Effect of Zinc and Nickel Treatments on Improvement of the Osmotic Defense System of Wheat Plant Under Salinity Stress

Hamdia M. Abd El-Samad, Rania Mohamed Taha


The present experiments were performed to determine the effects of Zn (20 µM and 200 µM) and Ni (1 µM and 100 µM) on the growth and metabolic activities in the roots, shoots, and spikes of wheat (Triticum aestivum L.) cv. Gimiza 11 grown under different salinity conditions. In addition to identifying the osmotic tolerance of wheat, the roles of Zn and Ni in alleviating osmotic stress were examined. The root was the organ most sensitive to osmotic stress, whereas the shoot was the most resistant, and the spike was the intermediate. These three organs negatively responded to increasing osmotic stress levels, as fresh and dry matter decreased, and related biochemical parameters were adversely affected. However, fresh and dry matter were generally elevated when plants were supplemented with Zn or Ni under increasing osmotic stress. The sensitivity of roots was associated with depletion in the concentrations of sugars and free proline, whereas soluble protein and amino acid levels were increased. The stress tolerance of shoots and spikes was accompanied by an increase in soluble sugars, soluble proteins, and proline, while amino acid levels increased in spikes only. The Na+ and K+ content in wheat plants increased with increasing NaCl-induced osmotic stress levels. In turn, the accumulation and partitioning of Na+ and K+ did not vary among the three organs, both at different salt concentrations and between Zn or Ni treatments. Moreover, the present results show that the concentrations of anthocyanins, flavonoids, and L-ascorbic acid increased under exposure to osmotic stress and did not change significantly under Zn or Ni treatments.


heavy metals; monocot plants; abiotic stress; antioxidant products

Full Text:



Abd El-Samad, H. M. (2016). The physiological role of proline and sodium as osmotic stress signal components of some crop plants. Triticeae Genomics and Genetics, 7, 1–9.

Abd El-Samad, H. M., & Mostafa, D. (2018). Growth, metabolites, protein profile and esterase enzyme of wheat grown under osmotic stress with exogenous application of Allium sativum. American Journal of Plant Sciences, 9, 902–919. https://doi.org/10.4236/ajps.2018.94069

Abd El-Samad, H. M., Mostafa, D., & Abd El-Hakeem, K. N. (2017). The combined action strategy of two stresses, salinity and Cu++ on growth, metabolites and protein pattern of wheat plant. American Journal of Plant Sciences, 8, 625–643. https://doi.org/10.4236/ajps.2017.83043

Abd El-Samad, H. M., & Shaddad, M. A. K. (2016). Mechanisms of salt tolerance of wheat cultivars. Triticeae Genomics and Genetics, 7, 1–16.

Abd El-Samad, H. M., Shaddad, M. A. K., & Ragaey, M. M. (2019). Drought strategy tolerance of four barley cultivars and combined effect with salicylic acid application. American Journal of Plant Sciences, 10, 512–535. https://doi.org/10.4236/ajps.2019.104037

Alfocea, F. P., Estañ, M. T., Caro, M., & Bolarín, M. C. (1993). Response of tomato cultivars to salinity. Plant and Soil, 150, 203–211. https://doi.org/10.1007/BF00013017

Ali, H. E. M., & Ismail, G. S. M. (2014). Tomato fruit quality as influenced by salinity and nitric oxide. Turkish Journal of Botany, 38, 122–129. https://doi.org/10.3906/bot-1210-44

Arif, N., Yadav, V., Singh, S., Singh, S., Ahmad, P., Mishra, R. K., Sharma, S., Tripathi, D. K., Dubey, N. K., & Chauhan, D. K. (2016). Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Frontiers in Environmental Science, 4, Article 69. https://doi.org/10.3389/fenvs.2016.00069

Babu, M. A., Singh, D., & Gothandam, K. M. (2012). The effect of salinity on growth, hormones and mineral element. The Journal of Animal and Plant Sciences, 22, 159–164.

Baek, D., Chun, H. J., Kang, S., Shin, G., Park, S. J., Hong, H., Kim, C., Kim, D. H., Lee, S. Y., Kim, M. C., & Yun, D.-J. (2016). Role of Arabidopsis miR399f in salt, drought, and ABA signaling. Molecules and Cells, 39, 111–118. https://doi.org/10.14348/molcells.2016.2188

Bates, L. W., Waldern, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–207. https://doi.org/10.1007/BF00018060

Benabderrahim, M. A., Guiza, M., & Haddad, M. (2020). Genetic diversity of salt tolerance in tetraploid alfalfa (Medicago sativa L.). Acta Physiologiae Plantarum, 42, Article 5. https://doi.org/10.1007/s11738-019-2993-8

Bhalerao, S., Sharma, A. S., & Poojari, A. C. (2015). Toxicity of nickel in plants. International Journal of Pure and Applied Bioscience, 3, 345–355.

Borowiak, K., Gąsecka, M., Mleczek, M., Dąbrowski, J., Chadzinikolau, T., Magdziak, Z., Goliński, P., Rutkowski, P., & Kozubik, T. (2015). Photosynthetic activity in relation to chlorophylls, carbohydrates, phenolics and growth of a hybrid Salix purpurea × triandra × viminalis 2 at various Zn concentrations. Acta Physiologiae Plantarum, 37, Article 155. https://doi.org/10.1007/s11738-015-1904-x

Bracale, M., Levi, M., Savini, C., Dicorato, W., & Galli, M. G. (1997). Water deficit in pea root tips: Effect on the cell cycle and on the production of dehydrin-like proteins. Annals of Botany, 79, 593–600. https://doi.org/10.1006/anbo.1996.0356

Chakhchar, A., Lamaoui, M., Wahbi, S., Ferradous, A., El Mousadik, A., Ibnsouda-Koraichi, S., Filali-Maltouf, A., & El Modafar, C. (2015). Leaf water status, osmoregulation and secondary metabolism as a model for depicting drought tolerance in Argania spinosa. Acta Physiologiae Plantarum, 37, 80–96. https://doi.org/10.1007/s11738-015-1833-8

Chunthaburee, S., Sakuanrungsirkul, S., Wangwarat, T., Sanitchon, J., Pattanagul, W., & Theerakulisut, P. (2016). Changes in anthocyanin content and expression of anthocyanin synthesis genes in seedlings of black glutinous rice in response to salt stress. Asian Journal of Plant Sciences, 15, 56–65. https://doi.org/10.3923/ajps.2016.56.65

Clemens, S. (2006). Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie, 88, 1707–1719. https://doi.org/10.1016/j.biochi.2006.07.003

Das, S., Jahiruddin, M., Islam, M. R., Mahmud, A. A., Hossain, A., & Laing, A. M. (2020). Zinc biofortification in the grains of two wheat (Triticum aestivum L.) varieties through fertilization. Acta Agrobotanica, 73(1), Article 7312. https://doi.org/10.5586/aa.7312

de la Torre-González, A., Navarro-León, E., Blasco, B., & Ruiz, J. M. (2020). Nitrogen and photorespiration pathways, salt stress genotypic tolerance effects in tomato plants (Solanum lycopersicum L.). Acta Physioloiae Plantarum, 42, Article 2. https://doi.org/10.1007/s11738-019-2985-8

Fabiano, C. C., Tezotto, T., Favarin, J. L., Polacco, J. C., & Mazzafera, P. (2015). Essentiality of nickel in plants: A role in plant stresses. Frontiers in Plant Science, 6, Article 754. https://doi.org/10.3389/fpls.2015.00754

Fales, F. W. (1951). The assimilation and degradation of carbohydrate by yeast cells. Journal of Biological Chemistry, 193, 113–124. https://doi.org/10.1016/S0021-9258(19)52433-4

Garcia, A., Rizzo, C. A., Ud-Din, J., Bartos, S. L., Senadhira, D., Folwers, T. J., & Yeo, A. R. (1997). Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium: Potassium selectivity differs between rice and wheat. Plant Cell & Environment, 20, 1167–1174. https://doi.org/10.1046/j.1365-3040.1997.d01-146.x

Gorham, J. (1990). Salt tolerance in the Triticeae: K/Na discrimination in Aegilops species. Journal of Experimental Botany, 41, 615–621. https://doi.org/10.1093/jxb/41.5.615

Hameed, A., Gulzar, S., Aziz, I., Hussain, T., Gul, B., & Khan, M. A. (2015). Effects of salinity and ascorbic acid on growth, water status and antioxidant system in a perennial halophyte. AoB PLANTS, 7, Article plv004. https://doi.org/10.1093/aobpla/plv004

Harborne, A. J. (1998). Phytochemical methods: A guide to modern techniques of plant analysis (3rd ed.). Springer.

Helaly, M. N., Mohammed, Z., El-Shaeery, N. I., Abdelaal, K. A. A., & Nofal, I. E. (2017). Cucumber grafting onto pumpkin can represent an interesting tool to minimize salinity stress. Physiological and anatomical studies. Middle East Journal of Agricultural Research, 6, 953–975.

Hernández, J. A. (2019). Salinity tolerance in plants: Trends and perspectives. Salinity tolerance in plants: Trends and perspectives. International Journal of Molecular Sciences, 20, Article 2408. https://doi.org/10.3390/ijms20102408

Iqbal, M. J. (2018). Role of osmolytes and antioxidant enzymes for drought tolerance in wheat. In S. Fahad, A. Basir, & M. Adnan (Eds.), Global wheat production (pp. 51–65). IntechOpen. https://doi.org/10.5772/intechopen.75926

Jagetiya, B., Soni, A., & Yadav, S. (2013). Effect of nickel on plant water relations and growth in green gram. Indian Journal of Plant Physiology, 18, 372–376. https://doi.org/10.1007/s40502-013-0053-8

Jagota, S. K., & Dani, H. M. (1982). A new colorimetric technique for the estimation of vitamin C using Folin phenol reagent. Analytical Biochemistry, 127, 178–182. https://doi.org/10.1016/0003-2697(82)90162-2

Jamalomidi, M., Esfahani, M., & Carapetian, J. (2006). Zinc and salinity interaction on agronomical traits, chlorophyll and proline content in lowland rice (Oryza sativa L.) genotypes. Pakistan Journal of Biological Sciences, 9(7), 1315–1319. https://doi.org/10.3923/pjbs.2006.1315.1319

Koselski, M., Trebacz, K., & Dziubinska, H. (2019). The role of vacuolar ion channels in salt stress tolerance in the liverwort Conocephalum conicum. Acta Physiologiae Plantarum, 41, Article 110. https://doi.org/10.1007/s11738-019-2889-7

Krizek, D. T., Kramer, G. F., Upadhyaya, A., & Mirecki, R. M. (1993). UV-B response of cucumber seedlings grown under metal halide and high pressure sodium/deluxe lamps. Physiologia Plantarum, 88, 350–358. https://doi.org/10.1111/j.1399-3054.1993.tb05509.x

Li, X., Gao, G., Li, Y., Sun, W., He, X., Li, R., Jin, D., Qi, X., Liu, Z., & Bian, S. (2018). Functional roles of two 14-3-3s in response to salt stress in common bean. Acta Physiologiae Plantarum, 40, Article 209. https://doi.org/10.1007/s11738-018-2787-4

Lowry, O. H., Rasebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193, 265–275. https://doi.org/10.1016/S0021-9258(19)52451-6

Mahmoud, A. W. M., Abdeldaym, E. A., Abdelaziz, S. M., El-Sawy, M. B. I., & Mottaleb, S. A. (2020). Synergetic effects of zinc, boron, silicon, and zeolite nanoparticles on confer tolerance in potato plants subjected to salinity. Agronomy, 10, Article 19. https://doi.org/10.3390/agronomy10010019

Majid, M., Ali, A., & Essia, B. (2012). Effect of salinity on sodium and chloride uptake, proline and soluble carbohydrate contents in three alfalfa varieties. IOSR Journal of Agriculture and Veterinary Science, 1, 1–6. https://doi.org/10.9790/2380-0160106

Manivasagaperumal, R., Vijayarengan, P., Balamurugan, S., & Thiyagarajan, G. (2011). Effect of copper on growth, dry matter yield and nutrient content of Vigna radiata (L.) Wilczek. Journal of Phytology, 3, 53–62.

Meng, X., Zhou, J., & Sui, N. (2018). Mechanisms of salt tolerance in halophytes: Current understanding and recent advances. Open Life Sciences, 13, 149–154. https://doi.org/10.1515/biol-2018-0020

Mohammad, F., Bhat, J. A., Chen, C., Alyemeni, M. N., Wijaya, L., Ahmad, P., & Yu, F. (2021). Zinc oxide nanoparticles (ZnO-NPs) induce salt tolerance by improving the antioxidant system and photosynthetic machinery in tomato. Plant Physiology and Biochemistry, 161, 122–130. https://doi.org/10.1016/j.plaphy.2021.02.002

Moore, S., & Stein, W. H. (1948). Photometric ninhydrin method for use in the chromatography of amino acids. Journal of Biological Chemistry, 176, 367–388. https://doi.org/10.1016/S0021-9258(18)51034-6

Pandey, N., & Sharma, C. P. (2002). Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Science, 163(4), 753–758. https://doi.org/10.1016/S0168-9452(02)00210-8

Parlak, K. U. (2016). Effect of nickel on growth and biochemical characteristics of wheat (Triticum aestivum L.) seedlings. NJAS: Wageningen Journal of Life Sciences, 76, 1–5. https://doi.org/10.1016/j.njas.2012.07.001

Ribaut, J.-M., & Pilet, P.-E. (1991). Effects of water stress on growth, osmotic potential and abscisic acid content of maize roots. Physiologia Plantarum, 81(2), 156–162. https://doi.org/10.1111/j.1399-3054.1991.tb02123.x

Saeidnejad, A. H., Kafi, M., & Pessarakli, M. (2016). Interactive effects of salinity stress and Zn availability on physiological properties, antioxidant activity, and micronutrients content of wheat (Triticum aestivum) plants. Communications in Soil Sciences and Plants Analysis, 47, 1048–1057. https://doi.org/10.1080/00103624.2016.1165831

Steel, R. G. D., & Torrie, J. H. (1960). Principles and procedures of statistics. McGraw-Hill.

Stetsenko, L. A., Kozhevnikova, A. D., & Kartashov, A. V. (2017). Salinity attenuates nickel-accumulating capacity of Atropa belladonna L. plants. Russian Journal of Plant Physiology, 64, 486–496. https://doi.org/10.1134/S102144371704015X

Sun, S.-J., Guo, S.-Q., Yang, X., Bao, Y.-M., Tang, H.-J., Sun, H., Huang, J., & Zhang, H.-S. (2010). Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. Journal of Experimental Botany, 61, 2807–2818. https://doi.org/10.1093/jxb/erq120

Tolay, I. (2021). The impact of different zinc (Zn) levels on growth and nutrient uptake of basil (Ocimum basilicum L.) grown under salinity stress. PLoS ONE, 16, Article e0246493. https://doi.org/10.1371/journal.pone.0246493

Uddin, M. R., Nuruzzaman, M., Briste, P. S., Islam, M. M., Bhuiyan, A. K., Joy, M. I. H., Ahmed, S., & Khatun, A. (2021). Boron facilitates rice growth, development, and related attributes under saline soil conditions. Acta Agrobotanica, 74, Article 743. https://doi.org/10.5586/aa.743

Vahid Dastjerdi, M., Ehsanpour, A. A., & Forghani, A. H. (2021). The role of exogenous glycinebetaine on some antioxidant activity of non-T and T tobacco (Nicotiana tabacum L.) under in vitro salt stress. Acta Agriculturae Slovanic, 117, 1–9. https://doi.org/10.14720/aas.2021.117.3.1056

Wang, J.-Z., Jin, C., Wang, Y.-P., & Chen, B.-Q. (2019). Effects of salt stress on antioxidant system activity and peroxidation damage in root tip cells of strawberry. African Journal of Biotechnology, 18, Article 07AABD661594. https://doi.org/10.5897/AJB2019.16840

Williams, V., & Twine, S. (1960). Flame photometric method for sodium, potassium and calcium. In K. Peach & M. V. Tracey (Eds.), Modern methods of plant analysis (pp. 3–5). Springer.

Woodruff, D. R., & Meinzer, F. C. (2011). Water stress, shoot growth and storage of non-structural carbohydrates along a tree height gradient in a tall conifer. Plant Cell & Environment, 34(11), 1920–1930. https://doi.org/10.1111/j.1365-3040.2011.02388.x

Zhao, D., Gao, S., Zhang, X., Zhang, Z., Zheng, H., Rong, K., Zhao, W., & Khan, S. A. (2021). Impact of saline stress on the uptake of various macro and micronutrients and their associations with plant biomass and root traits in wheat. Plant, Soil and Environment, 67, 61–70. https://doi.org/10.17221/467/2020-PSE

DOI: https://doi.org/10.5586/aa.757

Journal ISSN:
  • 2300-357X (online)
  • 0065-0951 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Polish Botanical Society