THE EFFECT OF HEAVY METAL IONS ON THE PEROXIDASE ACTIVITY IN ARABIDOPSIS THALIANA
DOI:
https://doi.org/10.31861/biosystems2023.02.144Keywords:
antioxidant enzymes, Arabidopsis thaliana, cadmium, copper, oxidative stress, heavy metals, peroxidaseAbstract
The biosphere pollution with the heavy metals (HM) has increased significantly in recent decades due to human activity. Plants can accumulate and concentrate HM, which negatively affects their growth, productivity and quality of agricultural products. Some HM, such as copper, belong to the group of biogenic elements that, in low concentrations, are essential for the normal functioning of plant organisms. Other HM such as cadmium are toxic even in low concentrations. The toxicity of HM is related to oxidative damage. In the plant cell, the antioxidant system provides protection against this kind of stress. However, data on changes in antioxidant enzyme activities in the early stage of the cellular response to HM-induced stress remain scarce. Therefore, we focused our research on studying peroxidase (POD) activity changes in Arabidopsis thaliana under conditions of rapid uptake of copper and cadmium ions into leaf tissue. For the experiments, 4.5–5-week-old A. thaliana plants were used. The plants were incubated on 0.5x MS liquid medium containing copper or cadmium chloride at concentrations of 0.1, 0.5 and 5 mM. The HM salt treatment was carried out in the dark at 20 °C for 2 (short-term stress) and 12 (long-term stress) hours. After that, the leaves were frozen and the POD activity was measured. Evaluation of the effects of Cd2+ and Cu2+ ions shows that these HM cause a decrease in POD activity after 2 hours and its increase after 12 hours of treatment. Therefore, modulation of POD activity is a component of the HM stress response in A. thaliana. Analysis of the available data revealed that the enzymes POD and CAT, which eliminate hydrogen peroxide, can partially replace each other and thus provide cellular protection in different phases of the stress response.
References
Afonne O. J., Ifediba E. C. Heavy metals risks in plant foods–need to step up precautionary measures. Curr. Opin. Toxicol. 2020; 22: 1-6. https://doi.org/10.1016/j.cotox.2019.12.006
Akbudak M. A., Filiz E., Vatansever R. et al. Genome-wide identification and expression profiling of ascorbate peroxidase (APX) and glutathione peroxidase (GPX) genes under drought stress in Sorghum (Sorghum bicolor L.). J Plant Growth Regul. 2018; 37: 925-936. https://doi.org/10.1007/s00344-018-9788-9
Amako K., Chen G., Asada K. Separate assays for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol. 1994; 35: 497–504. https://doi.org/10.1093/oxfordjournals.pcp.a078621
Badiaa O., Yssaad H. A. R., Topcuoglu B. Effect of heavy metals (copper and zinc) on proline, polyphenols and flavonoids content of tomato (Lycopersicon esculentum mill.). Plant Arch. 2020; 20: 2
Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt. Biochem. 1976; 72: 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Buzduga I. M., Panchuk I. I. Effect of copper on ascorbate peroxidase activity in Cat2 knock-out mutant of Arabidopsis thaliana. Biological Systems (Sci. Herald Chernivtsy Univ). 2013; 5: 466-470.
Buzduga I.M., Salamon I., Volkov R.A., Pаnchuk I.I. Rapid accumulation of cadmium and antioxidative response in tobacco leaves. The Open Agriculture J. 2022; 16: 1-11. https://doi.org/10.2174/18743315-v16-e2206271
Buzduga I.M., Volkov R.A., Pаnchuk I.I. Metabolic compensation in Arabidopsis thaliana catalase-deficient mutants. Cytol. Genet. 2018; 52 (1): 31–39
https://doi.org/10.3103/S0095452718010036
Chen L. M., Lin C. C., Kao C. H. Copper toxicity in rice seedlings: changes in antioxidative enzyme activities, H2O2 level, and cell wall peroxidase activity in roots. Bot. Bull. Acad. Sin. 2000; 41: 99-103
Dağhan H., Öztürk M. Soil pollution in Turkey and remediation methods. Soil remediation and plants: prospects and challenges. 2015; 287-312. https://doi.org/10.1016/B978-0-12-799937-1.00010-3
Diaconu M., Pavel L. V., Hlihor R. M. et al. Characterization of heavy metal toxicity in some plants and microorganisms - A preliminary approach for environmental bioremediation. New Biotechnol. 2020; 56: 130-139. https://doi.org/10.1016/j.nbt.2020.01.003
Dixit V., Pandey V., Shyam R. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J. Exp. Bot. 2001; 52: 1101–1109. https://doi.org/10.1093/jexbot/52.358.1101
Doliba I. M., Volkov R. A., Panchuk I. I. Activity of catalase and ascorbate peroxidase in cat2 knock-out mutant of Arabidopsis thaliana upon cadmium stress. Bull. Ukr. Soc. Geneticists and Breeders. 2011; 9(2): 200-208.
Doliba I. M., Volkov R. A., Panchuk I. I. Effect of copper on catalase and ascorbate peroxidase activity in Arabidopsis thaliana. Fiziologiia i biokhimiia kul'turnykh rastenii. 2012a; 44 (2): 157-161.
Doliba I. M., Volkov R. A., Panchuk I. I. Effect of copper ions on lipid peroxidation in cat2 knock-out mutant of Arabidopsis thaliana. Bull. Ukr. Soc. Geneticists and Breeders. 2012b; 10(1): 13-19.
Ghori N. H., Ghori T., Hayat M. Q. et al. Heavy metal stress and responses in plants. Int. J. Env. Sci. Techn. 2019; 16: 1807-1828. https://doi.org/10.1007/s13762-019-02215-8
Giannakoula A., Therios I., Chatzissavvidis C. Effect of lead and copper on photosynthetic apparatus in citrus (Citrus aurantium L.) plants. The role of antioxidants in oxidative damage as a response to heavy metal stress. Plants. 2021; 10(1): 155. https://doi.org/10.3390/plants10010155
Kidwai M., Ahmad I. Z., Chakrabarty D. Class III peroxidase: An indispensable enzyme for biotic/abiotic stress tolerance and a potent candidate for crop improvement. Plant cell reports. 2020; 39: 1381-1393. https://doi.org/10.1007/s00299-020-02588-y
Kidwai M., Dhar Y. V., Gautam N. et al. Oryza sativa class III peroxidase (OsPRX38) overexpression in Arabidopsis thaliana reduces arsenic accumulation due to apoplastic lignification. J Hazard Mater. 2019; 362: 383-393. https://doi.org/10.1016/j.jhazmat.2018.09.029
Lian Z., Zhang J., Hao Z. et al. The glutathione peroxidase gene family in Nitraria sibirica: genome-wide identification, classification, and gene expression analysis under stress conditions. Genes. 2023; 14(4): 950. https://doi.org/10.3390/genes14040950
Mir A. R., Pichtel J., Hayat S. Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals. 2021; 34 (4): 737-759. https://doi.org/10.1016/j.chemosphere.2019.05.001
Murtaza B., Naeem F., Shahid M. et al. A multivariate analysis of physiological and antioxidant responses and health hazards of wheat under cadmium and lead stress. Env. Sci. Pollution Res. 2019; 26: 362-370. https://doi.org/10.1007/s11356-018-3605-7
Raja V., Qadir S. U., Alyemeni M. N. et al. Impact of drought and heat stress individually and in combination on physio-biochemical parameters, antioxidant responses, and gene expression in Solanum lycopersicum. 3 Biotech. 2020; 10: 1-18. https://doi.org/10.1007/s13205-020-02206-4
Rohozynskyj M. S., Shelifist A. E., Kostyshyn S.S. et al. Influence of heavy metals ions on plants in vitro. Fiziologiia i biokhimiia kul'turnykh rastenii. 1998a; 30 (6): 465-471
Rohozynskyj M. S., Yaslovitskaya L. S., Volkov R. A. Accumulation of heavy metals by potato and corn plants. Sci Herald Chernivtsy Univ. Biol. 1998b; 20(1): 77-83.
Seneviratne M., Rajakaruna N., Rizwan M. et al. Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review. Env. Geochem. Health. 2019; 41: 1813-1831. https://doi.org/10.1007/s10653-017-0005-8
Shahzad B., Fahad S., Tanveer M. et al. Plant responses and tolerance to salt stress. Approaches for enhancing abiotic stress tolerance in plants. CRC Press. 2019; 61-78.
Singh P., Singh I., Shah K. Reduced activity of nitrate reductase under heavy metal cadmium stress in rice: an in silico answer. Front. Plant Sci. 2019; 9: 1948. https://doi.org/10.3389/fpls.2018.01948
Su P., Yan J., Li W. et al. A member of wheat class III peroxidase gene family, TaPRX-2A, enhanced the tolerance of salt stress. BMC plant biology, 2020; 20: 1-15. https://doi.org/10.1186/s12870-020-02602-1
Sudo E., Itouga M., Yoshida-Hatanaka K. et al. Gene expression and sensitivity in response to copper stress in rice leaves. J. Exp. Botany. 2008; 59 (12): 3465-3474. https://doi.org/10.1093/jxb/ern196
Wang Y., Wang Q., Zhao Y. et al. Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response. Gene. 2015; 566: 95–108. https://doi.org/10.1016/j.gene.2015.04.041
Wu Y., Yang Z., How J. et al. Overexpression of a peroxidase gene (AtPrx64) of Arabidopsis thaliana in tobacco improves plant’s tolerance to aluminum stress. Plant Molec Biol. 2017; 95: 157–168. https://doi.org/10.1007/s11103-017-0644-2
Yazlovytska L.S., Rohozynskyi M.S., Kostyshin S.S., Volkov R.A. Effect of Cu2+ and Ni2+ on the intensity of RNA synthesis in corn seedlings. Ukr Biochem J. 1999; 71(1): 56-60.
Zhang L., Wu M., Yu D. et al. Identification of glutathione peroxidase (GPX) gene family in Rhodiola crenulata and gene expression analysis under stress conditions. Int. J. Mol. Sci. 2018; 19 (11): 3329. https://doi.org/10.3390/ijms19113329