Role of antioxidative defense system in amelioration of cadmium-induced phytotoxic effects in germinating seeds of maize (Zea mays)
Aamer Abbas A , Muhammad Sajid Aqeel Ahmad A * , Muhammad Ashraf A , Qasim Ali B and Ambreen Khadija Alvi CA Department of Botany, University of Agriculture, Faisalabad 38000, Pakistan.
B Department of Botany, Government College University, Faisalabad 38000, Pakistan.
C Department of Botany, Government College Women University, Faisalabad 38000, Pakistan.
Crop & Pasture Science 73(5) 599-613 https://doi.org/10.1071/CP21329
Submitted: 12 May 2021 Accepted: 24 August 2021 Published: 22 December 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Anthropogenic activities are increasing Cd concentration in soil and environment that limits seed germination capacity and causes poor seedling establishment.
Aims: The effect of different Cd concentrations on seed germination and seedling growth of two maize cultivars (C-20 and EV-1098) was tested in this study.
Methods: Maize seeds were sown in Petri dishes lined with double filter paper. The seedlings were grown in a growth chamber, applied with different Cd concentrations (0, 2, 4, 6, 8 and 10 μM), and harvested 12 days after germination.
Key results: Seeds applied with higher levels of Cd showed a significant decrease in seed germination percentage (GP), seed emergence index (EI) and germination energy (GE). A significant delay in seed germination was observed at the highest Cd treatment in terms of increased mean emergence time (MET), days to 50% germination (T50) and coefficient of uniformity of emergence (CUE). A marked decline in leaf K, Ca, Na, and P was observed, whereas root K, Ca and P increased with an increase in external Cd concentration. The roots and leaves of maize C-20 showed greater activities of superoxide dismutase (SOD) than did those of EV-1098. In contrast, peroxidase (POD) activity was reasonably high in roots and leaves, whereas catalase (CAT) was high only in roots of EV-1098. Non-enzymatic antioxidants such as phenolics and ascorbicacid (AsA) also significantly increased, accompanied with substantially lowermalondialdehyde (MDA) contents in the roots and leaves of EV-1098 than of C-20.
Conclusions: The differential modulation of the activities of enzymatic and non-enzymaticanti-oxidative defense system in roots and leaves played a critical role intolerance of both cultivars to Cd stress.
Implications: The findings of this study are helpful in improving seed germination capacity and seedling growth of maize in Cd contaminated soils.
Keywords: ascorbic acid, cadmium, enzymatic anti-oxidants, MDA, non-enzymatic anti-oxidants, phenols, seed germination, seedling growth.
References
Ackova GD (2018) Heavy metals and their general toxicity on plants. Plant Science Today 5, 15–19.| Heavy metals and their general toxicity on plants.Crossref | GoogleScholarGoogle Scholar |
Anjum SA, Tanveer M, Hussain S, Shahzad B, Ashraf U, Fahad S, Hassan W, Jan S, Khan I, Saleem MF, Bajwa AA, Wang L, Mahmood A, Samad RA, Tung SA (2016) Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environmental Science and Pollution Research 23, 11864–11875.
| Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress.Crossref | GoogleScholarGoogle Scholar | 26957429PubMed |
Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252, 399–413.
| Minimising toxicity of cadmium in plants—role of plant growth regulators.Crossref | GoogleScholarGoogle Scholar | 25303855PubMed |
Association of Official Seed Analysts (1990) Rules for testing seeds. Journal of Seed Technology 12, 1–112.
Azcue JM (1996) Comparison of different cleaning procedures of root material for analysis of trace elements. International Journal of Environmental Analytical Chemistry 62, 137–145.
| Comparison of different cleaning procedures of root material for analysis of trace elements.Crossref | GoogleScholarGoogle Scholar |
Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212, 696–709.
| Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth.Crossref | GoogleScholarGoogle Scholar | 11346943PubMed |
Bavi K, Kholdebarin B, Moradshahi A (2011) Effect of cadmium on growth, protein content and peroxidase activity in pea plants. Pakistan Journal of Botany 43, 1467–1470.
Bewley JD, Black M (1985) ‘Seeds: physiology of development and germination.’ (Plenum Press)
Cakmak I, Horst WJ (1991) Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83, 463–468.
| Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar |
Chance B, Maehly AC (1955) Assay of catalases and peroxidases.. In ‘Methods of Biochemical Analysis. Vol. 1’. (Ed. D Glick) pp. 764–775. (Interscience Publishers)
| Crossref |
Chaudhary S, Sharma YK (2009) Interactive studies of potassium and copper with cadmium on seed germination and early seedling growth in maize (Zea mays L.). Journal of Environmental Biology 30, 427–432.
Chen L, Long C, Wang D, Yang J (2020) Phytoremediation of cadmium (Cd) and uranium (U) contaminated soils by Brassica juncea L. enhanced with exogenous application of plant growth regulators. Chemosphere 242, 125112.
| Phytoremediation of cadmium (Cd) and uranium (U) contaminated soils by Brassica juncea L. enhanced with exogenous application of plant growth regulators.Crossref | GoogleScholarGoogle Scholar | 31669993PubMed |
Ciećko Z, Kalembasa S, Wyszkowski M, Rolka E (2004) Effect of soil contamination by cadmium on potassium uptake by plants. Polish Journal of Environmental Studies 13, 333–337.
Coolbear P, Francis A, Grierson D (1984) The effect of low temperature pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds. Journal of Experimental Botany 35, 1609–1617.
| The effect of low temperature pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds.Crossref | GoogleScholarGoogle Scholar |
Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. Journal of Plant Physiology 165, 600–611.
| Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars.Crossref | GoogleScholarGoogle Scholar | 17728009PubMed |
Ellis RH, Roberts EH (1981) The quantification of aging and survival in orthodox seeds. Seed Science and Technology 9, 373–409.
Faizan S, Kausar S, Perveen R (2011) Varietal differences for cadmium-induced seedling mortality, foliar toxicity symptoms, plant growth, proline and nitrate reductase activity in chickpea (Cicer arietinum L.). Biology and Medicine 3, 196–206.
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
| Superoxide dismutases: I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |
Gupta D Gupta D (2011) Toxicity of copper and cadmium on germination and seedling growth of maize (Zea mays L.) seeds. Indian Journal of Scientific Research 2, 67–70.
Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjun M, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicology and Environmental Safety 211, 111887.
| Cadmium toxicity in plants: impacts and remediation strategies.Crossref | GoogleScholarGoogle Scholar |
He J-y, Ren Y-f, Zhu C, Jiang D-a (2008) Effects of cadmium stress on seed germination, seedling growth and seed amylase activities in rice (Oryza sativa). Rice Science 15, 319–325.
| Effects of cadmium stress on seed germination, seedling growth and seed amylase activities in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |
Huang D, Gong X, Liu Y, Zeng G, Lai C, Bashir H, Zhou L, Wang D, Xu P, Cheng M, Wan J (2017) Effects of calcium at toxic concentrations of cadmium in plants. Planta 245, 863–873.
| Effects of calcium at toxic concentrations of cadmium in plants.Crossref | GoogleScholarGoogle Scholar |
Jackson ML (1962) ‘Soil chemical analysis’, (Constable and Co. Ltd.)
Jain M, Pal M, Gupta P, Gadre R (2007) Effect of cadmium on chlorophyll biosynthesis and enzymes of nitrogen assimilation in greening maize leaf segments: role of 2-oxoglutarate. Indian Journal of Experimental Biology 45, 385–389.
Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. Journal of Agricultural and Food Chemistry 33, 213–217.
| Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics.Crossref | GoogleScholarGoogle Scholar |
Kasuba V, Rozgaj R (2000) Biological effects of cadmium. Periodicum Biologorum 102, 365–371.
Kibria MG, Osman KT, Ahmed MJ (2006) Cadmium and lead uptake by rice (Oryza sativa L.) grown in three different textured soils. Soil and Environment 25, 70–77.
Li X, Zhou Q, Sun X, Ren W (2016) Effects of cadmium on uptake and translocation of nutrient elements in different welsh onion (Allium fistulosum L.) cultivars. Food Chemistry 194, 101–110.
| Effects of cadmium on uptake and translocation of nutrient elements in different welsh onion (Allium fistulosum L.) cultivars.Crossref | GoogleScholarGoogle Scholar |
Liu Y-T, Chen Z-S, Hong C-Y (2011a) Cadmium-induced physiological response and antioxidant enzyme changes in the novel cadmium accumulator, Tagetes patula. Journal of Hazardous Materials 189, 724–731.
| Cadmium-induced physiological response and antioxidant enzyme changes in the novel cadmium accumulator, Tagetes patula.Crossref | GoogleScholarGoogle Scholar |
Liu ZL, Chen W, He XY (2011b) Cadmium-induced changes in growth and antioxidative mechanisms of a medicine plant (Lonicera japonica Thunb.). Journal of Medicinal Plants Research 5, 1411–1417.
Malekzadeh P, Khara J, Farsshian S, Jamal-Abad AK, Rahmatzadeh S (2007) Cadmium toxicity in maize seedlings: changes in antioxidant enzyme activities and root growth. Pakistan Journal of Biological Sciences 10, 127–131.
| Cadmium toxicity in maize seedlings: changes in antioxidant enzyme activities and root growth.Crossref | GoogleScholarGoogle Scholar |
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies 15, 523–530.
Morkunas I, Woźniak A, Mai VC, Rucińska-Sobkowiak R, Jeandet P (2018) The role of heavy metals in plant response to biotic stress. Molecules 23, 2320.
| The role of heavy metals in plant response to biotic stress.Crossref | GoogleScholarGoogle Scholar |
Mukherjee SP, Choudhuri MA (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.
| Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings.Crossref | GoogleScholarGoogle Scholar |
Onaga G, Wydra K (2016) Advances in plant tolerance to abiotic stresses. In ‘Plant genomics. Vol. 2’. (Ed. IY Abdurakhmonov) 1229–272. (IntechOpen)
| Crossref |
Ozturk L, Eker S, Ozkutlu F (2003) Effect of cadmium on growth and concentrations of cadmium, ascorbic acid and sulphydryl groups in durum wheat cultivars. Turkish Journal of Agriculture 27, 161–168.
Pal M, Horvath E, Janda T, Paldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. Journal of Plant Nutrition and Soil Science 169, 239–246.
| Physiological changes and defense mechanisms induced by cadmium stress in maize.Crossref | GoogleScholarGoogle Scholar |
Prasann K, Johnson Y, Kumar P, Lamneivah M, Nada J, Mohit N, Sunil K, Mandala H (2018) Cadmium induced changes in germination of maize seed treated with mycorrhiza. Annals of Agricultural and Biological Research 23, 169–170.
Ruan S, Xue Q, Tylkowska K (2002) Effects of priming on germination and health of rice (Oryza sativa L.) seeds. Seed Science and Technology 30, 451–458.
Shahid M, Dumat C, Khalid S, Niazi NK, Antunes PMC (2016) Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. In ‘Reviews of environmental contamination and toxicology. Vol. 241’. (Eds FA Gunther, P de Voogt) pp. 73–137. (Springer)
| Crossref |
Shanmugaraj BM, Malla A, Ramalingam S (2019) Cadmium stress and toxicity in plants: an overview. In ‘Cadmium toxicity and tolerance in plants’. (Eds M Hasanuzzaman, MNV Prasad, M Fujita) pp. 1–17. (Academic Press)
| Crossref |
Sharma RK, Agrawal M (2005) Biological effects of heavy metals: an overview. Journal of Environmental Biology 26, 301–313.
Sharma H, Rawal N, Mathew BB (2015) The characteristics, toxicity and effects of cadmium. International Journal of Nanotechnology and Nanoscience 3, 1–9.
Šimonová E, Henselová M, Masarovičová E, Kohanová J (2007) Comparison of tolerance of Brassica juncea and Vigna radiata to cadmium. Biologia Plantarum 51, 488–492.
| Comparison of tolerance of Brassica juncea and Vigna radiata to cadmium.Crossref | GoogleScholarGoogle Scholar |
Szőllősi R, Varga IS, Erdei L, Mihalik E (2009) Cadmium-induced oxidative stress and antioxidative mechanisms in germinating Indian mustard (Brassica juncea L.) seeds. Ecotoxicology and Environmental Safety 72, 1337–1342.
| Cadmium-induced oxidative stress and antioxidative mechanisms in germinating Indian mustard (Brassica juncea L.) seeds.Crossref | GoogleScholarGoogle Scholar |
Takarina ND, Pin TG (2017) Bioconcentration factor (BCF) and translocation factor (TF) of heavy metals in mangrove trees of Blanakan fish farm. Makara Journal of Science 21, 77–81.
| Bioconcentration factor (BCF) and translocation factor (TF) of heavy metals in mangrove trees of Blanakan fish farm.Crossref | GoogleScholarGoogle Scholar |
Tipu MI, Ashraf MY, Sarwar N, Akhtar M, Shaheen MR, Ali S, Damalas CA (2020) Growth and physiology of maize (Zea mays L.) in a nickel-contaminated soil and phytoremediation efficiency using EDTA. Journal of Plant Growth Regulation 40, 774–786.
| Growth and physiology of maize (Zea mays L.) in a nickel-contaminated soil and phytoremediation efficiency using EDTA.Crossref | GoogleScholarGoogle Scholar |
Wang Z, Zhang Y, Huang Z, Huang L (2008) Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant and Soil 310, 137.
| Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress.Crossref | GoogleScholarGoogle Scholar |
Wang F, Chu R, Yang J, Gong Y, Zhu X, Zhu C, Xu L, He X, Liu L, IEEE (2009) Cadmium accumulation and antioxidant enzyme activity in response to cadmium stress in radish (Raphanus sativus L.). In ‘3rd International conference on bioinformatics and biomedical engineering. Vols. 1–11’. pp. 4545–4548. (IEEE Engineering in Medicine and Biology Society: Piscataway, NJ, USA)
Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Communications in Soil Science and Plant Analysis 13, 1035–1059.
| A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status.Crossref | GoogleScholarGoogle Scholar |
Wu F-B, Chen F, Wei K, Zhang G-P (2004) Effect of cadmium on free amino acid, glutathione and ascorbic acid concentrations in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance. Chemosphere 57, 447–454.
| Effect of cadmium on free amino acid, glutathione and ascorbic acid concentrations in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi C, Takimoto Y, Ohkama-Ohtsu N, Hokura A, Shinano T, Nakamura T, Suyama A, Maruyama-Nakashita A (2016) Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana. Plant and Cell Physiology 57, 2353–2366.
| Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Yang J, Liu L, Gong Y, He L, Li X, Chen L (2008) Cadmium uptake character and stress effect on the growth and antioxidant enzymes activities in Raphanus sativus. In ‘Proceedings of the international symposium on sustainability through integrated and organic horticulture’. (Eds RK Prange, SD Bishop) pp. 249–255. (International Society for Horticultural Science, Leuven Publication: Belgium)
| Crossref |