Abstract
The present study was aimed to reveal the effect of cadmium (Cd)-polluted soil on the activation of antioxidant enzymes, photosynthesis, pigments, water relation, and other biochemical traits and comparative effect of synthetic and organic chelators. A pot experiment was conducted using two maize varieties grown in Cd-contaminated (15 and 30 mg kg−1) soil and chelators (1 mM EDTA, and 1 mM citric acid). Cd decreased biomass and photosynthetic traits while increased malondialdehyde (MDA) contents, total proteins, and antioxidant enzyme activities. Addition of EDTA enhanced Cd uptake, antioxidative enzyme, and total proteins; however, it reduced the water, osmotic, and turgor potential as compared to Cd alone. Addition of citric acid has lessened the antioxidant enzyme activities and MDA contents and enhanced the plant biomass as compared to Cd alone. Increases in antioxidants and MDA content were found to be positively related to the Cd contents in shoot and root. The application of citric acid significantly alleviated the Cd-induced toxic effects, showing remarkable improvement in biomass. These results indicated that EDTA was more effective for mobilizing Cd from soil to the root and shoot than citric acid; however, the physiological traits and plant biomass were more strongly inhibited by EDTA than by the Cd. Our study implies that citric acid ameliorated the negative effect of Cd on physiological traits and biomass, and hence could be used effectively for Cd phytoextraction.
Similar content being viewed by others
References
Al-Hakimi AMA (2007) Modification of cadmium toxicity in pea seedlings by kinetin. Plant Soil Environ 53:129–135
Anamika S, Eapen S, Fulekar MH (2009) Phytoremediation of cadmium, lead and zinc by Brassica juncea L. Czern and Coss. J Appl Biosci 13:726–736
Anwar S, Khan S, Ashraf MY, Baloch SU, Zafar S, Noman A (2016a) Impact of chelators induced phytoextraction of cadmium on yield and ionic uptake of maize. Int J Phytoremed 19:505–513
Anwar S, Nawaz MF, Gul S, Rizwan M, Ali S, Kareem A (2016b) Uptake and distribution of minerals and heavy metals in commonly grown leafy vegetable species irrigated with sewage water. Environ Monit Assess 188:541. https://doi.org/10.1007/s10661-016-5560-4
Arnon DI (1949) Copper enzymes in isolated chloroplast. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
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
Bashir W, Anwar S, Zhao Q, Hussain I, Xie F (2019) Interactive effect of drought and cadmium stress on soybean root morphology and gene expression. Ecotoxicol Environ Saf 175:90–101
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Bernard A (2008) Cadmium & its adverse effects on human health. Indian J Med Res 128(4):557–564
Bhardwaj P, Chaturrvedi AK, Prasad P (2009) Effect of enhanced lead and cadmium in soil on physiological and biochemical attributes of Phaseolus vulgaris L. Nat Sci 7:63–75
Bi Y, Chen W, Zhang W, Zhou Q, Yun L, Xing D (2009) Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium-induced cell death in Arabidopsis thaliana. Biol Cell 101:629–643
Bouchard RA, Yang Z, Greyson RI, Walden DB (2004) Zinc and cadmium induction of small heat shock gene transcripts in maize seedlings. Maydica 49:105–114
Carmo JD, Araujo TD, Nascimento CWAD (2010) Phytoextraction of lead from soil from a battery recycling site: the use of citric acid and NTA. Water Air Pollut 211:113–120
Chaffei C, Paqeau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to metabolism safeguard through an amino acid storage strategy. Plant Cell Physiol 45:1681–1693
Chance B, Maehly AC (1955) Assay of catalase and peroxidase. Methods Enzymol 2:764–775
Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Bot Stud 52:41–46
Cheng S, Ren F, Grosse W, Wu Z (2002) Effects of cadmium on chlorophyll content, photochemical efficiency, and photosynthetic intensity of Canna indica Linn. Int J Phytoremed 4:239–246
Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99
Davies BH (1976) Carotenoids, in: Goodwin, T.W. (Ed.), chemistry and biochemistry of plant pigments, London, pp. 38-165
Deng X, Xia Y, Hu W, Zhang H, Shen Z (2010) Cadmium induced oxidative damage and protective effects of N-acetyl-L-cysteine against cadmium toxicity in Solanum nigrum L. J Hazard Mater 180:722–729
Dinakar N, Nagajyothi PC, Suresh S, Damodharam T, Suresh C (2009) Cadmium induced changes on proline, antioxidant enzymes, and nitrite and nitrate reductase in Arachis hypogaea L. J Environ Biol 30:289–294
Dixit P, Mukherjee PK, Ramachandran V, Eapen S (2011) Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6(1):e16360
Dong J, Wu FB, Zhang GP (2005) Effect of cadmium on growth and photosynthesis of tomato seedlings. J Zhejiang Univ (Sci) 6B:974–980
Dunwei C, Jiang D, Dai T, Jing Q, Cao W (2009) Effects of cadmium on plant growth and physiological traits in contrast wheat recombinant inbred lines differing cadmium tolerance. Chemosphere 77:1620–1625
Ederli L, Reale L, Ferranti L, Pasqualini S (2004) Responses induced by high concentration of cadmium in Phragmites australis roots. Plant Physiol 121:66–74
Ehsan S, Ali S, Noureen S, Mahmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol Environ Saf 106:164–172
Esfandiari E, Shekari F, Shekari F, Esfandiari M (2007) The effect of salt stress on antioxidant enzymes’ activity and lipid peroxidation on the wheat seedling. Not Bot Hort Agrobot Cluj 35(1):48–56
Farid M, Ali S, Ishaque W, Shakoor MB, Niazi NK, Bibi I, Dawood M, Gill RA, Abbas F (2015) Exogenous application of ethylenediamminetetraacetic acid enhanced phytoremediation of cadmium by Brassica napus L. Int J Environ Sci Technol 12:3981–3992
Farouk S, Mosa AA, Taha AA, Ibrahim HM, El-Gahmery AM (2011) Protective effect of humic acid and chitosan on radish (Raphanus sativus, L. var. sativus) plants subjected to cadmium stress. J Stress Physiol Biochem 7:99–116
Geneva MM, Petrov P, Boychinova M, Lazarova I, Todorov I, Stancheva I (2013) EDTA reduces heavy metal impacts on Tribulus terrestris photosynthesis and antioxidants. Russ J Plant Physiol 60:623–632
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314
Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants. Plant Signal Behav 6:215–222
Gillet S, Decottignies P, Chardonnet S, Le Maréchal P (2006) Cadmium response and redoxin targets in Chlamydomonas reinhardtii: a proteomic approach. Photosynth Res 89:201–211
Greger M, Johansson M (2006) Cadmium effects on leaf transpiration of sugar beet (Beta vulgaris). Physiol Plant 86:465–473
Guo H, Hong C, Chen X, Xu Y, Liu Y, Jiang D, Zheng B (2016) Different growth and physiological responses to cadmium of the three miscanthus species. PLoS One 11(4):e0153475. https://doi.org/10.1371/journal.pone.0153475
Guo P, Li Q, Qi YP, Yang LT, Ye X, Chen HH, Chen LS (2017) Sulfur-mediated-alleviation of aluminum-toxicity in Citrus grandis seedlings. Int J Mol Sci 18(12):2570
Guo P, Qi YP, Cai YT, Yang TY, Yang LT, Huang ZR, Chen LS (2018) Aluminum effects on photosynthesis, reactive oxygen species and methylglyoxal detoxification in two Citrus species differing in aluminum tolerance. Tree Physiol 38(10):1548–1565
Habiba U, Ali S, Farid M, Shakoor MB, Rizwan M, Ibrahim M, Abbasi GH, Hayat T, Ali B (2015) EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environ Sci Pollut Res 22:1534–1544
Hajduch M, Rakwal R, Agrawal GK, Yonekura M, Pretova A (2001) High-resolution two dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/ fragmentation of ribulose-1,5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electrophoresis 22:2824–2831
Hamilton PB, Van Slyke DD (1943) The gasometric determination of free amino acids in blood filtrate by the ninhydrin-carbon dioxide method. J Biol Chem 150:231–250
Haroun SA, Aldesuquy HS, Abo-Hamed SA, El-Said AA (2003) Kinetin-induced modification in growth criteria, ion contents and water relations of sorghum plants treated with cadmium chloride. Acta Bot Hungar 45:113–126
Hashem A, Abd_Allah EF, Alqarawi AA, Malik JA, Wirth S, Egamberdieva D (2016) Role of calcium in AMF-mediated alleviation of the adverse impacts of cadmium stress in Bassia indica [Wight] AJ Scott. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2016.11.003
Hong-xia X, Xiao-yan W, Wei-hua M, Yong Y (2005) Effects of cadmium stress on photosynthesis, chlorophyll fluorescence characteristics and excitation energy distribution in leaves of rice. Chin J Rice Sci 19:338–342
Hsu YT, Kao CH (2003) Changes in protein and amino acid contents in two cultivars of rice seedlings with different apparent tolerance to cadmium. Plant Growth Regul 40:147–155
Ingwersen J, Streck T (2005) A regional-scale study on the crop uptake of cadmium from sandy soils: measurement and modeling. J Environ Qual 34:1026–1035
Irfan M, Ahmad A, Hayat S (2014) Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21(2):125–131
Januškaitienė I (2010) Impact of low concentration of cadmium on photosynthesis and growth of pea and barley. Environ Res Engineering Manag 3:24–29
Januškaitienė I (2012) The effect of cadmium on several photosynthetic parameters of pea (Pisum sativum L.) at two growth stages. Zemdirbyste-Agriculture 99:71–76
Kasim WA (2005) The correlation physiological and structural alterations induced by copper and cadmium stress in broad beans (Vicia faba L.). Egypt J Biol 7:20–32
Kholodova V, Volkov K, Abdeyeva A, Kuznetsov V (2011) Water status in Mesembryanthemum crystallinum under heavy metal stress. Environ Exp Bot 71:382–389. https://doi.org/10.1016/j.envexpbot.2011.02.007
Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353
Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674
Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200:241–250
Larbi A, Morales F, Abadia A, Gogorcena Y, Lucena JJ, Abadia J (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition. Funct Plant Biol 29:1453–1464
Lefevre I, Marshal G, Ghanem ME, Correal E, Lutts S (2010) Cadmium has contrasting effects on polyethylene glycol-sensitive and resistant lines in the Mediterranean halophytes Atriplex halimus L. J Plant Physiol 167:365–374
Lesko K, Stefanovits-Bányai É, Simon-Sarkadi L (2002) Effect of magnesium on free amino acid and polyamine content in wheat seedlings exposed to cadmium. Acta Biologica Szegediensis 46:109–111
Ling T, Gao Q, Du H, Zhao Q, Ren J (2017) Growing, physiological responses and Cd uptake of corn (Zea mays L.) under different Cd supply. Chem Speciat Bioavailab 29(1):216–221
Lopez-Millan A, Sagardoy R, Solanas M, Abadia A, Abadia J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65:376–385
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Lu LL, Tian SK, Yang XE, Peng HY, Li TQ (2013) Improved cadmium uptake and accumulation in the hyperaccumulator Sedum alfredii: the impact of citric acid and tartaric acid. J Zhejiang Univ Sci B 14:106–114. https://doi.org/10.1631/jzus.B1200211
Markovska Y, Geneva M, Petrov P, Boychinova M, Lazarova I, Todorov I, Stancheva I (2013) EDTA reduces heavy metal impacts on Tribulus terrestris photosynthesis and antioxidants. Russ J Plant Physiol 60(5):623–632
Meers E, Hopgood M, Lesage E, Vervaeke P, Tack FGM, Verloo M (2004) Enhanced phytoremediation: in search of EDTA alternatives. Int J Phytorem 6:95–100
Mihailovic N (2010) Growth and ion uptake in maize plants exposed to Pb, Cd and Ni depend on NO3 −/NH4 + ratio. Bot Serb 34:15–20
Mysliwa-Kurdziel B, Prasad MNV, Strzabka K (2004) Photosynthesis in metal stressed plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems, 2nd edn. Springer-Verlag, Heidelberg, pp 146–181
Najeeb U, Jilanic G, Alia S, Sarward M, Xua L, Zhoua W (2011) Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574
Nakamura S, Akiyama C, Sasaki T, Hattori H, Chino M (2008) Effect of cadmium on the chemical composition of xylem exudates from oilseed rape plants (Brassica napus L.). Soil Sci Plant Nutr 54:118–127
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Neelu MK, Tomar M, Bhatnagar AK (2000) Influence of cadmium on growth and development of Vicia faba Linn. Indian J Exp Biol 38:819–823
Niu Z, Sun L, Sun T, Li Y, Wang H (2007) Evaluation of phytoextracting cadmium and lead by sunflower, ricinus, alfalfa and mustard in hydroponic culture. J Environ Sci 19(8):961–967
Nocito FF, Lancilli C, Dendena B, Lucchini G, Sacchi GA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34(6):994–1008
Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45. https://doi.org/10.1186/1999-3110-54-45
Paynel F, Schaumann A, Arkoun M, Douchiche O, Morvan C (2009) Temporal regulation of cell-wall pectin methylesterase and peroxidase isoforms in cadmium-treated flax hypocotyls. Ann Bot 104:1363–1372
Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960. https://doi.org/10.1073/pnas.97.9.4956
Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex steudel. Plant Physiol 133:829–837
Romero-Puertas MC, Palma JM, Go’mez M, Rio LA, del Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686
Romero-Puertas MC, Rodriguez-Serrano M, Corpas FJ, Gomez M, Del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2*- and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134
Rucińska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38(11):257
Sadiq R, Maqbool N, Haseeb M (2017) Ameliorative effect of chelating agents on photosynthetic attributes of Cd stressed sunflower. Agric Sci 8(02):149–160
Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126
Sapundjieva K, Kartalska Y, Vassilev A, Krastev S, Kuzmanova Y (2003) Effects of EDTA on metal solubility in the soil, metal uptake and performance of maize plants, and soil microorganisms. Bulg J Agric Sci 9:1–5
Sarangthem J, Jain M, Gadre R (2011) Inhibition of δ-aminolevulinic acid dehydratase activity by cadmium in excised etiolated maize leaf segments during greening. Plant Soil Environ 57(7):332–337
Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by micorrhization. J Exp Bot 53:1351–1365
Shahrtash M, Mohsenzadeh S, Zare H, Mohabatkar H (2011) Role of calcium in alleviation of cadmium toxicity in maize seedlings. Elec J Environ Agric Food Chem 10:2404–2412
Shilev S, Naydenov M, Tahsin N, Sancho ED, Benlloch M, Vancheva V, Sapundjieva K, Kuzmanova J (2007) Effects of easily biodegradable amendments on heavy metal solubilization and accumulation in technical crops- a field trial. J Environ Eng Landsc Manag 4:237–242
Sigfridsson KGV, Bernat G, Mamedov F, Styring S (2004) Molecular interference of Cd2+ with photosystem II. Biochem Biophys Acta 1659:19–31
Singh PK, Tewari RK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–112
Singh S, Khan NA, Nazar R, Anjum NA (2008) Photosynthetic traits and activities of antioxidant enzymes in black gram (Vigna mungo L. Hepper) under cadmium stress. Amer J Plant Physiol 3:25–32
Skrebsky EC, Tabaldi LA, Pereira LB, Rauber R, Maldaner J, Cargnelutti D, Goncalves JF, Castro GY, Shetinger MRC, Nicoloso FT (2008) Effect of cadmium on growth, micronutrient concentration, and δ-aminolevulinic acid dehydratase and acid phosphatase activities in plants of Pfaffia glomerata. Braz Society Plant Physiol 20:285–294
Song Y, Jin L, Wang X (2017) Cadmium absorption and transportation pathways in plants. Int J Phytorem 19(2):133–141
Srivastava R, Khan R, Nasim SA, Manzoor N, Mahmooduzzafar (2011) Cadmium treatment alters phytochemical and biochemical activity in Glycine max. L. Int J Bot 7:305–309
Suthar V, Memon KS, Mahmood-Ul-Hassan M (2014) EDTA-enhanced phytoremediation of contaminated calcareous soils: heavy metal bioavailability, extractability, and uptake by maize and sesbania. Environ Monit Assess 186:3957–3968
Touiserkani T, Haddad R (2012) Cadmium-induced stress and antioxidative responses in different Brassica napus cultivars. J Agric Sci Technol 14:929–937
Veselov, D., Kudoyarova, G., Symonyan, M., Veselov, S., 2003. Effect of cadmium on ion uptake, transpiration and cytokinin in wheat seedlings. Bulg J Plant Physiol Special issue, 353–359
Wang H, Zhao SC, Liu RL, Zhou W, Jin JY (2009) Changes of photosynthetic activities of maize (Zea mays L.) seedlings in response to cadmium stress. Photosynthetica 47:277–283
Wuana RA, Okieimen FA, Imborvungu JA (2010) Removal of heavy metals from a contaminated soil using organic chelating acids. Int J Environ Sci Technol 7:485–496
Xie Y, Hu L, Du Z, Sun X, Amombo E, Fan J, Fu J (2014) Effects of cadmium exposure on growth and metabolic profile of bermudagrass [Cynodon dactylon (L.) Pers.]. PLoS One 9(12):e115279
Xu W, Li Y, He J, Ma Q, Zhang X, Chen G, Wang H, Zhang H (2010) Cd uptake in rice cultivars treated with organic acids and EDTA. J Environ Sci 22:441–447
Xu Q, Min H, Cai S, Fu Y, Sha S, Xie K, Du K (2012) Subcellular distribution and toxicity of cadmium in Potamogeton crispus L. Chemosphere 89:114–1120. https://doi.org/10.1016/j.chemosphere.2012.04.046
Zhang F, Zhang H, Wang G, Xu L, Shen Z (2009) Cadmium induced accumulation of hydrogen peroxide in the leaf apoplast of Phaseolus aureus and Vicia sativa and the roles of different antioxidant enzymes. J Hazard Mater 168:76–84
Zhang X, Zhang S, Xu X, Li T, Gong G, Jia Y, Li Y, Deng L (2010) Tolerance and accumulation characteristics of cadmium in Amaranthus hybridus L. J Hazard Mater 180:303–308
Zhang, X., Zhong, B., Shafi, M., Guo, J., Liu, C., Guo, H., Peng, D., Wang, Y., Liu, D., 2018. Effect of EDTA and citric acid on absorption of heavy metals and growth of Moso bamboo. Environ Sci Poll Res 1-7. Doi.org/10.1007/s11356-018-2040-0
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Anwar, S., Khan, S., Hussain, I. et al. Chelators induced uptake of cadmium and modulation of water relation, antioxidants, and photosynthetic traits of maize. Environ Sci Pollut Res 26, 17577–17590 (2019). https://doi.org/10.1007/s11356-019-05170-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05170-6