Abstract
Soil contamination with cadmium (Cd) is problem nowadays due to industrialization. A pot experiment was conducted to assess the exogenous effect of calcium nitrate (CaNO3) on morphological traits, photosynthetic efficiency, oxidative stress indicators, secondary metabolites and enzymatic antioxidative capacity in two chickpea (chickpea-brittle and chickpea-2008) cultivars under Cd stress (0 and 200 μM). Results revealed that the Cd stress caused a significant (p < 0.05) reduction in biomass production, photosynthetic pigments, flavonoids and phenolics whereas increase in the activities of various antioxidative enzymes like superoxidase dismutase (SOD), peroxidase (POD), catalase (CAT) and ascorbate peroxidase (APX) as well as malondialdehyde (MDA) and H2O2 content. Cd-administered plants accumulated proline and total soluble proteins in substantial amount. However, results also show that chickpea-brittle showed more tolerance to the chickpea-2008 under the same levels of Cd in the soil. The leaves may be treated with Ca(NO3)2 to reduce toxic effects of Cd, which enhances biomass through increased plant growth along elevated pigments of photosynthetic, activities of antioxidant enzymes and levels of secondary metabolites, in comparison to untreated plants. Additionally, fortifying the Ca(NO3)2 application also decreases the levels of oxidative damaged to membrane-bounded organelles in the plants. Our findings suggested that Ca(NO3)2 spray can mitigate Cd toxicity and leads to increased chickpea growth and yield under Cd-contaminated conditions depicting by decreasing oxidative stress within cell. It was concluded that foliar application of Ca(NO3)2 may alleviate toxic effects of Cd in studied chickpea cultivars through enhanced plant growth, high content of photosynthetic pigments and low oxidative stress under Cd treatments.
Graphical abstract
![](http://media.springernature.com/lw685/springer-static/image/art%3A10.1007%2Fs12517-022-09638-7/MediaObjects/12517_2022_9638_Figa_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12517-022-09638-7/MediaObjects/12517_2022_9638_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12517-022-09638-7/MediaObjects/12517_2022_9638_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12517-022-09638-7/MediaObjects/12517_2022_9638_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12517-022-09638-7/MediaObjects/12517_2022_9638_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12517-022-09638-7/MediaObjects/12517_2022_9638_Fig5_HTML.png)
Similar content being viewed by others
References
Aebi H (1984): [13] Catalase in vitro, Methods in enzymology. Elsevier, pp. 121-126
Afzal J, Hu C, Imtiaz M, Elyamine A, Rana M, Imran M, Ismael M (2018): Cadmium tolerance in rice cultivars associated with antioxidant enzymes activities and Fe/Zn concentrations. International journal of Environmental Science and Technology
Afzal J, Saleem MH, Batool F, Elyamine AM, Rana MS, Shaheen A, El-Esawi MA, Tariq Javed M, Ali Q, Arslan Ashraf M, Hussain GS, Hu C (2020) Role of ferrous sulfate (FeSO4) in resistance to cadmium stress in two rice (Oryza sativa L.) Genotypes. Biomolecules 10:1693
Ahmad P, Abdel Latef AA, Abd Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513
Alam P, Kaur Kohli S, Al Balawi T, Altalayan FH, Alam P, Ashraf M, Bhardwaj R, Ahmad P (2020) Foliar application of 24-epibrassinolide improves growth, ascorbate-glutathione cycle, and glyoxalase system in brown mustard (Brassica juncea (L.) Czern.) under cadmium toxicity. Plants 9:1487
Ali N, Masood S, Mukhtar T, Kamran MA, Rafique M, Munis MFH, Chaudhary HJ (2015) Differential effects of cadmium and chromium on growth, photosynthetic activity, and metal uptake of Linum usitatissimum in association with Glomus intraradices. Environ Monit Assess 187:311
Allen S, Grimshaw H, Rowland A (1986) Chemical analysis: In: Moore, PD, Chapman, SB,(Eds), Methods in Plant Ecology. Blackwell Scientific Publication, Oxford
Alyemeni MN, Ahanger MA, 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
Anjum SA, Tanveer M, Hussain S, Ullah E, Wang L, Khan I, Shahzad B (2016) Morpho-physiological growth and yield responses of two contrasting maize cultivars to cadmium exposure. Clean Soil Air Water 44(1):29–36
Anwar S (2019): Chelators induced uptake of cadmium and modulation of water relation, antioxidants and photosynthetic traits of maize. Environ Sci Pollut Res
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1
Ashraf U, Tang X (2017) Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere 176:141–155
Ashraf MA, Hussain I, Rasheed R, Iqbal M, Riaz M, Arif MS (2017) Advances in microbe-assisted reclamation of heavy metal contaminated soils over the last decade: a review. J Environ Manag 198:132–143
Bae YJ, Kratzsch J (2018) Vitamin D and calcium in the human breast milk. Best Pract Res Clin Endocrinol Metab 32:39–45
Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bolat I, Kaya C, Almaca A, Timucin S (2006) Calcium sulfate improves salinity tolerance in rootstocks of plum. J Plant Nutr 29:553–564
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bray H, Thorpe W (1954): Analysis of phenolic compounds of interest in metabolism. Methods Biochem Anal 27-52
Chen C-N, Pan S-M (1996) Assay of superoxide dismutase activity by combining electrophoresis and densitometry. Bot Bull Acad Sin 37:107–111
Cui W, Gao C, Fang P, Lin G, Shen W (2013) Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. J Hazard Mater 260:715–724
El-Beltagi HS, Mohamed HI (2013) Alleviation of cadmium toxicity in Pisum sativum L. seedlings by calcium chloride. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 41:157–168
Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249
Farzadfar S, Zarinkamar F, Modarres-Sanavy SAM, Hojati M (2013) Exogenously applied calcium alleviates cadmium toxicity in Matricaria chamomilla L. plants. Environ Sci Pollut Res 20:1413–1422
Gill M (2014) Heavy metal stress in plants: a review. Int J Adv Res 2:1043–1055
Gong X, Huang D, Liu Y, Zeng G, Wang R, Xu P, Chen S (2019) Roles of multiwall carbon nanotubes in phytoremediation: cadmium uptake and oxidative burst in Boehmeria nivea (L.). Gaudich Environ Sci: Nano 6(3):851–862
Hasanuzzaman M, Hossain MA, Fujita M (2012) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261
Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system. Front Plant Sci 8:1061
Hasanuzzaman M, Nahar K, Anee TI, Khan MIR, Fujita M (2018) Silicon-mediated regulation of antioxidant defense and glyoxalase systems confers drought stress tolerance in Brassica napus L. S Afr J Bot 115:50–57
Hashem IA, Abbas AY, Abd El-Hamed AE-NH, Salem HMS, El-hosseiny OEM, Abdel-Salam MA, Saleem MH, Zhou W, Hu R (2020) Potential of rice straw biochar, sulfur and ryegrass (Lolium perenne L.) in remediating soil contaminated with nickel through irrigation with untreated wastewater. PeerJ 8:e9267
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hoseini SM, Zargari F (2013) Cadmium in plants: a review. Int J Farm Allied Sci 2:579–581
Huang D, Gong X, Liu Y, Zeng G, Lai C, Bashir H, Zhou L, Wang D, Xu P, Cheng M (2017) Effects of calcium at toxic concentrations of cadmium in plants. Planta 245:863–873
Huq ME, Fahad S, Shao Z, Sarven MS, Al-Huqail AA, Siddiqui MH, Ur Rahman MH, Khan IA, Alam M, Saeed M (2019) High arsenic contamination and presence of other trace metals in drinking water of Kushtia district, Bangladesh. J Environ Manag 242:199–209
Imran M, Hussain S, El-Esawi MA, Rana MS, Saleem MH, Riaz M, Ashraf U, Potcho MP, Duan M, Rajput IA (2020a) Molybdenum supply alleviates the cadmium toxicity in fragrant rice by modulating oxidative stress and antioxidant gene expression. Biomolecules 10:1582
Imran M, Sun X, Hussain S, Rana MS, Saleem MH, Riaz M, Tang X, Khan I, Hu C (2020b): Molybdenum supply increases root system growth of winter wheat by enhancing nitric oxide accumulation and expression of NRT genes. Plant Soil, 1-14
Jan R, Khan MA, Asaf S, Lee I-J, Kim KM (2019) Metal resistant endophytic bacteria reduces cadmium, nickel toxicity, and enhances expression of metal stress related genes with improved growth of Oryza sativa, via regulating its antioxidant machinery and endogenous hormones. Plants 8:363
Jana S, Choudhuri MA (1981) Glycolate metabolism of three submersed aquatic angiosperms: effect of heavy metals. Aquat Bot 11:67–77
Javed MT, Akram MS, Tanwir K, Chaudhary HJ, Ali Q, Stoltz E, Lindberg S (2017) Cadmium spiked soil modulates root organic acids exudation and ionic contents of two differentially Cd tolerant maize (Zea mays L.) cultivars. Ecotoxicol Environ Saf 141:216–225
Javed MT, Tanwir K, Akram MS, Shahid M, Niazi NK, Lindberg S (2019): Phytoremediation of cadmium-polluted water/sediment by aquatic macrophytes: role of plant-induced pH changes, Cadmium Toxicity and Tolerance in Plants. Elsevier, pp. 495-529
Javed MT, Saleem MH, Aslam S, Rehman M, Iqbal N, Begum R, Ali S, Alsahli AA, Alyemeni MN, Wijaya L (2020): Elucidating silicon-mediated distinct morpho-physio-biochemical attributes and organic acid exudation patterns of cadmium stressed Ajwain (Trachyspermum ammi L.). Plant Physiol Biochem
Kambhampati MS (2013) EDTA enhanced phytoremediation of copper contaminated soils using chickpea (Cicer aeritinum L.). Bull Environ Contam Toxicol 91:310–313
Kamran M, Danish M, Saleem MH, Malik Z, Parveen A, Abbasi GH, Jamil M, Ali S, Afzal S, Riaz M (2020) Application of abscisic acid and 6-benzylaminopurine modulated morpho-physiological and antioxidative defense responses of tomato (Solanum lycopersicum L.) by minimizing cobalt uptake. Chemosphere 263:128169
Kumar V, Singh J, Kumar P (2019) Heavy metals accumulation in crop plants: sources, response mechanisms, stress tolerance and their effects. Contam Agric Environ: Health Risks Remediat 1:38
Kuo-Huang L-L, Ku MS, Franceschi VR (2007) Correlations between calcium oxalate crystals and photosynthetic activities in palisade cells of shadeadapted Peperomia glabella. Bot Stud 48:155–164
Liu H, Zhang C, Wang J, Zhou C, Feng H, Mahajan MD, Han X (2017) Influence and interaction of iron and cadmium on photosynthesis and antioxidative enzymes in two rice cultivars. Chemosphere 171:240–247
Madhu PM, Sadagopan RS (2020) Effect of heavy metals on growth and development of cultivated plants with reference to cadmium, chromium and lead–a review. J Stress Physiol Biochem 16:84–102
Manetas Y (2006) Why some leaves are anthocyanic and why most anthocyanic leaves are red? Flora-Morphol Distrib Funct Ecol Plants 201(3):163–177
Nagajyoti PC, Lee KD, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Parveen A, Saleem MH, Kamran M, Haider MZ, Chen J-T, Malik Z, Rana MS, Hassan A, Hur G, Javed MT (2020) Effect of citric acid on growth, ecophysiology, chloroplast ultrastructure, and phytoremediation potential of jute (Corchorus capsularis L.) seedlings exposed to copper stress. Biomolecules 10:592
Pękal A, Pyrzynska K (2014) Evaluation of aluminium complexation reaction for flavonoid content assay. Food Anal Methods 7:1776–1782
Pereira AS, Dorneles AOS, Bernardy K, Sasso VM, Bernardy D, Possebom G, Rossato LV, Dressler VL, Tabaldi LA (2018) Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in Pfaffia glomerata (Spreng.) Pedersen plants by activation antioxidant enzyme system. Environ Sci Pollut Res 25:18548–18558
Rana M, Bhantana P, Imran M, Saleem M (2020) Molybdenum potential vital role in plants metabolism for optimizing the growth and development. Ann Environ Sci Toxicol 4:032–044
Rehman M, Saleem MH, Fahad S, Maqbool Z, Peng D, Deng G, Liu L (2020) Medium nitrogen optimized Boehmeria nivea L. growth in copper contaminated soil. Chemosphere 128972
Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng L, Wang Y, Zhou Y, Anastopoulos I (2020) Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. J Hazard Mater 123919
Rizwan M, Meunier J-D, Miche H, Keller C (2012) Effect of silicon on reducing cadmium toxicity in durum wheat (Triticum turgidum L. cv. Claudio W.) grown in a soil with aged contamination. J Hazard Mater 209:326–334
Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879
Rizwan M, Ali S, Ali B, Adrees M, Arshad M, Hussain A, Ur Rehman MZ, Waris AA (2019a) Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere 214:269–277
Rizwan M, Ali S, ur Rehman MZ, Maqbool A (2019b) A critical review on the effects of zinc at toxic levels of cadmium in plants. Environ Sci Pollut Res 26:6279–6289
Saeed Z, Naveed M, Imran M, Bashir MA, Sattar A, Mustafa A, Hussain A, Xu M (2019) Combined use of Enterobacter sp. MN17 and zeolite reverts the adverse effects of cadmium on growth, physiology and antioxidant activity of Brassica napus. PLoS One 14:e0213016
Sakharov IY, Ardila GB (1999) Variations of peroxidase activity in cocoa (Theobroma cacao L.) beans during their ripening, fermentation and drying. Food Chem 65:51–54
Sakouhi L, Kharbech O, Massoud MB, Gharsallah C, Hassine SB, Munemasa S, Murata Y, Chaoui A (2021): Calcium and ethylene glycol tetraacetic acid mitigate toxicity and alteration of gene expression associated with cadmium stress in chickpea (Cicer arietinum L.) shoots. Protoplasma, 1-13
Saleem MH, Ali S, Seleiman MF, Rizwan M, Rehman M, Akram NA, Liu L, Alotaibi M, Al-Ashkar I, Mubushar M (2019) Assessing the correlations between different traits in copper-sensitive and copper-resistant varieties of jute (Corchorus capsularis L.). Plants 8:545
Saleem M, Ali S, Rehman M, Rana M, Rizwan M, Kamran M, Imran M, Riaz M, Hussein M, Elkelish A, Lijun L (2020a) Influence of phosphorus on copper phytoextraction via modulating cellular organelles in two jute (Corchorus capsularis L.) varieties grown in a copper mining soil of Hubei Province, China. Chemosphere 248:126032
Saleem MH, Ali S, Hussain S, Kamran M, Chattha MS, Ahmad S, Aqeel M, Rizwan M, Aljarba NH, Alkahtani S (2020b) Flax (Linum usitatissimum L.): a potential candidate for phytoremediation? Biological and Economical Points of View. Plants 9:496
Šamec D, Karalija E, Šola I, Vujčić Bok V, Salopek-Sondi B (2021) The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants 10(1):118
Shahid M, Javed MT, Tanwir K, Akram MS, Tazeen SK, Saleem MH, Masood S, Mujtaba S, Chaudhary HJ (2020): Plant growth-promoting Bacillus sp. strain SDA-4 confers Cd tolerance by physio-biochemical improvements, better nutrient acquisition and diminished Cd uptake in Spinacia oleracea L. Physiol Mol Biol Plants 1-17
Shanying H, **aoe Y, Zhenli H, Baligar VC (2017) Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere 27:421–438
Tang H, Liu Y, Gong X, Zeng G, Zheng B, Wang D, Sun Z, Zhou L, Zeng X (2015) Effects of selenium and silicon on enhancing antioxidative capacity in ramie (Boehmeria nivea (L.) Gaud.) under cadmium stress. Environ Sci Pollut Res 22:9999–10008
Thind S, Hussain I, Ali S, Hussain S, Rasheed R, Ali B, Hussain HA (2020) Physiological and biochemical bases of foliar silicon-induced alleviation of cadmium toxicity in wheat. J Soil Sci Plant Nutr 20(4):2714–2730
Turan V (2020) Potential of pistachio shell biochar and dicalcium phosphate combination to reduce Pb speciation in spinach, improved soil enzymatic activities, plant nutritional quality, and antioxidant defense system. Chemosphere 245:125611
Wang J, Chen X, Chi Y, Chu S, Hayat K, Zhi Y, Hayat S, Terziev D, Zhang D, Zhou P (2020a) Optimization of NPK fertilization combined with phytoremediation of cadmium contaminated soil by orthogonal experiment. Ecotoxicol Environ Saf 189:109997
Wang X, Deng S, Zhou Y, Long J, Ding D, Du H, Lei M, Chen C, Tie BQ (2020b): Application of different foliar iron fertilizers for enhancing the growth and antioxidant capacity of rice and minimizing cadmium accumulation. Environ Sci Pollut Res 1-12
Wen E, Yang X, Chen H, Shaheen SM, Sarkar B, Xu S, Song H, Liang Y, Rinklebe J, Hou D (2020) Iron-modified biochar and water management regime-induced changes in plant growth, enzyme activities, and phytoavailability of arsenic, cadmium and lead in a paddy soil. J Hazard Mater 407:124344
Yadav SS, Kumar J, Yadav S, Singh S, Yadav V, Turner NC, Redden R (2006) Evaluation of Helicoverpa and drought resistance in desi and kabuli chickpea. Plant Gen Resources 4:198–203
Yaseen R, Aziz O, Saleem MH, Riaz M, Zafar-ul-Hye M, Rehman M, Ali S, Rizwan M, Nasser Alyemeni M, El-Serehy HA (2020) Ameliorating the drought stress for wheat growth through application of ACC-deaminase containing rhizobacteria along with biogas slurry. Sustainability 12:6022
Zaheer IE, Ali S, Saleem MH, Arslan Ashraf M, Ali Q, Abbas Z, Rizwan M, El-Sheikh MA, Alyemeni MN, Wijaya L (2020a) Zinc-lysine supplementation mitigates oxidative stress in rapeseed (Brassica napus L.) by preventing phytotoxicity of chromium, when irrigated with tannery wastewater. Plants 9:1145
Zaheer IE, Ali S, Saleem MH, Noor I, El-Esawi MA, Hayat K, Rizwan M, Abbas Z, El-Sheikh MA, Alyemeni MN (2020b) Iron–lysine mediated alleviation of chromium toxicity in spinach (Spinacia oleracea L.) plants in relation to morpho-physiological traits and iron uptake when irrigated with tannery wastewater. Sustainability 12:6690
Zahoor A, Ahmad F, Hameed M, Basra SMA (2018) Structural and functional aspects of photosynthetic response in Eichhornia crassipes (Mart.) Solms under cadmium stress. Pak J Bot 50:489–493
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Responsible Editor: Haroun Chenchouni
Highlights
• Exogenous Ca enhances chickpea growth and yield in both cultivars.
• Exogenous Ca decline oxidative stress by decreasing level of H2O2 and MDA.
• Exogenous Ca boosts antioxidants and secondary metabolites, etc.
• Exogenous Ca enhanced growth and yield in control and Cd-contaminated conditions.
Supplementary Information
ESM 1
(DOCX 102 kb)
Rights and permissions
About this article
Cite this article
Parveen, A., Hussain, I., Perveen, S. et al. Fertigation of calcium nitrate [Ca(NO3)2] confers metal tolerance in two chickpea (Cicer arietinum L.) cultivars. Arab J Geosci 15, 1078 (2022). https://doi.org/10.1007/s12517-022-09638-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12517-022-09638-7