Plant Soil Environ., 2024, 70(10):617-631 | DOI: 10.17221/66/2024-PSE
Alleviating cadmium toxicity in maize plants: role of glycine betaine in enhancing growth, photosynthetic efficiency, water status, and antioxidant defense mechanismOriginal Paper
- 1 Department of Biology, College of Sciences and Humanities, Prince Sattam Bin Abdulaziz University, Al-Kharj, Saudi Arabia
The issue of heavy metals (HMs) contamination poses a significant challenge in the environment, exerting a severe impact on the growth and productivity of crops. Cadmium (Cd) is specifically identified as the seventh heavy metal among the top 20 pollutants, primarily due to its elevated phytotoxicity and its solubility in water. In the current study, foliar application of glycine betaine (GB) (500 µmol) investigated the toxic effects of cadmium in maize plants subjected to two Cd concentrations (50 and 100 µmol) as CdCl2. The maize plants exposed to Cd stress exhibited a massive reduction in growth, biomass, photosynthetic pigments [chlorophyll a (Chl a), chlorophyll b (Chl b), carotenoids, and total pigments], gas exchange parameters [transpiration rate (Tr), net photosynthetic rate (Pn), intracellular CO2 concentration (ci), and stomatal conductance (gs)], relative water content (RWC), and organic osmolytes content [total soluble protein (TSS), and total soluble sugar (TSS)]. These impacts were significant with the 100 µmol CdCl2 treatment. Moreover, Cd led to remarked increase in proline, nonenzymatic antioxidants levels [ascorbic acid (AsA) and glutathione (GSH)] as well as the activity of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR). On the other hand, GB application efficiently relieved the Cd toxic impacts on maize and maintained higher growth criteria, gas exchange parameters, photosynthetic pigments, RWC, and organic osmolytes. In addition, the exogenous application of GB added more enhancement to the antioxidative system (enzymatic and nonenzymatic). These results imply that GB could significantly preserve maize growth under Cd toxicity conditions by maintaining photosynthetic characteristics, water status, and antioxidant system. This suggests an enhancement in the plant’s resilience to stress induced by heavy metals.
Keywords: Zea mays L.; environmental pollutants; water homeostasis; physiological parameters; stomatal behaviour; adaptation
Received: February 16, 2024; Revised: August 1, 2024; Accepted: August 5, 2024; Prepublished online: September 6, 2024; Published: September 23, 2024 Show citation
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References
- Abedi T., Mojiri A. (2020): Cadmium uptake by wheat (Triticum aestivum L.): an overview. Plants, 9: 500.
Go to original source...
Go to PubMed...
- Aebi H. (1984): Catalase in vitro. Methods in Enzymology, 105: 121-126.
Go to original source...
Go to PubMed...
- Ahmad R., Ali S., Abid M., Rizwan M., Ali B., Tanveer A., Ghani M.A. (2020): Glycine betaine alleviates the chromium toxicity in Brassica oleracea L. by suppressing oxidative stress and modulating the plant morphology and photosynthetic attributes. Environmental Science and Pollution Research, 27: 1101-1111.
Go to original source...
Go to PubMed...
- Ali S., Abbas Z., Seleiman M.F., Rizwan M., Yava I., Alhammad B.A., Ashwag A., Hasanuzzaman M., Kalderis D. (2020): Glycine betaine accumulation, significance, and interests for heavy metal tolerance in plants. Plants, 9: 896.
Go to original source...
Go to PubMed...
- Almuwayhi M.A. (2021): Effect of cadmium on the molecular and morphophysiological traits of Pisum sativum L. Biotechnology and Biotechnological Equipment, 35: 1374-1384.
Go to original source...
- Alyemeni M.N., Ahanger M.A., Wijaya L., Alam P., Bhardwaj R., Ahmad P. (2018): Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma, 255: 459-469.
Go to original source...
Go to PubMed...
- Amin F., Shah F., Ullah S., Shah W., Iftikhar Ahmed I., Ali B., Khan A.A., Malik T., Mustafa A.M.A. (2024): The germination response of Zea mays L. to osmotic potentials across optimal temperatures via halo-thermal time model. Science Reports, 14: 3225.
Go to original source...
Go to PubMed...
- Anwar S., Shafiq F., Nisa Z., Usman U., Ashraf M.Y., Ali N. (2021): Effect of cadmium stress on seed germination, plant growth and hydrolysing enzymes activities in mungbean seedlings. Journal of Seed Science, 43: e202143042.
Go to original source...
- Bayer W.F., Fridovich J.L. (1987): Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry, 161: 559-566.
Go to original source...
Go to PubMed...
- Bradford M.M. (1976): A rapid and sensitive method for quantitating microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
Go to original source...
- Chowardhara B., Borgohain P., Saha B., Awasthi J.P., Panda S.K. (2020): Differential oxidative stress responses in Brassica juncea (L.) Czern and Coss cultivars induced by cadmium at germination and early seedling stage. Acta Physiologiae Plantarum, 42: 105.
Go to original source...
- Daniel W.W. (1995): Biostatistics: A Foundation for Analysis in the Health Science. 6th Edition. New York, John Wiley and Sons.
- Elhakem A.H. (2020): Salicylic acid ameliorates salinity tolerance in maize by regulation of phytohormones and osmolytes. Plant, Soil and Environment, 66: 533-541.
Go to original source...
- Ellman G.L. (1959): Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82: 70-77.
Go to original source...
Go to PubMed...
- Foyer C.H., Halliwell B. (1976): The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta, 133: 21-25.
Go to original source...
Go to PubMed...
- Ghosh U.K., Islam Md.N., Siddiqui Md.N., Khan Md.A.R. (2021): Understanding the roles of osmolytes for acclimatizing plants to changing environment: a review of potential mechanism. Plant Signaling and Behavior, 16: e1913306.
Go to original source...
Go to PubMed...
- Guo J., Qin S., Rengel Z., Gao W., Nie Z., Liu H., Li C., Zhao P. (2019): Cadmium stress increases antioxidant enzyme activities and decreases endogenous hormone concentrations more in Cd-tolerant than Cd-sensitive wheat varieties. Ecotoxicology and Environmental Safety, 172: 380-387.
Go to original source...
Go to PubMed...
- Haider F.U., Liqun C., Coulter J.A., Cheema S.A., Wu J., Zhang R., Wenjun M., Farooq M. (2021): Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicology and Environmental Safety, 211: 111887.
Go to original source...
Go to PubMed...
- Hasanuzzaman M., Bhuyan M., Anee T.I., Parvin K., Nahar K., Mahmud J.A., Fujita M. (2019): Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants, 8: 384.
Go to original source...
Go to PubMed...
- He X., Richmond M.E.A., Williams D.V., Zheng W., Wu F. (2019): Exogenous glycinebetaine reduces cadmium uptake and mitigates cadmium toxicity in two tobacco genotypes differing in cadmium tolerance. International Journal of Molecular Sciences, 31: 1612.
Go to original source...
Go to PubMed...
- Kumar K., Singh J., Singh B.R., Chandra S., Chauhan N., Yadav M.K., Pankaj Kumar P. (2022): Consumption and processing patterns of maize (Zea mays): a review. The Pharma Innovation Journal, 11: 51-57.
- Kumar P. (2021): Soil applied glycine betaine with arbuscular mycorrhizal fungi reduces chromium uptake and ameliorates chromium toxicity by suppressing the oxidative stress in three genetically different sorghum (Sorghum bicolor L.) cultivars. BMC Plant Biology, 21: 336.
Go to original source...
Go to PubMed...
- Lee M.R., Kim C.S., Park T., Choi Y.S., Lee K.H. (2018): Optimization of the ninhydrin reaction and development of a multiwell plate-based highthroughput proline detection assay. Analytical Biochemistry, 556: 57-62.
Go to original source...
Go to PubMed...
- Lichtenthaler H., Wellburn A. (1983): Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11: 591-592.
Go to original source...
- Lowry O.H., Rosebraugh N.S., Farrand A.L., Randall R.J. (1951): Protein measurement with folin phenol reagent. Journal of Biological Chemistry, 193: 263-275.
Go to original source...
- Marques D.N., Carvalho M.E.A., Piotto F.A., Batagin-Piotto K.D., Nogueira M.L., Gaziola S.A., Azevedo R.A. (2019): Antioxidant defense response in plants to cadmium stress. In: Hasanuzzaman M., Prasad M.N.V., Nahar L. (eds.): Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches. New York, Academic Press, 423-461.
Go to original source...
- Mukherjee S.P., Choudhuri M.A. (1983): Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in vigna seedlings. Physiologia Plantarum, 58: 166-170.
Go to original source...
- Nakano Y., Asada K. (1981): Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22: 867-880.
- Riyazuddin R., Nisha N., Ejaz B., Khan M.I.R., Kumar M., Ramteke P.W., Gupta R.A. (2022): Comprehensive review on the heavy metal toxicity and sequestration. Plants Biomolecules, 12: 43.
Go to original source...
Go to PubMed...
- Sadeghipour O. (2018): Enhancing cadmium tolerance in common bean plants by potassium application. The Philippine Agricultural Scientist, 101: 167-175.
- Sadeghipour O. (2020): Cadmium toxicity alleviates by seed priming with proline or glycine betaine in cowpea (Vigna unguiculata (L.) Walp.). Egyptian Journal of Agronomy, 42: 163-170.
Go to original source...
- Schonfeld M.A., Johnson R.C., Carver B.F., Mornhinweg D.W. (1988): Water relations in winter wheat as drought resistance indicators. Crop Sciences, 28: 526-531.
Go to original source...
- Seifikalhor M., Aliniaeifard S., Bernard F., Seif M., Latifi M., Hassani B., Didaran F., Bosacchi M., Rezadoost H., Li T. (2020): γ-aminobutyric acid confers cadmium tolerance in maize plants by concerted regulation of polyamine metabolism and antioxidant defense systems. Scientific Reports, 10: 3356.
Go to original source...
Go to PubMed...
- Sharma A., Shahzad B., Kumar V., Kohli S.K., Sidhu G.P.S., Bali A.S., Handa N., Kapoor D., Bhardwaj R., Zheng B. (2019): Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules, 9: 285-320.
Go to original source...
Go to PubMed...
- Tiwari S., Lata C. (2018): Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Frontiers in Plant Science, 9: 452.
Go to original source...
Go to PubMed...
- Ullah S., Khan J.K., Elateeq A.A., Salam U., Yu B., Ma Y., Wang H., Tang Z.-H. (2020): Comparative study of growth, cadmium accumulation and tolerance of three chickpea (Cicer arietinum L.) cultivars. Plants, 9: 310.
Go to original source...
Go to PubMed...
- Woodis T.C., Hunter G.B., Johnson F.J. (1977): Statistical studies of matrix effects on the determination of cadmium and lead in fertilizer materials and plant tissue by flameless atomic absorption spectrometry. Analytica Chimica Acta, 90: 127-136.
Go to original source...
- Yoshida S., Forno D.A., Cock J.K., Gomez K.A. (1976): Laboratory Manual for Physiological Studies of Rice. Los Banos, International Rice Research Institute.
- Zhang G., Ba Q., Chen S., Liu F., Li G. (2020): Exogenous application of glycine betaine alleviates cadmium toxicity in super black waxy maize by improving photosynthesis, the antioxidant system and glutathione-ascorbic acid cycle metabolites. Cereal Research Communications, 48: 449-458.
Go to original source...
- Zhao H., Guan J., Liang Q., Zhang X., Hu H., Zhang J. (2021): Effects of cadmium stress on growth and physiological characteristics of sassafras seedlings. Scientific Reports, 11: 9913.
Go to original source...
Go to PubMed...
- Zulfiqar U., Jiang W., Xiukang W., Hussain S., Ahmad M., Maqsood M.F., Ali N., Ishfaq M., Kaleem M., Haider F.U., Farooq N., Naveed M., Kucerik J., Brtnicky M., Mustafa A. (2022): Cadmium phytotoxicity, tolerance, and advanced remediation approaches in agricultural soils; a comprehensive review. Frontiers in Plant Science, 13: 773815.
Go to original source...
Go to PubMed...
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