Abstract
Whether the ascorbic acid (AsA)-(glutathione) GSH cycle and glyoxalase (Gly) system in plants synergistically cope with potentially toxic elements have scarcely ever been evaluated. Consequently, a hydroponic experiment was adopted to investigate variations in AsA-GSH cycle, Gly system, antioxidative enzyme activity, membrane permeability, and chlorophyll content in Pontederia cordata leaves with 0 ~ 5.0 mg L−1 copper (Cu2+) exposure. Cu2+ concentration immobilized in the plant roots, stems, and leaves were also evaluated. With various Cu2+ concentration exposure, approximately 51.54 ~ 69.27% Cu2+ was immobilized in the roots, accounting for the leaves defense against Cu2+. The 5.0 mg L−1 Cu2+ exposure decreased Cu2+ translocation from stems to leaves by 64.55% compared to that in the treatment of 1.0 mg L−1 Cu2+ exposure. With 1.0 ~ 5.0 mg L−1 Cu2+ exposure for 7 d and 14 d, the plant normally grew by stable chlorophyll content, and this attributed to the increased peroxidase, ascorbate peroxidase, dehydroascorbate reductase activities in the leaves. And meanwhile, GSH, non-protein thiol total peptide (NPT), and phytochelatins (PCs) in the leaves significantly increased with 5.0 mg L−1 Cu2+ exposure for 7 d. With 1.0 ~ 5.0 mg L−1 Cu2+ exposure for 21 d and 28 d, chlorophyll content markedly decreased, and this resulted in chlorosis and wilting. However, Gly system did not function well in MG detoxification. Generally, to alleviate the toxic symptoms induced by Cu2+, the positive role of GSH, NPT, and PCs, while not Gly system in the leaves was observed.
Similar content being viewed by others
Data Availability
The data is available from corresponding author upon reasonable request.
References
Alfadul, S. M. S., & Al-Fredan, M. A. A. (2013). Effects of Cd, Cu, Pb, and Zn combinations on Phragmitesaustralis metabolism, metal accumulation and distribution. Arabian Journal for Science and Engineering, 38, 11–19.
Amin, H., Arain, B. A., Abbasi, M. S., Jahangir, T. M., & Amin, F. (2018). Potential for phytoextraction of Cu by Sesamumindicum L. and Cyamopsistetragonoloba L.: A green solution to decontaminate soil. Earth Systems and Environment, 2, 133–143.
Aneke, F., & Adu, J. (2023). Adsorption of heavy metals from contaminated water using leachate modular tower. Civil Engineering Journal, 9, 1522–1541.
Aravind, P., & Prasad, M. N. V. (2005). Modulation of cadmium-induced oxidative stress in Ceratophyllumdemersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiology and Biochemistry, 43, 107–116.
Chen, J., & Wang, X. (2015). Experimental Guidelines in Plant Physiology. East China University of Science and Technology Press.
Conry, R. R. (2011). Copper: Inorganic and coordination chemistry. In Encyclopedia of inorganic and bioinorganic chemistry (1st ed.). American Cancer Society.
Cule, N., Lucic, A., Nesic, M., & Brasanac-Bosanac, L. (2021). Accumulation of chromium and nickel by Canna indica and decorative macrophytes grown in floating treatment wetland. Fresenius Environmental Bulletin, 30, 7881–7890.
Cuypers, A., Vangronsveld, J., & Clijsters, H. (2001). The redox status of plant cells (AsA and GSH) is sensitive to zinc imposed oxidative stress in roots and primary leaves of Phaseolus vulgaris. Plant Physiology and Biochemistry, 39, 657–664.
Fariduddin, Q., Khalil, R. A. E., Mir, B. A., Bilal, A., & Yusuf, A. A. (2013). 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumissativus under salt and/or copper stress. Environmental Monitoring and Assessment, 185, 7845–7856.
Farooq, M. A., Gill, R. A., Ali, B., Wang, J., Islam, F., Ai, S., & Zhou, W. J. (2016). Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Barssicanapus L. Ecotoxicology, 25, 350–366.
Gong, Q., Li, Z. H., Wang, L., Zhou, J. Y., Kang, Q., & Niu, D. D. (2021). Gibberellic acid application on biomass, oxidative stress response, and photosynthesis in spinach (Spinaciaoleracea L.) seedlings under copper stress. Environmental Science and Pollution Research, 28, 53594–53604.
Gupta, B. K., Sahoo, K. K., Ghosh, A., Tripathi, A. K., Anwar, K., Das, P., Singh, A. K., Pareek, A., Sopory, S. K., & Singla-Pareek, S. L. (2018). Manipulation of glyoxalase pathway confers tolerance to multiple stresses in rice. Plant, Cell & Environment, 41, 1186–1200.
Halliwell, B., & Foyer, C. H. (1978). Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta, 139, 9–17.
Hasanuzzaman, M., Nahar, K., Anee, T. I., & Fujita, M. (2017a). Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system. Frontiers in Plant Science, 8, 1061.
Hasanuzzaman, M., Nahar, K., Anee, T. I., & Fujita, M. (2017b). Glutathione in plants: Biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants, 23, 249–268.
Hasanuzzaman, M., Alam, M. M., Nahar, K., Mohsin, S. M., BorhannuddinBhuyan, M. H. M., Parvin, K., Hawrylak-Nowak, B., & Fujita, M. (2019). Silicon-induced antioxidant defense and methylglyoxal detoxification works coordinately in alleviating nickel toxicity in Oryza sativa L. Ecotoxicology, 28, 261–276.
Hossain, M. A., Hossain, M. Z., & Fujita, M. (2009). Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Australian Journal of Crop Science, 3, 53–64.
Javed, T., Ali, M. M., Shabbir, R., Anwar, R., & Mauro, R. P. (2021). Alleviation of copper-induced stress in pea (Pisumsativum L.) through foliar application of gibberellic acid. Biology-Basel, 10, 120.
Jiang, B., Ma, Y., Zhu, G., & Li, Z. (2020). Prediction of soil copper phytotoxicity to barley root elongation by an EDTA extraction method. Journal of Hazardous Materials, 389, 121869.
Juang, K. W., Lee, Y. I., Lai, H. Y., Wang, C. H., & Chen, B. C. (2012). Copper accumulation, translocation, and toxic effects in grapevine cuttings. Environmental Science and Pollution Research, 19, 1315–1322.
Kampfenkel, K., Van, M. M., & Inzã, D. (1995). Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry, 225, 165–167.
Kaur, C., Ghosh, A., Pareek, A., Sopory, S. K., & Singla-Pareek, S. L. (2014). Glyoxalases and stress tolerance in plants. Biochemical Society Transactions, 42, 485–490.
Khalilzadeh, R., Pirzad, A., Sepehr, E., Khan, S., & Anwar, S. (2020). Long-term effect of heavy metal-polluted wastewater irrigation on physiological and ecological parameters of Salicornia europaea L. Journal of Soil Science and Plant Nutrition, 20, 1574–1587.
Li, H. S. (2000). Principles and Techniques of Plant Physiological Biochemical Experiment. Higher Education Press.
Li, Z. G. (2016). Methylglyoxal and glyoxalase system in plants: Old players, new concepts. Botanical Review, 82, 183–203.
Li, Z. G., Li, J. H., Du, C. K., Huang, H. D., & Gong, M. (2002). Simultaneous measurement of five antioxidant enzyme activities using a single extraction system. Journal of Yunnan Normal University, 22, 44–48.
Li, G., Shah, A. A., Khan, W. U., Yasin, N. A., & Ahmad, A. (2016). Hydrogen sulfide mitigates cadmium induced toxicity in Brassica rapa by modulating physiochemical attributes, osmolyte metabolism and antioxidative machinery. Chemosphere, 263, 127999.
Li, Y., Xin, J., Ge, W., & Tian, R. N. (2022). Tolerance mechanism and phytoremediation potential of Pistia stratiotes to zinc and cadmium co-contamination. International Journal of Phytoremediation. https://doi.org/10.1080/15226514.2021.2025201
Liu, J., Xin, X., & Zhou, Q. (2018). Phytoremediation of contaminated soils using ornamental plants. Environmental Reviews, 26, 43–54.
Mahmud, J. A., Hasanuzzaman, M., Nahar, K., BorhannuddinBhuyan, M. H. M., & Fujita, M. (2018). Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: Coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicology and Environmental Safety, 147, 990–1001.
Matayoshi, C. L., Pena, L. B., Arbona, V., Gómez-Cadenas, A., & Gallego, S. M. (2020). Early responses of maize seedlings to Cu stress include sharp decreases in gibberellins and jasmonates in the root apex. Protoplasma, 257, 1243–1256.
Mir, A. R., Pichtel, J., & Hayat, S. (2021). Copper: Uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. BioMetals, 34, 737–759.
Nahar, K., Hasanuzzaman, M., Alam, M. M., Rahman, A., Suzuki, T., & Fujita, M. (2016). Polyamine and nitric oxide crosstalk: Antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology and Environmental Safety, 126, 245–255.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22, 867–880.
Nawrot, N., Wojciechowska, E., Pazdro, K., Szmaglinski, J., & Pempkowiak, J. (2021). Uptake, accumulation, and translocation of Zn, Cu, Pb, Cd, Ni, and Cr by P. australis seedlings in an urban dredged sediment mesocosm: Impact of seedling origin and initial trace metal content. Science of The Total Environment, 768, 144983.
Nazir, F., Fariduddin, Q., Hussain, A., & Khan, T. A. (2021). Brassinosteroid and hydrogen peroxide improve photosynthetic machinery, stomatal movement, root morphology and cell viability and reduce cutriggered oxidative burst in tomato. Ecotoxicology and Environmental Safety, 207, 111081.
Neill, N., Desikan, R., & Hancock, J. (2002). Hydrogen peroxide signaling. Current Opinion in Plant Biology, 5, 388–395.
Pérez-Sirvent, C., Hernández-Pérez, C., Martínez-Sánchez, M. J., García-Lorenzo, M. L., & Bech, J. (2017). Metal uptake by wetland plants: Implications for phytoremediation and restoration. Journal of Soils and Sediments, 17, 1384–1393.
Pilon, M., Abdel-Ghany, S. E., Cohu, C. M., Gogolin, K. A., & Ye, H. (2006). Copper cofactor delivery in plant cells. Current Opinion in Plant Biology, 9, 256–263.
Prasad, R. (2018). Mycoremediation and environmental sustainability. Springer.
Principato, G. B., Rosi, G., Talesa, V., Giovanni, E., & Uotila, L. (1987). Purification and characterization of two forms of glyoxalase II from the liver and brain of Wistar rats. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 911, 349–355.
Rahman, A., Mostofa, M. G., Alam, M. M., Nahar, K., Hasanuzzaman, M., & Fujita, M. (2015). Calcium mitigates arsenic toxicity in rice seedlings by reducing arsenic uptake and modulating the antioxidant defense and glyoxalase systems and stress markers. BioMed Research International, 2015, 340812.
Rama, D. S., & Prasad, M. N. V. (1998). Copper toxicity in Ceratophyllumdemersum L. (Coontail), a free floating macrophyte: Response of antioxidant enzymes and antioxidants. Plant Science, 138, 157–165.
Rout, J. R., Sahoo, S. L., Das, R., Ram, S. S., Chakraborty, A., & Sudarshan, M. (2017). Changes in antioxidant enzyme activities and elemental profiling of Abutilon indicum L. subjected to copper stress. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 87, 1469–1478.
Sabeen, M., Mahmood, Q., Irshad, M., Fareed, I., Khan, A., Ullah, F., Hussain, J., Yousaf, H., & Tabassum, S. (2013). Cadmium phytoremediation by Arundodonax L. from contaminated soil and water. BioMed Research International, 2013, 1–9.
Stuckey, J. W., Neaman, A., Verdejo, J., Navarro-Villarroel, C. N., Peñaloza, P., & Dovletyarova, E. A. (2021). Zinc alleviates copper toxicity to lettuce and oat in copper-contaminated soils. Journal of Soil Science and Plant Nutrition, 21, 1229–1235.
Wang, J. (2003). Techniques and principles of plant physiological biochemical experiment. Northeast Forestry University Press.
Wild, R., Ooi, L., Srikanth, V., & Münch, G. (2012). A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: The N-acetyl-L-cysteine assay. Analytical and Bioanalytical Chemistry, 403, 2577–2581.
Xiao, Z. H., Zhang, Y. X., Zhang, X. W., & Li, P. (2012). Effects of exogenous Pb and Cu stress on eco-physiological characteristics on foxtail millet seedlings of different genotypes. Acta Ecologica Sinica, 32, 889–897.
Xin, J., Ma, S., Li, Y., Zhao, C., & Tian, R. N. (2020). Pontederiacordata, an ornamental aquatic macrophyte with great potential in phytoremediation of heavy-metal-contaminated wetlands. Ecotoxicology and Environmental Safety, 203, 111024.
Yang, Y., & Shen, Q. (2020). Phytoremediation of cadmium-contaminated wetland soil with Typhalatifolia L. and the underlying mechanisms involved in the heavy-metal uptake and removal. Environmental Science and Pollution Research, 27, 4905–4916.
Yemets, A., Horiunova, I., & Blume, Y. (2021). Cadmium, nickel, copper, and zinc influence on microfilament organization in Arabidopsis root cells. Cell Biology International, 45, 211–226.
Younis, M. E., Tourky, S. M. N., & Elsharkawy, S. E. A. (2018). Symptomatic parameters of oxidative stress and antioxidant defense system in Phaseolus vulgaris L. in response to copper or cadmium stress. South African Journal of Botany, 117, 207–214.
Zaouali, W., Mahmoudi, H., Salah, I. B., Mejri, F., Casabianca, H., Hosni, K., & Ouerghi, Z. (2020). Copper-induced changes in growth, photosynthesis, antioxidative system activities and lipid metabolism of cilantro (Coriandrumsativum L.). Biologia, 75, 367–380.
Zehra, A., Choudhary, S., Mukarram, M., Naeem, N., & Aftab, T. (2020). Impact of long-term copper exposure on growth, photosynthesis, antioxidant defence system and artemisinin biosynthesis in soilgrown Artemisia annua genotypes. Bulletin of Environment Contamination and Toxicology, 104, 609–618.
Zhang, T. T., Hong, M. H., Wu, M. J., Chen, B. B., & Ma, Z. L. (2020). Oxidative stress responses to cadmium in the seedlings of a commercial seaweed Sargassumfusiforme. Acta Oceanologica Sinica, 39, 147–154.
Zhao, L., Huang, Y., Paglia, K., Vaniya, A., Wancewicz, B., & Keller, A. A. (2018). Metabolomics reveals the molecular mechanisms of copper induced cucumber leaf (Cucumissativus) senescence. Environmental Science and Technology, 52, 7092–7100.
Acknowledgements
The present study was funded by the National Natural Science Foundation of China (No. 30972408), the China Postdoctoral Science Foundation (2020M671509), and the Priority Academic Program Development of Jiangsu Higher Education Institutions. And, the author also thanks the Advanced Analysis and Testing Center (AATC) of Nanjing Forestry University for their kind support, and LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
Jianpan Xin principally contributed to data analysis and paper writing and modification. Sisi Ma devoted herself to conducting the experiment and collecting the data. Runan Tian modified the article and also provide the work with funding assistance.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Xin, J., Ma, S., Xiao, H. et al. Copper Accumulation and its Effect on Glyoxalase System, AsA-GSH Cycle, Antioxidase Activity in Pontederia cordota Leaves. Water Air Soil Pollut 235, 323 (2024). https://doi.org/10.1007/s11270-024-07030-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-024-07030-7