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Environmental Science and Pollution Research

, Volume 26, Issue 19, pp 19261–19271 | Cite as

Exogenous application of ascorbic acid mitigates cadmium toxicity and uptake in Maize (Zea mays L.)

  • Kangping Zhang
  • Guiyin Wang
  • Mingchen Bao
  • Longchang WangEmail author
  • Xiaoyu XieEmail author
Research Article

Abstract

Cadmium (Cd) contamination in agricultural soils is a prevalent environmental issue and poses potential threats to food security. Foliar ascorbic acid might prove a potent tool to alleviate toxicity of Cd toxicity in maize. An experiment was conducted with objectives to study exogenous ascorbic acid–modulated improvements in physiochemical attributes of maize under Cd toxicity. The experiment was conducted under completely randomized design. Treatments were comprised of varying concentrations of foliar ascorbic acid viz. 0.0, 0.1, 0.3, and 0.5 mM of AsA. Toxicity of Cd decreased the maize growth, increased lipid peroxidation, disturbed protein metabolism, and reduced the antioxidant defense capabilities compared with the control. However, foliar AsA significantly improved maize growth and development, photosynthetic capabilities, and protein concentrations in Cd-stressed maize plants. Meanwhile, the malondialdehyde contents and hydrogen peroxide accumulation levels in Cd-stressed maize plants decreased remarkably with increasing AsA concentrations. Furthermore, the combined treatments conspicuously boosted activities of superoxide dismutase, peroxidase, catalase, and glutathione reductase under the Cd stress alone. In addition, the application of AsA reduced the Cd uptake by 10.3–12.3% in grains. Conclusively, foliar ascorbic acid alleviated the negative effects of Cd stress in maize and improved photosynthetic processes, osmolytes, and antioxidant defense systems.

Keywords

Ascorbic acid Cadmium uptake Cadmium toxicity Oxidative damage Maize Antioxidant defense 

Notes

Acknowledgments

The authors thank Dr. Meichun Duan, Dr. Sai Zhang, and Yi Xing of Southwest University for supporting the analytical work, and also thank Shakeel Ahmad Anjum from the Department of Agronomy, University of Agriculture Faisalabad, Pakistan, for the critical revision of the manuscript.

Funding information

This research was financially supported by the Special Fund for Agro-scientific Research in the Public Interest (201503127) and National Natural Science Foundation of China (31271673, 31871583).

References

  1. Abbas T, Rizwan M, Ali S, Zia-ur-Rehman M, Qayyum MF, Abbas F, Hannan F, Rinklebe J, Ok YS (2017) Effect of biochar on cadmium bioavailability and uptake in wheat (Triticum aestivum L.) grown in a soil with aged contamination. Ecotoxicol Environ Saf 140:37–47.  https://doi.org/10.1016/j.ecoenv.2017.02.028 CrossRefGoogle Scholar
  2. Adhikari S, Ghosh S, Azahar I, Adhikari A, Shaw AK, Konar S, Roy S, Hossain Z (2018) Sulfate improves cadmium tolerance by limiting cadmium accumulation, modulation of sulfur metabolism and antioxidant defense system in maize. Environ Exp Bot 153:143–162.  https://doi.org/10.1016/j.envexpbot.2018.05.008 CrossRefGoogle Scholar
  3. Aebi H (1984) Catalase in vitro. Methods Enzymol 105(105):121–126.  https://doi.org/10.1016/S0076-6879(84)05016-3 CrossRefGoogle Scholar
  4. Ahmad P, Abd Allah EF, Hashem A, Sarwat M, Gucel S (2016) Exogenous application of selenium mitigates cadmium toxicity in Brassica juncea L. (Czern & Cross) by up-regulating antioxidative system and secondary metabolites. J Plant Growth Regul 35(4):936–950.  https://doi.org/10.1007/s00344-016-9592-3 CrossRefGoogle Scholar
  5. Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P (2018) Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255(1):79–93.  https://doi.org/10.1007/s00709-017-1132-x CrossRefGoogle Scholar
  6. Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid—a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8(613).  https://doi.org/10.3389/fpls.2017.00613
  7. Alamri SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Ali HM, Alaraidh IA, Alsahli AA, Al-Rabiah H, Mateen M (2018) Ascorbic acid improves the tolerance of wheat plants to lead toxicity. J Plant Interact 13(1):409–419.  https://doi.org/10.1080/17429145.2018.1491067 CrossRefGoogle Scholar
  8. Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R, Ahmad P (2018) Correction to: selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255(3):985–986.  https://doi.org/10.1007/s00709-018-1231-3 CrossRefGoogle Scholar
  9. Amin B, Mahleghah G, Mahmood HMR, Hossein M (2009) Evaluation of interaction effect of drought stress with ascorbate and salicylic acid on some of physiological and biochemical parameters in Okra (Hibiscus esculentus L.). Res J Biol Sci 4:380–387 http://medwelljournals.com/abstract/?doi=rjbsci.2009.380.387 Google Scholar
  10. Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22(21):17022–17030.  https://doi.org/10.1007/s11356-015-4882-z CrossRefGoogle Scholar
  11. 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. Environ Sci Pollut Res 23(12):11864–11875.  https://doi.org/10.1007/s11356-016-6382-1 CrossRefGoogle Scholar
  12. Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252(2):399–413.  https://doi.org/10.1007/s00709-014-0710-4 CrossRefGoogle Scholar
  13. Aziz A, Akram NA, Ashraf M (2018) Influence of natural and synthetic vitamin c (ascorbic acid) on primary and secondary metabolites and associated metabolism in quinoa (Chenopodium quinoa Willd.) plants under water deficit regimes. Plant Physiol Biochem 123:192–203.  https://doi.org/10.1016/j.plaphy.2017.12.004
  14. Baldi E, Miotto A, Ceretta CA, Brunetto G, Muzzi E, Sorrenti G, Toselli M, Quartieri M (2018) Soil application of p can mitigate the copper toxicity in grapevine: physiological implications. Sci Hortic 238:400–407.  https://doi.org/10.1016/j.scienta.2018.04.070 CrossRefGoogle Scholar
  15. Bashri G, Prasad SM (2016) Exogenous IAA differentially affects growth, oxidative stress and antioxidants system in Cd stressed Trigonella foenum-graecum L. seedlings: toxicity alleviation by up-regulation of ascorbate-glutathione cycle. Ecotoxicol Environ Saf 132:329–338.  https://doi.org/10.1016/j.ecoenv.2016.06.015
  16. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287.  https://doi.org/10.1016/0003-2697(71)90370-8 CrossRefGoogle Scholar
  17. 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(s1-2):248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  18. Castillo FJ, Penel C, Greppin H (1984) Peroxidase release induced by ozone in sedum album leaves: involvement of Ca2+. Plant Physiol 74(4):846–851.  https://doi.org/10.1104/pp.74.4.846 CrossRefGoogle Scholar
  19. Chao YY, Kao CH (2010) Heat shock-induced ascorbic acid accumulation in leaves increases cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 336(1-2):39–48.  https://doi.org/10.1007/s11104-010-0438-7 CrossRefGoogle Scholar
  20. Chen Q, Zhang XY, Liu YY, Wei JY, Shen WB, Shen ZG (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(2):253–264.  https://doi.org/10.1007/s10725-016-0202-y CrossRefGoogle Scholar
  21. Gao M, Zhou J, Liu HL, Zhang WT, Hu YM, Liang JN, Zhou J (2018) Foliar spraying with silicon and selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. Sci Total Environ 631–632:1100–1108.  https://doi.org/10.1016/j.scitotenv.2018.03.047 CrossRefGoogle Scholar
  22. Geng AJ, Wang X, Wu LS, Wang FH, Wu ZC, Yang H, Chen Y, Wen D, Liu XX (2018) Silicon improves growth and alleviates oxidative stress in rice seedlings (Oryza sativa L.) by strengthening antioxidant defense and enhancing protein metabolism under arsanilic acid exposure. Ecotoxicol Environ Saf 158:266–273.  https://doi.org/10.1016/j.ecoenv.2018.03.050
  23. Gondor OK, Pál M, Darkó É, Janda T, Szalai G (2016) Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS One 11(8):e160157.  https://doi.org/10.1371/journal.pone.0160157 CrossRefGoogle Scholar
  24. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212.  https://doi.org/10.1016/0003-2697(80)90139-6 CrossRefGoogle Scholar
  25. Han Y, Wu M, Hao L, Yi H (2018) Sulfur dioxide derivatives alleviate cadmium toxicity by enhancing antioxidant defence and reducing Cd2+ uptake and translocation in foxtail millet seedlings. Ecotoxicol Environ Saf 157:207–215.  https://doi.org/10.1016/j.ecoenv.2018.03.084 CrossRefGoogle Scholar
  26. Huang P, Jiang Q, Yu P, Yang L, Mao L (2013) Alkaline post-treatment of Cd(II)-glutathione coordination polymers: toward green synthesis of water-soluble and cytocompatible Cds quantum dots with tunable optical properties. ACS Appl Mater Interfaces 5:5239–5246.  https://doi.org/10.1021/am401082n
  27. Huang B, Li Z, Li D, Yuan Z, Nie X, Huang J, Zhou Y (2018) Effect of moisture condition on the immobilization of Cd in red paddy soil using passivators. Environ Technol:14(2):1–14(2)10.  https://doi.org/10.1080/09593330.2018.1449900
  28. Khan MI, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173(3):9–18.  https://doi.org/10.1016/j.jplph.2014.09.011 CrossRefGoogle Scholar
  29. Kováčik J, Babula P (2017) Fluorescence microscopy as a tool for visualization of metal-induced oxidative stress in plants. Acta Physiol Plant 39(8):157–359.  https://doi.org/10.1016/j.algal.2017.04.026 CrossRefGoogle Scholar
  30. Kumar M, Bijo AJ, Baghel RS, Reddy CRK, Jha B (2012) Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiol Biochem 51:129–138.  https://doi.org/10.1016/j.plaphy.2011.10.016 CrossRefGoogle Scholar
  31. Liang YC, Zhu J, Li ZJ, Chu GX, Ding YF, Zhang J, Sun WC (2008) Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environ Exp Bot 64(3):286–294.  https://doi.org/10.1016/j.envexpbot.2008.06.005 CrossRefGoogle Scholar
  32. Lichtenthaler HK (1987) Chlorophylls and carotenoids pigments of photosynthetic. Methods Enzymol 148C(1):350–382.  https://doi.org/10.1016/0076-6879(87)48036-1 CrossRefGoogle Scholar
  33. Liu YZ, Xiao TF, Baveye PC, Zhu JM, Ning ZP, Li HJ (2015) Potential health risk in areas with high naturally-occurring cadmium background in southwestern China. Ecotoxicol Environ Saf 112:122–131.  https://doi.org/10.1016/j.ecoenv.2014.10.022 CrossRefGoogle Scholar
  34. Lu QQ, Zhang TT, Zhang W, Su CL, Yang YR, Hu D, Xu QS (2018) Alleviation of cadmium toxicity in Lemna minor by exogenous salicylic acid. Ecotoxicol Environ Saf 147:500–508.  https://doi.org/10.1016/j.ecoenv.2017.09.015 CrossRefGoogle Scholar
  35. Mahalingam R, Jambunathan N, Gunjan SK, Faustin E, Weng H, Ayoubi P (2006) Analysis of oxidative signalling induced by ozone in Arabidopsis thaliana. Plant Cell Environ 29(7):1357–1371.  https://doi.org/10.1111/j.1365-3040.2006.01516.x CrossRefGoogle Scholar
  36. 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 PollutRes 25(19):18548–18558.  https://doi.org/10.1007/s11356-018-2005-3 CrossRefGoogle Scholar
  37. Rizwan M, Ali S, Qayyum MF, Ok YS, Zia-ur-Rehman M, Abbas Z, Hannan F (2017) Use of maize (Zea mays L.) for phytomanagement of Cd-contaminated soils: a critical review. Environ Geochem Hlth 39(2):259–277.  https://doi.org/10.1007/s10653-016-9826-0 CrossRefGoogle Scholar
  38. Rizwan M, Ali S, Abbas T, Adrees M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Qayyum MF, Nawaz R (2018) Residual effects of biochar on growth, photosynthesis and cadmium uptake in rice (Oryza sativa L.) under Cd stress with different water conditions. J Environ Manag 206:676–683.  https://doi.org/10.1016/j.jenvman.2017.10.035 CrossRefGoogle Scholar
  39. Shafiq S, Akram NA, Ashraf M, Arshad A (2014) Synergistic effects of drought and ascorbic acid on growth, mineral nutrients and oxidative defense system in canola (Brassica napus L.) plants. Acta Physiol Plant 36(6):1539–1553.  https://doi.org/10.1007/s11738-014-1530-z CrossRefGoogle Scholar
  40. Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52(364):2207–2211.  https://doi.org/10.1093/jexbot/52.364.2207 CrossRefGoogle Scholar
  41. Shen G, Niu J, Deng Z (2017) Abscisic acid treatment alleviates cadmium toxicity in purple flowering stalk (Brassica campestris L. ssp. chinensis var. purpurea Hort.) seedlings. Plant Physiol Biochem 118(3):471–478.  https://doi.org/10.1016/j.plaphy.2017.07.018 CrossRefGoogle Scholar
  42. Shi GR, Cai QS, Liu CF, Wu L (2010) Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul 61(1):45–52.  https://doi.org/10.1007/s10725-010-9447-z CrossRefGoogle Scholar
  43. Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide Biol Chem 20(4):289–297.  https://doi.org/10.1016/j.niox.2009.02.004
  44. Vaculík M, Pavlovič A, Lux A (2015) Silicon alleviates cadmium toxicity by enhanced photosynthetic rate and modified bundle sheath’s cell chloroplasts ultrastructure in maize. Ecotoxicol Environ Saf 120(9):66–73.  https://doi.org/10.1016/j.ecoenv.2015.05.026 CrossRefGoogle Scholar
  45. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151(1):59–66.  https://doi.org/10.1016/S0168-9452(99)00197-1
  46. Wang GY, Zhang SR, Xu XX, Zhong QM, Zhang CR, Jia YX, Li T, Deng OP, Li Y (2016) Heavy metal removal by GLDA washing: optimization, redistribution, recycling, and changes in soil fertility. Sci Total Environ 569–570:557–568.  https://doi.org/10.1016/j.scitotenv.2016.06.155 CrossRefGoogle Scholar
  47. Wang LR, Li P,F Wen Y, Yang Q, Zhen LQ, Fu JL, Li YH, Li SS, Han CX, Li XH (2018a) Vitamin C exerts novel protective effects against cadmium toxicity in mouse spermatozoa by inducing the dephosphorylation of dihydrolipoamide dehydrogenase. Reprod Toxicol 75:23–32.  https://doi.org/10.1016/j.reprotox.2017.11.008
  48. Wang GY, Zhang SR, Zhong Q, Peijnenburg WJGM, Vijver MG (2018b) Feasibility of Chinese cabbage (Brassica bara) and lettuce (Lactuca sativa) cultivation in heavily metals—contaminated soil after washing with biodegradable chelators. J Clean Prod 197:479–490.  https://doi.org/10.1016/j.jclepro.2018.06.225 CrossRefGoogle Scholar
  49. Wu ZC, Zhao XH, Sun XC, Tian QL, Tang YF, Nie ZJ, Qu CJ, Chen ZX, Hu CX (2015) Antioxidant enzyme systems and the ascorbate—glutathione cycle as contributing factors to cadmium accumulation and tolerance in two oilseed rape cultivars (Brassica napus L.) under moderate cadmium stress. Chemosphere 138:526–536.  https://doi.org/10.1016/j.chemosphere.2015.06.080 CrossRefGoogle Scholar
  50. Zhang JJ, Wang YK, Zhou JH, Xie F, Guo QNLFF, Jin SF, Zhu HM, Yang H (2018) Reduced phytotoxicity of propazine on wheat, maize and rapeseed by salicylic acid. Ecotoxicol Environ Saf 162:42–50.  https://doi.org/10.1016/j.ecoenv.2018.06.068 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Agronomy and Biotechnology, Ministry of EducationSouthwest University/Engineering Research Center of South Upland AgricultureChongqingChina
  2. 2.College of Environmental ScienceSichuan Agricultural UniversityWenjiangChina

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