Skip to main content

Advertisement

Log in

Exogenously applied zinc and copper mitigate salinity effect in maize (Zea mays L.) by improving key physiological and biochemical attributes

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

Abstract

Zinc or copper deficiency and salinity are known soil problems and often occur simultaneously in agriculture soils. Plants undergo various changes in physiological and biochemical processes to respond to high salt in the growing medium. There is lack of information on the relation of exogenous application of Zn and Cu with important salinity tolerance mechanisms in plants. Therefore, the present study was conducted to determine the effect of foliar Zn and Cu on two maize cultivars (salt-tolerant cv. Yousafwala Hybrid and salt-sensitive cv. Hybrid 1898). Salinity caused a significant reduction in water and turgor potentials, stomatal conductance, and transpiration and photosynthetic rate, while increase in glycine betaine, proline, total soluble sugars, and total free amino acids was evident in plants under saline regimes. Furthermore, there was significant decline in P, N, Ca, K, Mn, Fe, Zn, and Cu and increase in Na and Cl contents in plants fed with NaCl salinity. Nitrate reductase activity was lower in salt-stressed plants. However, foliar application of Zn and Cu circumvented salinity effect on water relations, photosynthesis, and nutrition and this was attributed to the better antioxidant system and enhanced accumulation of glycine betaine, proline, total free amino acids, and sugars. The results of the present study suggested that Zn application was superior to Cu for mediating plant defense responses under salinity.

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

Abbreviations

P:

Phosphorous

N:

Nitrogen

Ca:

Calcium

K:

Potassium

Mn:

Manganese

Fe:

Iron

Zn:

Zinc

Cu:

Copper

Na:

Sodium

Cl:

Chloride

References

  • Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Egamberdieva D, Bhardwaj R, Ashraf M (2017) Zinc application mitigates the adverse effects of NaCl stress on mustard [Brassica juncea (L.) Czern & Coss] through modulating compatible organic solutes, antioxidant enzymes, and flavonoid content. J Plant Interact 12(1):429–437

    Article  CAS  Google Scholar 

  • Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S (2018) Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress. Protoplasma 255:163–174

    Article  CAS  Google Scholar 

  • Alzahrani Y, Kuşvuran A, Alharby HF, Kuşvuran S, Rady MM (2018) The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicol Environ Saf 154:187–196

    Article  CAS  Google Scholar 

  • Amirjani MR (2011) Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice. Int J Bot 7:73–81

    Article  CAS  Google Scholar 

  • Ashraf MA, Ashraf M (2012) Salt-induced variation in some potential physiochemical attributes of two genetically diverse spring wheat (Triticum aestivum L.) cultivars: photosynthesis and photosystem II efficiency. Pak J Bot 44:53–64

    CAS  Google Scholar 

  • Ashraf MA, Ashraf M (2016) Growth stage-based modulation in physiological and biochemical attributes of two genetically diverse wheat (Triticum aestivum L.) cultivars grown in salinized hydroponic culture. Environ Sci Pollut Res 23:6227–6243

    Article  CAS  Google Scholar 

  • Ashraf M, Harris P (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  CAS  Google Scholar 

  • Ashraf MA, Ashraf M, Shahbaz M (2012) Growth stage-based modulation in antioxidant defense system and proline accumulation in two hexaploid wheat (Triticum aestivum L.) cultivars differing in salinity tolerance. Flora-Morphology, Distribution, Functional Ecology of Plants 207:388–397

    Article  Google Scholar 

  • Ashraf MY, Iqbal N, Ashraf M, Akhter J (2014) Modulation of physiological and biochemical metabolites in salt stressed rice by foliar application of zinc. J Plant Nutr 37(3):447–457

    Article  CAS  Google Scholar 

  • Ashraf M, Iqbal M, Hussain I, Rasheed R (2015) Physiological and biochemical approaches for salinity tolerance. In: Managing salt tolerance in plants: molecular and genomic perspectives, p 79

  • Ashraf MA, Akbar A, Parveen A, Rasheed R, Hussain I, Iqbal M (2018) Phenological application of selenium differentially improves growth, oxidative defense and ion homeostasis in maize under salinity stress. Plant Physiol Biochem 123:268–280

    Article  CAS  Google Scholar 

  • Azevedo Neto ADD, Prisco JT, Enéas-Filho J, Lacerda CFD, Silva JV, Costa PHAD, Gomes-Filho E (2004) Effects of salt stress on plant growth, stomatal response and solute accumulation of different maize genotypes. Braz J Plant Physiol 16:31–38

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    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(1-2):248–254

    Article  CAS  Google Scholar 

  • Bremner J (1965) Total Nitrogen. In: Black CA (ed) Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy, Soil Science Society of America, Madison, pp 1149–1178

    Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  Google Scholar 

  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) (Third Edition). Academic Press, San Diego, pp. 191–248

  • Burkhead JL, Gogolin Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  CAS  Google Scholar 

  • Cakmak I (1994) Activity of ascorbate-dependent H O -scavenging enzymes and leaf chlorosis are enhanced in magnesium- and potassium-deficient leaves, but not in phosphorus-deficient leaves. J Exp Bot 45(9):1259–1266

    Article  CAS  Google Scholar 

  • Chance B, Maehly A (1955) Assay of catalase and peroxidase. Meth Enzymol 2:764–817

    Article  Google Scholar 

  • Çiçek N, Oukarroum A, Strasser RJ, Schansker G (2017) Salt stress effects on the photosynthetic electron transport chain in two chickpea lines differing in their salt stress tolerance. Photosynth Res:1–11

  • Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad)1. J Exp Bot 52(358):1101–1109

    Article  CAS  Google Scholar 

  • Eker S, Heybet EH, Barut H, Erdem H (2013) Effects of zinc on growth and sodium, potassium and calcium concentrations of shoot in bread wheat under salt stress. Fresenius Environ Bull 22:1622–1627

    CAS  Google Scholar 

  • Elhindi KM, Al-Suhaibani NA, El-Din AFS, Yakout SM, Al-Amri SM (2016) Effect of foliar-applied iron and zinc on growth rate and essential oil in sweet basil (Ocimum basilicum L.) under saline conditions. Prog Nutr 18(3):288–298

    Google Scholar 

  • Farooq M, Hussain M, Wakeel A, Siddique KHM (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review. Agron Sustain Dev 35:461–481

    Article  CAS  Google Scholar 

  • Feki K, Tounsi S, Brini F (2018) Comparison of an antioxidant system in tolerant and susceptible wheat seedlings in response to salt stress. Span J Agric Res 15:0805

    Article  Google Scholar 

  • Fukami J, de la Osa C, Ollero FJ, Megías M, Hungria M (2018) Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Funct Plant Biol 45:328–339

    Article  CAS  Google Scholar 

  • Geilfus C-M, Ludwig-Müller J, Bárdos G, Zörb C (2018) Early response to salt ions in maize (Zea mays L.). J Plant Physiol 220:173–180

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide Dismutases: I. Occurrence in Higher Plants. Plant Physiol 59(2):309–314

    Article  CAS  Google Scholar 

  • Goussi R, Barbato R, Abdelly C, Manaa A, Derbali W (2018) comparative analysis of short and long term salt stress on the photosynthetic apparatus and chloroplast ultrastructure of Thellungiella salsuginea. World Acad Sci Eng Technol 12(9):1528

  • Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70(2):303–307

    Article  CAS  Google Scholar 

  • Hamilton PB, Van-Slyke DD (1943) Amino acid determination with ninhydrin. J Biol Chem 150:231–233

    CAS  Google Scholar 

  • Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    Article  CAS  Google Scholar 

  • Hejazi-Mehrizi M, Shariatmadari H, Khoshgoftarmanesh AH, Dehghani F (2011) Copper effects on growth, lipid peroxidation, and total phenolic content of rosemary leaves under salinity stress. J Agric Sci Technol 14(1):205–212

    Google Scholar 

  • Hu Y, Schmidhalter U (1997) Interactive effects of salinity and macronutrient level on wheat. II. Composition. J Plant Nutr 20:1169–1182

    Article  CAS  Google Scholar 

  • Ibrahim W, Ahmed IM, Chen X, Wu F (2017) Genotype-dependent alleviation effects of exogenous GSH on salinity stress in cotton is related to improvement in chlorophyll content, photosynthetic performance, and leaf/root ultrastructure. Environ Sci Pollut Res 24:9417–9427

    Article  CAS  Google Scholar 

  • Jackson ML (1962) Soil Chemical Analysis, 1st edn. Prentice Hall, New Jersey, p 498

    Google Scholar 

  • Jiang C, Zu C, Lu D, Zheng Q, Shen J, Wang H, Li D (2017) Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Sci Rep 7:42039

    Article  CAS  Google Scholar 

  • Kaya C, Akram N, Ashraf M, Sonmez O (2017) Exogenous application of humic acid mitigates salinity stress in maize (Zea mays L.) plants by improving some key physico-biochemical attributes. Cereal Res Commun:1–12

  • Kaya C, Ashraf M, Akram NA (2018) Hydrogen sulfide regulates the levels of key metabolites and antioxidant defense system to counteract oxidative stress in pepper (Capsicum annuum L.) plants exposed to high zinc regime. Environ Sci Pollut Res 25(13):12612–12618

  • Klein A, Hüsselmann L, Keyster M, Ludidi N (2018) Exogenous nitric oxide limits salt-induced oxidative damage in maize by altering superoxide dismutase activity. S Afr J Bot 115:44–49

    Article  CAS  Google Scholar 

  • Marschner H (2011) Marschner's mineral nutrition of higher plants, 3rd edn. Academic press, US

  • Padua M, Cavaco AM, Aubert S, Bligny R, Casimiro A (2010) Effects of copper on the photosynthesis of intact chloroplasts: interaction with manganese. Physiol Plant 138(3):301–311. https://doi.org/10.1111/j.1399-3054.2009.01335.x

    Article  CAS  Google Scholar 

  • Pilon M, Abdel-Ghany SE, Cohu CM, Gogolin KA, Ye H (2006) Copper cofactor delivery in plant cells. Curr Opin Plant Biol 9:256–263

    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(11):1716–1725

    Article  CAS  Google Scholar 

  • Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars. Plant Signal Behav 4:388–393

    Article  CAS  Google Scholar 

  • Saeidnejad AH, 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. Commun Soil Sci Plant Anal 47(8):1048–1057

    Article  CAS  Google Scholar 

  • Shaverdi AM, Omidi H, Tabatabaei S (2018) Morpho-physiological response of stevia (Stevia rebaudiana bertoni) to salinity under hydroponic culture condition (a case study in Iran). Appl Ecol Environ Res 16:17–28

    Article  Google Scholar 

  • Sym GJ (1984) Optimisation of the in-vivo assay conditions for nitrate reductase in barley (Hordeum vulgare L. cv. Igri). J Sci Food Agric 35(7):725–730

    Article  CAS  Google Scholar 

  • Syuhada N, Jahan MS, Nashriyah M, Khairi M, Nozulaidi M, Razali MHB (2014) Application of copper increased corn yield through enhancing physiological functions. Aust J Basic Appl Sci 8(16):282–286

    CAS  Google Scholar 

  • Torabian S, Zahedi M, Khoshgoftar AH (2016) Effects of foliar spray of two kinds of zinc oxide on the growth and ion concentration of sunflower cultivars under salt stress. J Plant Nutr 39(2):172–180

    Article  CAS  Google Scholar 

  • Tufail A, Li H, Naeem A, Li TX, Thiel G (2018) Leaf cell membrane stability-based mechanisms of zinc nutrition in mitigating salinity stress in rice. Plant Biol 20(2):338–345

    Article  CAS  Google Scholar 

  • Vallee BL, Auld DS (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29:5647–5659

    Article  CAS  Google Scholar 

  • Vinit-Dunand F, Epron D, Alaoui-Sossé B, Badot P-M (2002) Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants. Plant Sci 163:53–58

    Article  CAS  Google Scholar 

  • Wang X, Wang W, Huang J, Peng S, Xiong D (2018) Diffusional conductance to CO2 is the key limitation to photosynthesis in salt‐stressed leaves of rice (Oryza sativa). Physiol Plant 163:45-58

  • Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012) Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics 5: 60

  • Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Badakhshan H (2014) Effects of Zinc Application on Growth, Absorption and Distribution of Mineral Nutrients Under Salinity Stress in Soybean ( L.). J Plant Nutr 37(14):2255–2269

    Article  CAS  Google Scholar 

  • Yamasaki H, Pilon M, Shikanai T (2008) How do plants respond to copper deficiency? Plant Signal Behav 3:231–232

    Article  Google Scholar 

  • Yasmeen A, Basra SMA, Farooq M, Rehman H, Hussain N, Athar HR (2013) Exogenous application of moringa leaf extract modulates the antioxidant enzyme system to improve wheat performance under saline conditions. Plant Growth Regul 69:225–233

    Article  CAS  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430

    Article  CAS  Google Scholar 

  • Zafar S, Ashraf MY, Saleem M (2018) Shift in physiological and biochemical processes in wheat supplied with zinc and potassium under saline condition. J Plant Nutr 41:19–28

    Article  CAS  Google Scholar 

  • Zhang M, Cao Y, Wang Z, Wang Z-q, Shi J, Liang X, Song W, Chen Q, Lai J, Jiang C (2018a) A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. New Phytol 217:1161–1176

    Article  CAS  Google Scholar 

  • Zhang W, Yu X, Li M, Lang D, Zhang X, Xie Z (2018b) Silicon promotes growth and root yield of Glycyrrhiza uralensis under salt and drought stresses through enhancing osmotic adjustment and regulating antioxidant metabolism. Crop Prot 107:1–11

    Article  CAS  Google Scholar 

  • Zonouri M, Javadi T, Ghaderi N, Saba MK (2014) Effect of foliar spraying of ascorbic acid on chlorophyll a, chlorophyll b, total chlorophyll, carotenoids, hydrogen peroxide, leaf temperature and leaf relative water content under drought stress in grapes. Bull Environ Pharmacol Life Sci 3:178–184

    Google Scholar 

Download references

Acknowledgements

The work presented in this manuscript is a part of Ph.D. work of Mr. Naveed Iqbal. The data reported in the manuscript have been taken from Mr. Naveed Iqbal’s Ph.D. thesis submitted to Government College University Faisalabad, Pakistan, and Higher Education Commission, Pakistan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rizwan Rasheed.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iqbal, M.N., Rasheed, R., Ashraf, M.Y. et al. Exogenously applied zinc and copper mitigate salinity effect in maize (Zea mays L.) by improving key physiological and biochemical attributes. Environ Sci Pollut Res 25, 23883–23896 (2018). https://doi.org/10.1007/s11356-018-2383-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-2383-6

Keywords

Navigation