need for sustainable mitigation strategies. Here, we investigated the physiological and metabolic mechanisms by which chitosan nanoparticles (CSNPs) alleviate WNP stress in chickpea. Seeds were primed with 20 μg mL-1 CSNPs and grown in soil contaminated with 500 mg kg-1 WNPs. WNP exposure markedly suppressed growth and triggered oxidative stress, whereas CSNP application restored biomass accumulation, increasing shoot and root dry weight in response to CSNPs (by 76%-129%) and CSNPs + WNPs (by 99%-109%). CSNPs improved photosynthetic performance, as reflected by an increase in net photosynthetic rate, partially compensating for the high reduction induced by WNPs, and thereby enhanced carbon assimilation. Consequently, soluble sugars and starch accumulated in shoots and roots by 39%-70% under combined CSNP and WNP treatment. Increased carbon availability promoted amino acid biosynthesis, including glutamine, glutamate, proline, and phenylalanine, which function in osmotic adjustment and antioxidant defense, and activated the phenylpropanoid pathway via enhanced phenylalanine ammonia-lyase activity, thereby contributing to the mitigation of nanoparticle-induced stress. The enhanced phenylalanine pool was preferentially channeled into lignin biosynthesis via upregulation of COMT and CAD, resulting in a 130%-161% increase in lignin content. Collectively, these findings demonstrate that CSNPs mitigate WNP toxicity by restoring photosynthetic carbon flux and reallocating assimilates toward stress-responsive metabolites and lignin-based structural defense. (© 2026 Scandinavian Plant Physiology Society.) |
| References: | AbdElgawad, H., D. De Vos, G. Zinta, M. A. Domagalska, G. T. Beemster, and H. Asard. 2015. “Grassland Species Differentially Regulate Proline Concentrations Under Future Climate Conditions: An Integrated Biochemical and Modelling Approach.” New Phytologist 208, no. 2: 354–369. AbdElgawad, H., D. Peshev, and G. Zinta. 2014. “Climate Extreme Effects on the Chemical Composition of Temperate Grassland Species Under Ambient and Elevated CO2: A Comparison of Fructan and Non‐Fructan Accumulators.” PLoS One 9: e92044. https://doi.org/10.1371/journal.pone.0092044. Abuelsoud, W., A. M. Saleh, A. E. Mohammed, M. O. Alotaibi, and H. AbdElgawad. 2023. “Chitosan Nanoparticles Upregulate C and N Metabolism in Soybean Plants Grown Under Elevated Levels of Atmospheric Carbon Dioxide.” International Journal of Biological Macromolecules 252: 126434. Adamakis, I. D., E. Panteris, and E. P. Eleftheriou. 2012. “Tungsten Toxicity in Plants.” Plants (Basel) 1, no. 2: 82–99. Afzal, S., N. Chaudhary, and N. K. Singh. 2021. “Role of Soluble Sugars in Metabolism and Sensing Under Abiotic Stress.” In Plant Growth Regulators: Signalling Under Stress Conditions, 305–334. Springer International Publishing. Albqmi, M., S. Selim, M. Yaghoubi Khanghahi, et al. 2023. “Chromium(VI) Toxicity and Active Tolerance Mechanisms of Wheat Plant Treated With Plant Growth‐Promoting Actinobacteria and Olive Solid Waste.” ACS Omega 8, no. 36: 32458–32467. https://doi.org/10.1021/acsomega.3c02447. Albqmi, M., M. Yaghoubi Khanghahi, S. Selim, et al. 2023. “Positive Interaction of Selenium Nanoparticles and Olive Solid Waste on Vanadium‐Stressed Soybean Plant.” Agriculture‐Basel 13, no. 2: 426. Balusamy, S. R., S. Rahimi, J. Sukweenadhi, et al. 2022. “Chitosan, Chitosan Nanoparticles and Modified Chitosan Biomaterials, a Potential Tool to Combat Salinity Stress in Plants.” Carbohydrate Polymers 284: 119189. Barot, M., A. Modi, and A. Husen. 2025. “Understanding the Roles of Sugar and Polyols (Sugar Alcohols) for Plants Tolerance and Acclimatization Under Changing Environmental Situations.” In Roles of Osmolytes in Changing Environment, 119–134. Academic Press. Benzie, I. F., and J. J. Strain. 1996. “The Ferric Reducing Ability of Plasma (FRAP) as a Measure of ‘Antioxidant Power’: The FRAP Assay.” Analytical Biochemistry 239, no. 1: 70–76. Bocso, N. S., and M. Butnariu. 2022. “The Biological Role of Primary and Secondary Plants Metabolites.” Journal of Nutrition and Food Processing 5, no. 3: 1–7. Burrell, M. M., and T. Ap Rees. 1974. “Carbohydrate Metabolism of Rice Leaves Infected by Piricularia oryzae.” Physiological Plant Pathology 4, no. 4: 489–496. Caretto, S., V. Linsalata, G. Colella, G. Mita, and V. Lattanzio. 2015. “Carbon Fluxes Between Primary Metabolism and Phenolic Pathway in Plant Tissues Under Stress.” International Journal of Molecular Sciences 16, no. 11: 26378–26394. Chi, Z., L. Hao, H. Dong, et al. 2020. “The Innovative Application of Organosolv Lignin for Nanomaterial Modification to Boost Its Heavy Metal Detoxification Performance in the Aquatic Environment.” Chemical Engineering Journal 382: 122789. Croft, H., J. M. Chen, X. Luo, P. Bartlett, B. Chen, and R. M. Staebler. 2017. “Leaf Chlorophyll Content as a Proxy for Leaf Photosynthetic Capacity.” Global Change Biology 23, no. 9: 3513–3524. Dong, Q., Q. Tao, B. Li, et al. 2023. “The Mechanism of Enhanced Lignin Regulating Foliar cd Absorption and Yield in Rice (Oryza Sativa L.).” Ecotoxicology and Environmental Safety 249: 114481. Faizan, M., V. D. Rajput, A. A. Al‐Khuraif, et al. 2021. “Effect of Foliar Fertigation of Chitosan Nanoparticles on Cadmium Accumulation and Toxicity in Solanum lycopersicum.” Biology 10, no. 7: 666. Feduraev, P., L. Skrypnik, A. Riabova, et al. 2020. “Phenylalanine and Tyrosine as Exogenous Precursors of Wheat (Triticum aestivum L.) Secondary Metabolism Through PAL‐Associated Pathways.” Plants 9, no. 4: 476. Galtier, N., C. H. Foyer, and E. Murchie. 1995. “Effects of Light and Atmosphere CO2 Enrichment on Photosynthetic Carbon Partitioning and Carbon/Nitrogen Ratios in Tomato (Lycopersicon esculentum L.) Plants Over‐Expressing Sucrose Phosphate Synthase.” Journal of Experimental Botany 46: 1335–1344. Gao, F., X. Zhang, J. Zhang, et al. 2022. “Zinc Oxide Nanoparticles Improve Lettuce (Lactuca sativa L.) Plant Tolerance to Cadmium by Stimulating Antioxidant Defense, Enhancing Lignin Content and Reducing the Metal Accumulation and Translocation.” Frontiers in Plant Science 13: 1015745. Ge, Y., and Z. Li. 2018. “Application of Lignin and Its Derivatives in Adsorption of Heavy Metal Ions in Water: A Review.” ACS Sustainable Chemistry & Engineering 6, no. 5: 7181–7192. Goffner, D., M. M. Campbell, C. Campargue, et al. 1994. “Purification and Characterization of Cinnamoyl‐Coenzyme A: NADP Oxidoreductase in Eucalyptus gunnii.” Plant Physiology 106, no. 2: 625–632. Gross, G. G. 2008. “From Lignins to Tannins: Forty Years of Enzyme Studies on the Biosynthesis of Phenolic Compounds.” Phytochemistry 69, no. 18: 3018–3031. Gui, J. 2024. “Acetyl Bromide Method for Total Lignin Content Determination in Plant Biomass.” In Plant Protein Secretion: Methods and Protocols, 95–100. Springer. Guo, D., F. Chen, K. Inoue, J. W. Blount, and R. A. Dixon. 2001. “Downregulation of Caffeic Acid 3‐O‐Methyltransferase and Caffeoyl CoA 3‐O‐Methyltransferase in Transgenic Alfalfa: Impacts on Lignin Structure and Implications for the Biosynthesis of G and S Lignin.” Plant Cell 13, no. 1: 73–88. Guo, X., S. Zhang, and X. Q. Shan. 2008. “Adsorption of Metal Ions on Lignin.” Journal of Hazardous Materials 151, no. 1: 134–142. Halawani, R. F., H. AbdElgawad, F. A. Aloufi, M. A. Balkhyour, A. Zrig, and A. H. Hassan. 2023. “Synergistic Effect of Carbon Nanoparticles With Mild Salinity for Improving Chemical Composition and Antioxidant Activities of Radish Sprouts.” Frontiers in Plant Science 14: 1158031. Hemphill, J. K., and S. Venketeswaran. 1978. “Chlorophyll and Carotenoid Accumulation in Three Chlorophyllous Callus Phenotypes of Glycine max.” American Journal of Botany 65, no. 10: 1055–1063. Hossain, Z., G. Mustafa, and S. Komatsu. 2015. “Plant Responses to Nanoparticle Stress.” International Journal of Molecular Sciences 16, no. 11: 26644–26653. Jin, Z., J. Wungsintaweekul, S. H. Kim, et al. 2020. “4‐Coumarate: Coenzyme A Ligase Isoform 3 From Piper nigrum (Pn4CL3) Catalyzes the CoA Thioester Formation of 3, 4‐Methylenedioxycinnamic and Piperic Acids.” Biochemical Journal 477, no. 1: 61–74. Khan, P., A. M. Abdelbacki, M. Albaqami, R. Jan, and K. M. Kim. 2025. “Proline Promotes Drought Tolerance in Maize.” Biology 14, no. 1: 41. Kokilavani, S., I. A. Alaraidh, M. K. Okla, et al. 2022. “Efficient Photocatalytic Degradation of Methyl Orange and Malachite Green by Ag3PO4 Decorated BiOBr Nanoflower Under Visible Light: Performance Evaluation, Mechanism Insights and Toxicology of the By‐Products.” Journal of Alloys and Compounds 909: 164703. Kondal, R., A. Kalia, O. Krejcar, et al. 2021. “Chitosan‐Urea Nanocomposite for Improved Fertilizer Applications: The Effect on the Soil Enzymatic Activities and Microflora Dynamics in N Cycle of Potatoes (Solanum tuberosum L.).” Polymers 13, no. 17: 2887. Koul, B., K. Sharma, V. Sehgal, D. Yadav, M. Mishra, and C. Bharadwaj. 2022. “Chickpea (Cicer arietinum L.) Biology and Biotechnology: From Domestication to Biofortification and Biopharming.” Plants (Basel) 11, no. 21: 2926. https://doi.org/10.3390/plants11212926. Kumar, A., and N. C. Aery. 2011. “Effect of Tungsten on Growth, Biochemical Constituents, Molybdenum and Tungsten Contents in Wheat.” Plant, Soil and Environment 57, no. 11: 519–525. Kume, A., T. Akitsu, and K. N. Nasahara. 2018. “Why Is Chlorophyll b Only Used in Light‐Harvesting Systems?” Journal of Plant Research 131: 961–972. Liu, H., X. Gao, W. Fan, and X. Fu. 2025. “Optimizing Carbon and Nitrogen Metabolism in Plants: From Fundamental Principles to Practical Applications.” Journal of Integrative Plant Biology 67, no. 6: 1447–1466. Lowe, L. E. 1993. Soil Sampling and Methods of Analysis, edited by M. R. Carter. CRC Press. Melis, A. 2009. “Solar Energy Conversion Efficiencies in Photosynthesis: Minimizing the Chlorophyll Antennae to Maximize Efficiency.” Plant Science 177, no. 4: 272–280. Nandini, T., C. Sudhalakshmi, K. Sivakumar, E. Parameswari, and C. Thangamani. 2025. “A Review‐Chitosan Nanoparticles Towards Enhancing Nutrient Use Efficiency in Crops.” International Journal of Biological Macromolecules 24: 141433. Naudts, K., J. Van den Berge, E. Farfan, et al. 2014. “Future Climate Alleviates Stress Impact on Grassland Productivity Through Altered Antioxidant Capacity.” Environmental and Experimental Botany 99: 150–158. Pascual, M. B., J. El‐Azaz, F. N. de la Torre, R. A. Cañas, C. Avila, and F. M. Cánovas. 2016. “Biosynthesis and Metabolic Fate of Phenylalanine in Conifers.” Frontiers in Plant Science 7: 1030. Peng, Q., A. Shrestha, Y. Zhang, J. Fan, F. Yu, and G. Wang. 2024. “How Lignin Biosynthesis Responds to Nitrogen in Plants: A Scoping Review.” Plant Biology 26, no. 6: 881–895. Prasad, R., A. Bhattacharyya, and Q. D. Nguyen. 2017. “Nanotechnology in Sustainable Agriculture: Recent Developments, Challenges, and Perspectives.” Frontiers in Microbiology 8: 1014. Qin, Y., Q. Li, Q. An, et al. 2022. “A Phenylalanine Ammonia Lyase From Fritillaria unibracteata Promotes Drought Tolerance by Regulating Lignin Biosynthesis and SA Signaling Pathway.” International Journal of Biological Macromolecules 213: 574–588. Riaz, M. W., M. I. Yousaf, Q. Hussain, M. Yasir, M. Sajjad, and L. Shah. 2023. “Role of Lignin in Wheat Plant for the Enhancement of Resistance Against Lodging and Biotic and Abiotic Stresses.” Stress 3, no. 2: 434–453. Robinson, S. A., A. P. Slade, G. G. Fox, R. Phillips, R. G. Ratcliffe, and G. R. Stewart. 1991. “The Role of Glutamate Dehydrogenase in Plant Nitrogen Metabolism.” Plant Physiology 95, no. 2: 509–516. Saleh, A. M., M. Abdel‐Mawgoud, A. R. Hassan, T. H. Habeeb, R. S. Yehia, and H. AbdElgawad. 2020. “Global Metabolic Changes Induced by Arbuscular Mycorrhizal Fungi in Oregano Plants Grown Under Ambient and Elevated Levels of Atmospheric CO2.” Plant Physiology and Biochemistry 151: 255–263. Saleh, A. M., W. M. El‐Soud, M. O. Alotaibi, G. T. Beemster, A. E. Mohammed, and H. AbdElgawad. 2023. “Chitosan Nanoparticles Support the Impact of Arbuscular Mycorrhizae Fungi on Growth and Sugar Metabolism of Wheat Crop.” International Journal of Biological Macromolecules 235: 123806. Salvador, V. H., R. B. Lima, W. D. dos Santos, et al. 2013. “Cinnamic Acid Increases Lignin Production and Inhibits Soybean Root Growth.” PLoS One 8, no. 7: e69105. Sandhu, J. S., S. Tripathi, and S. K. Chaturvedi. 2023. “Chickpea Nutritional Status and Value Chain for Sustainable Development.” In Sustainable Food Value Chain Development: Perspectives From Developing and Emerging Economies, vol. 4, 175–183. Springer Nature. Selim, S., H. AbdElgawad, A. M. Reyad, et al. 2022. “Potential Use of a Novel Actinobacterial Species to Ameliorate Tungsten Nanoparticles‐Induced Oxidative Damage in Cereal Crops.” Plant Physiology and Biochemistry 171: 226–239. Singh, A., A. Sharma, O. Singh, et al. 2024. “In‐Depth Exploration of Nanoparticles for Enhanced Nutrient Use Efficiency and Abiotic Stresses Management: Present Insights and Future Horizons.” Plant Stress 25: 100576. Steduto, P., R. Albrizio, P. Giorio, and G. Sorrentino. 2000. “Gas‐Exchange Response and Stomatal and Non‐Stomatal Limitations to Carbon Assimilation of Sunflower Under Salinity.” Environmental and Experimental Botany 44, no. 3: 243–255. Strigul, N., A. Koutsospyros, P. Arienti, C. Christodoulatos, D. Dermatas, and W. Braida. 2005. “Effects of Tungsten on Environmental Systems.” Chemosphere 61, no. 2: 248–258. Sturm, K., D. Koron, and F. Stampar. 2003. “The Composition of Fruit of Different Strawberry Varieties Depending on Maturity Stage.” Food Chemistry 83: 417–422. https://doi.org/10.1016/S0308‐8146(03)00124‐9. Twaij, B. M., H. K. M. Al‐Aubaidi, and N. Hasan. 2025. “Characterization of Phenylalanine Ammonium Lyase Gene Family in Datura Stramonium and Expression Analysis in Response to Nanoparticles‐Aluminium Oxide (Al2O3NPs) and Tungsten Oxide (WO3NPs).” Plant Nano Biology 12: 100151. Wyrambik, D., and H. Grisebach. 1975. “Purification and Properties of Isoenzymes of Cinnamyl‐Alcohol Dehydrogenase From Soybean‐Cell‐Suspension Cultures.” European Journal of Biochemistry 59, no. 1: 9–15. Yaghoubi Khanghahi, M., B. Leoni, and C. Crecchio. 2021. “Photosynthetic Responses of Durum Wheat to Chemical/Microbiological Fertilization Management Under Salt and Drought Stresses.” Acta Physiologiae Plantarum 43, no. 8: 123. Yaghoubi Khanghahi, M., H. Pirdashti, H. Rahimian, et al. 2019. “Leaf Photosynthetic Characteristics and Photosystem II Photochemistry of Rice (Oryza Sativa L.) Under Potassium‐Solubilizing Bacteria Inoculation.” Photosynthetica 57, no. 2: 500–511. Yaghoubi Khanghahi, M., S. Strafella, and C. Crecchio. 2020. “Changes in Photo‐Protective Energy Dissipation of Photosystem II in Response to Beneficial Bacteria Consortium in Durum Wheat Under Drought and Salinity Stresses.” Applied Sciences 10, no. 15: 5031. Yang, J., W. Cao, and Y. Rui. 2017. “Interactions Between Nanoparticles and Plants: Phytotoxicity and Defense Mechanisms.” Journal of Plant Interactions 12, no. 1: 158–169. Zhang, J., J. Wang, C. Zhu, R. P. Singh, and W. Chen. 2024. “Chickpea: Its Origin, Distribution, Nutrition, Benefits, Breeding, and Symbiotic Relationship With Mesorhizobium Species.” Plants 13, no. 3: 429. Zheng, J., R. Sun, D. Wu, P. Chen, and P. Zheng. 2024. “Engineered Zea mays Phenylalanine Ammonia‐Lyase for Improve the Catalytic Efficiency of Biosynthesis Trans‐Cinnamic Acid and p‐Coumaric Acid.” Enzyme and Microbial Technology 176: 110423. |
| Grant Information: | IPP: 690-155-2025 King Abdulaziz University |
| Contributed Indexing: | Keywords: antioxidant metabolites; chitosan nanoparticles; lignin biosynthesis; phenylpropanoid pathway |
| Substance Nomenclature: | 9012-76-4 (Chitosan) 9005-53-2 (Lignin) |
| Entry Date(s): | Date Created: 20260610 Date Completed: 20260613 Latest Revision: 20260613 |
| Update Code: | 20260615 |
| DOI: | 10.1111/ppl.70928 |
| PMID: | 42269688 |
| Βάση Δεδομένων: | MEDLINE |
| ISSN: | 1399-3054 |
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| DOI: | 10.1111/ppl.70928 |