Skip to main content
Log in

Elucidating the distinct interactive impact of cadmium and nickel on growth, photosynthesis, metal-homeostasis, and yield responses of mung bean (Vigna radiata L.) varieties

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

A Correction to this article was published on 23 February 2021

This article has been updated

Abstract

Contamination of soils with heavy metals (HMs) caused serious problems because plants tend to absorb HMs from the soil. In view of HM hazards to plants as well as agro-ecosystems, we executed this study to assess metal toxicity to mung bean (Vigna radiata) plants cultivated in soil with six treatment levels of cadmium (Cd) and nickel (Ni) and to find metal tolerant variety, i.e., M-93 (V1) and M-1(V2) with multifarious plant biochemical and physiological attributes. Increasing doses of Cd and Ni inhibited plant growth and photosynthesis and both varieties showed highly significant differences in the morpho-physiological attributes. V2 showed sensitivity to Cd and Ni treatments alone or in combination. Tolerance indices for attributes presented a declined growth of Vigna plants under HM stress accompanied by highly significant suppression in gas exchange characteristics. Of single element applications, the adverse effects on mung bean were more pronounced in Cd treatments. V1 showed much reduction in photosynthesis attributes except sub-stomatal CO2 concentration in all treatments compared to V2. The yield attributes, i.e., seed yield/plant and 100-seed weight, were progressively reduced in T5 for both varieties. In combination, we have observed increased mobility of Cd and Ni in both varieties. The results showed that water use efficiency (WUE) generally increased in all the treatments for both varieties compared to control. V2 exhibited less soluble sugars and free amino acids compared to V1 in all the treatments. Similarly, we recorded an enhanced total free amino acid contents in both varieties among all the metal treatments against control plants. We conclude that combinatorial treatment proved much lethal for Vigna plants, but V1 performed better than V2 in counteracting the adverse effects of Cd and Ni.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Not applicable

Change history

References

  • Ahmad MS, Ashraf M, Hussain M (2011) Phytotoxic effects of nickel on yield and concentration of macro- and micro-nutrients in sunflower (Helianthus annuus L.) achenes. J Hazard Mater 185:1295–1303. https://doi.org/10.1016/j.jhazmat.2010.10.045

    Article  CAS  Google Scholar 

  • Ahmad MSA, Hussain M, Ashraf M, Ahmad R, Ashraf MY (2009) Effect of nickel on seed germinability of some elite sunflower (Helianthus annuus L.) cultivars. Pak J Bot 41:1871–1882

    CAS  Google Scholar 

  • Amirjani M (2012) Effects of cadmium on wheat growth and some physiological factors. Int J For Soil Eros 2:50–58

    Google Scholar 

  • Ashraf MY, Ashraf M, Arshad M (2010) Major nutrients supply in legume crops under stress environments. Climate change and management of cool season grain legume crops. Springer, In, pp 155–169

    Google Scholar 

  • Ashraf MY, Roohi M, Iqbal Z, Ashraf M, Öztürk M, Gücel S (2016) Cadmium (Cd) and lead (Pb) induced changes in growth, some biochemical attributes, and mineral accumulation in two cultivars of mungbean [Vigna radiata (L.) Wilczek]. Commun Soil Sci Plant Anal 47:405–413

    CAS  Google Scholar 

  • Ashraf MY, Sadiq R, Hussain M, Ashraf M, Ahmad MSA (2011) Toxic effect of nickel (Ni) on growth and metabolism in germinating seeds of sunflower (Helianthus annuus L.). Biol Trace Elem Res 143:1695–1703

    Article  CAS  Google Scholar 

  • Bahmani R, Bihamta M, Habibi D, Forozesh P, Ahmadvand S (2012) Effect of cadmium chloride on growth parameters of different bean genotypes (Phaseolus vulgaris L.). ARPN J Agric Biol Sci 7:35–40

    CAS  Google Scholar 

  • Bartholomae E, Incollingo A, Vizcaino M, Wharton C, Johnston CS (2019) Mungbean protein supplement improves muscular strength in healthy, underactive vegetarian adults. Nutrients 11:2423

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z, Cui J (2017) Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul 81:253–264

    Article  CAS  Google Scholar 

  • Ci D, Jiang D, Wollenweber B, Dai T, Jing Q, Cao W (2010) Cadmium stress in wheat seedlings: growth, cadmium accumulation and photosynthesis. Acta Physiol Plant 32:365–373

    Article  CAS  Google Scholar 

  • Cwielag-Drabek M, Piekut A, Gut K, Grabowski M (2020) Risk of cadmium, lead and zinc exposure from consumption of vegetables produced in areas with mining and smelting past. Sci Rep 10:1–9

    Article  Google Scholar 

  • De Filippis L, Ziegler H (1993) Effect of sublethal concentrations of zinc, cadmium and mercury on the photosynthetic carbon reduction cycle of Euglena. J Plant Physiol 142:167–172

    Article  Google Scholar 

  • Dong J, Wu FB, Zhang GP (2005) Effect of cadmium on growth and photosynthesis of tomato seedlings. J Zhejiang Univ Sci B 6:974–980. https://doi.org/10.1631/jzus.2005.B0974

    Article  CAS  Google Scholar 

  • Figlioli F, Sorrentino MC, Memoli V, Arena C, Maisto G, Giordano S, Capozzi F, Spagnuolo V (2019) Overall plant responses to cd and Pb metal stress in maize: growth pattern, ultrastructure, and photosynthetic activity. Environ Sci Pollut Res 26:1781–1790. https://doi.org/10.1007/s11356-018-3743-y

    Article  CAS  Google Scholar 

  • Greger M, Johansson M (1992) Cadmium effects on leaf transpiration of sugar beet (Beta vulgaris). Physiol Plant 86:465–473

    Article  CAS  Google Scholar 

  • Hamilaton P, Van Slyke D (1943) Amino acids determination with ninhydrin. J Biol Chem 150:223–231

    Article  Google Scholar 

  • Hou D et al (2019) Mungbean (Vigna radiata L.): bioactive polyphenols, polysaccharides, peptides, and health benefits. Nutrients 11:1238

    Article  CAS  Google Scholar 

  • Ilyas N, Ambreen F, Batool N, Arshad M, Mazhar R, Bibi F, Saeed M (2018) Contribution of nitrogen fixed by mungbean to the following wheat crop. Commun Soil Sci Plant Anal 49:148–158

    Article  CAS  Google Scholar 

  • Irshad MK, Chen C, Noman A, Ibrahim M, Adeel M, Shang J (2020) Goethite-modified biochar restricts the mobility and transfer of cadmium in soil-rice system. Chemosphere 242:125152

    Article  Google Scholar 

  • Jackson ML (1962) Soil chemical analysis vol 497. Constable and Co Ltd., London

    Google Scholar 

  • Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-Sattari T (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126:402–407

    Article  CAS  Google Scholar 

  • Khalid N, Aqeel M, Noman A (2019a) System biology of metal tolerance in plants: An integrated view of genomics, Transcriptomics, metabolomics, and Phenomics. Plant Metallomics and Functional Omics, In, pp 107–144. https://doi.org/10.1007/978-3-030-19103-0_6

    Book  Google Scholar 

  • Khalid N, Hussain M, Hameed M, Ahmad R (2017a) Physiological, biochemical and defense system responses of Parthenium hysterophorus to vehicular exhaust pollution. Pak J Bot 49:67–75

    CAS  Google Scholar 

  • Khalid N, Masood A, Noman A, Aqeel M, Qasim M (2019b) Study of the responses of two biomonitor plant species (Datura alba & Ricinus communis) to roadside air pollution. Chemosphere 235:832–841. https://doi.org/10.1016/j.chemosphere.2019.06.143

    Article  CAS  Google Scholar 

  • Khalid N, Noman A, Aqeel M, Hadayat N, Anjum S (2017b) NPK could alleviate the adverse effects of simulated acid rain in sunflower (Helianthus annuus L.). J Plant Nutr 41:584–595. https://doi.org/10.1080/01904167.2017.1406108

    Article  CAS  Google Scholar 

  • Khalid N, Noman A, Sanaullah T, Akram MA, Aqeel M (2018) Vehicle pollution toxicity induced changes in physiology, defence system and biochemical characteristics of Calotropis procera L. Chem Ecol 34:565–581. https://doi.org/10.1080/02757540.2018.1452917

    Article  CAS  Google Scholar 

  • Kotapati KV, Palaka BK, Ampasala DR (2017) Alleviation of nickel toxicity in finger millet (Eleusine coracana L.) germinating seedlings by exogenous application of salicylic acid and nitric oxide. Crop J 5:240–250. https://doi.org/10.1016/j.cj.2016.09.002

    Article  Google Scholar 

  • Li Q, Lu Y, Shi Y, Wang T, Ni K, Xu L, Liu S, Wang L, Xiong Q, Giesy JP (2013) Combined effects of cadmium and fluoranthene on germination, growth and photosynthesis of soybean seedlings. J Environ Sci 25:1936–1946

    Article  CAS  Google Scholar 

  • Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) Nitrogen. In: Principles of plant nutrition. Kluwer Academic Publishers, Springer, Dordrecht, pp 397–434. https://doi.org/10.1007/978-94-010-1009-2_7

    Chapter  Google Scholar 

  • Noman A, Aqeel M (2017) miRNA-based heavy metal homeostasis and plant growth. Environ Sci Pollut Res 24:10068–10082. https://doi.org/10.1007/s11356-017-8593-5

    Article  CAS  Google Scholar 

  • Noman A, Fahad S, Aqeel M, Ali U, Amanullah, Anwar S, Baloch SK, Zainab M (2017) miRNAs: major modulators for crop growth and development under abiotic stresses. Biotechnol Lett 39:685–700. https://doi.org/10.1007/s10529-017-2302-9

    Article  CAS  Google Scholar 

  • Noman A, Sanaullah T, Khalid N, Islam W, Khan S, Irshad MK, Aqeel M (2019) Crosstalk between plant miRNA and heavy metal toxicity. Plant Metallomics and Functional Omics, In, pp 145–168. https://doi.org/10.1007/978-3-030-19103-0_7

    Book  Google Scholar 

  • Osman ME, El-Naggar AH, El-Sheekh MM, El-Mazally EE (2004) Differential effects of Co2+ and Ni2+ on protein metabolism in Scenedesmus obliquus and Nitzschia perminuta. Environ Toxicol Pharmacol 16:169–178

    Article  CAS  Google Scholar 

  • Rai PK, Lee SS, Zhang M, Tsang YF, Kim K-H (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environ Int 125:365–385

    Article  CAS  Google Scholar 

  • Riazi A, Matsuda K, Arslan A (1985) Water-stress induced changes in concentrations of proline and other solutes in growing regions of young barley leaves. J Exp Bot 36:1716–1725

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Rizvi H, Rinklebe J, Tsang DCW, Meers E, Ok YS, Ishaque W (2016) Phytomanagement of heavy metals in contaminated soils using sunflower: a review. Crit Rev Environ Sci Technol 46:1498–1528

    Article  CAS  Google Scholar 

  • Rubio M, Escrig I, Martinez-Cortina C, Lopez-Benet F, Sanz A (1994) Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regul 14:151–157

    Article  CAS  Google Scholar 

  • Rucińska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38:257

    Article  Google Scholar 

  • Sandalio L, Dalurzo H, Gomez M, Romero-Puertas M, Del Rio L (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    Article  CAS  Google Scholar 

  • Schlegel H, Godbold DL, Hüttermann A (1987) Whole plant aspects of heavy metal induced changes in CO2, uptake and water relations of spruce (Picea abies) seedlings. Physiol Plant 69:265–270

    Article  CAS  Google Scholar 

  • Shah SS, Mohammad F, Shafi M, Bakht J, Zhou W (2011) Effects of cadmium and salinity on growth and photosynthesis parameters of Brassica species. Pak J Bot 43:333–340

    Google Scholar 

  • Shamsi IH, Wei K, Jilani G, G-p Z (2007) Interactions of cadmium and aluminum toxicity in their effect on growth and physiological parameters in soybean. J Zhejiang Univ Sci B 8:181–188

    Article  CAS  Google Scholar 

  • Sreekanth T, Nagajyothi P, Lee K, Prasad T (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Envrion Sci Technol 10:1129–1140

    Article  CAS  Google Scholar 

  • Sundari T (2009) Morphological and physiological characteristics of shading tolerant and sensitive mungbean genotypes. HAYATI J Biosci 16:127–134

    Article  Google Scholar 

  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Molecular, clinical and environmental toxicology. Springer, In, pp 133–164

    Google Scholar 

  • Wahid A, Ghani A (2008) Varietal differences in mungbean (Vigna radiata) for growth, yield, toxicity symptoms and cadmium accumulation. Ann Appl Biol 152:59–69. https://doi.org/10.1111/j.1744-7348.2007.00192.x

    Article  CAS  Google Scholar 

  • Wahid A, Ghani A, Javed F (2008) Effect of cadmium on photosynthesis, nutrition and growth of mungbean. Agron Sunstain Develop 28:273–280. https://doi.org/10.1051/agro:2008010

    Article  CAS  Google Scholar 

  • Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059

    Article  CAS  Google Scholar 

  • Yadav S (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  • Yi-Shen Z, Shuai S, Fitzgerald R (2018) Mungbean proteins and peptides: nutritional, functional and bioactive properties. Food. Nutr Res 62:1290. https://doi.org/10.29219/fnr.v62.1290

    Article  CAS  Google Scholar 

  • Younis U, Qayyum MF, Shah MHR, Danish S, Shahzad AN, Malik SA, Mahmood S (2015) Growth, survival, and heavy metal (cd and Ni) uptake of spinach (Spinacia oleracea) and fenugreek (Trigonella corniculata) in a biochar-amended sewage-irrigated contaminated soil. J Plant Nutr Soil Sci 178:209–217

    Article  CAS  Google Scholar 

  • Zhang H, Zhang LL, Li J, Chen M, An RD (2020) Comparative study on the bioaccumulation of lead, cadmium and nickel and their toxic effects on the growth and enzyme defence strategies of a heavy metal accumulator, Hydrilla verticillata (L.f.) Royle. Environ Sci Pollut Res 27:9853–9865. https://doi.org/10.1007/s11356-019-06968-0

    Article  CAS  Google Scholar 

Download references

Funding

The Deanship of Scientific Research, King Khalid University, funded this work through research groups program under grant number R.G.P. 2/101/41.

Author information

Authors and Affiliations

Authors

Contributions

MA, AN: conceived the idea, designed the experiment, and drafted the manuscript; MA, NK, MH, AN: writing, review, editing; AT, RZA, ML, MKI: performed experiment, gathered literature; MSA, MTJ, SA: analyzed the data, and helps in interpretation of results; SA, MH, AN: critically revised the manuscript; all authors approved the final version of the manuscript.

Corresponding author

Correspondence to Ali Noman.

Ethics declarations

Ethical approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare no competing interests.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aqeel, M., Khalid, N., Tufail, A. et al. Elucidating the distinct interactive impact of cadmium and nickel on growth, photosynthesis, metal-homeostasis, and yield responses of mung bean (Vigna radiata L.) varieties. Environ Sci Pollut Res 28, 27376–27390 (2021). https://doi.org/10.1007/s11356-021-12579-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-12579-5

Keywords

Navigation