Skip to main content
SpringerLink
Log in

Zinc Application Enhances Superoxide Dismutase and Carbonic Anhydrase Activities in Zinc-Efficient and Zinc-Inefficient Wheat Genotypes

  • Original Paper
  • Published:
Journal of Soil Science and Plant Nutrition Aims and scope Submit manuscript

Abstract

Deficiency of zinc (Zn) in soils and crops of the world is established fact. There is need for application of Zn application and growing Zn-efficient crop genotypes to tide over the situation. However, information pertaining to application of Zn to Zn-efficient and Zn-inefficient crop genotypes grown in field condition on plant enzyme (wherein Zn is a co-factor) activities is limited. To investigate the influence of different Zn regimes on superoxide dismutase (SOD) and carbonic anhydrase (CA) activities of Zn-efficient and Zn-inefficient wheat genotypes, the present study was carried out comprising three each of Zn-efficient and Zn-inefficient genotypes of wheat grown under field experiment with four Zn treatments such as no Zn, soil Zn, foliar Zn, and both soil and foliar Zn. Application of Zn (soil/foliar/both) enhanced SOD and CA activities of both Zn-efficient and Zn-inefficient genotypes at pre- and post-anthesis growth stages of wheat compared to no Zn. Under no Zn, SOD activities were higher in both Zn-efficient and Zn-inefficient genotypes at post-anthesis stage; however, reverse was true for CA activities. Application Zn enhanced Zn concentration in leaves, stem, and grain of both Zn-efficient and Zn-inefficient genotypes. Grain Zn concentration increased by 25.1, 35.7, and 38.2% with soil, foliar, and both soil and foliar applications of Zn, respectively in Zn-inefficient genotypes and by 7.2, 21.1, and 30.6% with soil, foliar, and both and foliar applications of Zn, respectively in Zn-efficient genotypes, compared to no Zn. In Zn-efficient genotypes, SOD and CA activities contributed about 63 and 77% towards grain Zn concentration, respectively, whereas SOD and CA activities contributed about 50 and 66% towards grain Zn concentration, respectively in Zn-inefficient genotypes. The results indicated that both soil and foliar applications are needed for enhanced SOD and CA activities and plant Zn concentration in wheat. Physiological utilization of Zn plays an important role in Zn efficiency of wheat genotypes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alloway BJ (2008) Zinc in soils and crop nutrition. Second edition, published by IZA and IFA, North American Version. International Plant Nutrition Institute, Norcross

    Google Scholar 

  • Alloway BJ (2009) Soil factors associated with zinc deficiencies in crops and humans. Environ Geochem Health 31(5):537–548

    Article  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplast: scavenging of active oxygen and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  Google Scholar 

  • Bar-Akiva A, Lavon R (1969) Carbonic anhydrase activity as an indicator of zinc deficiency in citrus leaves. J Hortic Sci 44:359–362

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287

    Article  CAS  Google Scholar 

  • Bharti K, Pandey N, Shankhdhar D, Srivastava PC, Shankhdhar SC (2014) Effect of different zinc levels on activity of superoxide dismutase and acid phosphatases and organic acid exudation on wheat genotypes. Physiol Mol Biol Plants 20(1):41–48

    Article  CAS  Google Scholar 

  • Bouis HE, Welch RM (2010) Biofortification—a sustainable agricultural strategy for reducing micronutrient malnutrition in the Global South. Crop Sci 50:S20–S32

    Article  Google Scholar 

  • Cakmak I (2002) Plant nutrition research priorities to meet human needs for food in sustainable ways. Plant Sci 247:3–24

    CAS  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

    Article  CAS  Google Scholar 

  • Cakmak I (2012) Harvest plus zinc fertilizer project: harvest zinc. Better Crops 96:17–19

    Google Scholar 

  • Cakmak I, Ekiz H, Yilmaz A, Torun B, Koleli N, Gultekin I, Alkan AE (1997a) Differential response of rye, triticale, bread and durum wheats to zinc deficiency in calcareous soils. Plant Soil 188:1–10

    Article  CAS  Google Scholar 

  • Cakmak I, Ozturk L, Eker S, Torun B, Kalfa H, Yilmaz A (1997b) Concentration of Zn and activity of Cu/Zn SOD in leaves of rye and wheat genotypes differing in sensitivity to Zn deficiency. J Plant Physiol 151:91–95

    Article  CAS  Google Scholar 

  • Cakmak I, Pfeiffer WH, Mc Clafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87(1):10–20

    Article  CAS  Google Scholar 

  • Cochran WG, Cox GM (1957) Experimental designs. Wiley, New York

    Google Scholar 

  • Coleman JE (1998) Zinc enzymes. Curr Opin Chem Biol 2:222–234

    Article  CAS  Google Scholar 

  • Fageria NK, Baligar VC, Clark RB (2002) Micronutrients in crop production. Adv Agron 77:185–250

    Article  CAS  Google Scholar 

  • Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11

    Article  CAS  Google Scholar 

  • Furlani AMC, Furlani PR, Meda AR, Duarte AP (2005) Efficiency of maize cultivars for zinc uptake and use. Sci Agric 62:264–273

    Article  CAS  Google Scholar 

  • Genc Y, McDonald GK, Graham RD (2006) Contribution of different mechanisms to zinc efficiency in bread wheat during early vegetative stage. Plant Soil 281:353–367

    Article  CAS  Google Scholar 

  • Gibson RS, Hess SY, Hotz C, Brown KH (2008) Indicators of zinc status at the population level: a review of the evidence. Brit J Nutr 99(3):14–23

    Article  Google Scholar 

  • Gomez-Coronado F, Poblaciones MJ, Almeida AS, Cakmak I (2016) Zinc (Zn) concentration of bread wheat grown under Mediterranean conditions as affected by genotype and soil/foliar Zn application. Plant Soil 401:331–346

    Article  CAS  Google Scholar 

  • Graham RD, Rengel Z (1993) Genotypic variation in Zn uptake and utilization by plants. In: Robson D (ed) Zinc in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 107–114

    Chapter  Google Scholar 

  • Graham RD, Ascher JS, Hynes SC (1992) Selecting zinc efficient cereal genotypes for soils of low zinc status. Plant Soil 146:241–250

    Article  CAS  Google Scholar 

  • Graham RD, Welch RM, Saunders DA, Ortiz MI, Bouis HE, Bonierbale MD, Haan S, Burgos G, Thiele G, Liria R, Misner CA, Beebe SE, Potts MJ, Kadian M, Hobbs M, Gupta RK, Tomlow S (2007) Nutritious subsistence food system. Adv Agron 92:1–74

    Article  CAS  Google Scholar 

  • Hacisalihoglu G, Kochian LV (2003) How do some plants tolerate low levels of soil zinc? Mechanisms of zinc efficiency in crop plants. New Phytol 159:341–350

    Article  CAS  Google Scholar 

  • Hacisalihoglu G, Hart JJ, Wang Y, Cakmak I, Kochian LV (2003) Zinc efficiency is correlated with enhanced expression and activity of Cu/Zn superoxide dismutase and carbonic anhydrase in wheat. Plant Physiol 131:595–602

    Article  CAS  Google Scholar 

  • Han JL, Li YM, Ma CY (2004) The impact of zinc on crop growth and yield (review). J Hebei Normal Univ Sci Technol 18(4):72–75

    Google Scholar 

  • Haslett BS, Reid RJ, Rengel Z (2001) Zinc mobility in wheat: uptake and distribution of zinc applied to leaves or roots. Ann Bot 87:379–386

    Article  CAS  Google Scholar 

  • He HY, Feng BL, Gao XL, Gao JF, Liu PT, Zhang J (2009) Comparison on the flag leaf aging metabolism of different winter wheat genotypes under three planting models. Acta Ecol Sin 29(7):3775–3781

    CAS  Google Scholar 

  • Hidoto L, Worku W, Mohammed H, Taran B (2017) Effects of zinc application strategy on zinc content and productivity of chickpea grown under zinc deficient soils. J Soil Sci Plant Nutr 17(1):112–126

    CAS  Google Scholar 

  • Hussain S, Maqsood MA, Rengel Z, Aziz T (2012) Biofortification and estimated human bioavailability of zinc in wheat grains as influenced by methods of zinc application. Plant Soil 361:279–290

    Article  CAS  Google Scholar 

  • Jackson ML (1973) Soil Chemical Analysis. Prentice Hall of India Pvt. Ltd, New Delhi

    Google Scholar 

  • Jiang L, Zhang D, Song F, Zhang X, Shao Y, Li C (2013) Effects of zinc on growth and physiological characters of flag leaf and grains of winter wheat after anthesis. Adv J Food Sci Technol 5(5):571–577

    Article  CAS  Google Scholar 

  • Kannan S (1990) Role of foliar fertilization in plant nutrition. In: Baligar VC, Duncan RR (eds) Crops as enhancers of nutrient use. Academic Press, San Diego, pp 313–348

    Chapter  Google Scholar 

  • Kim KR, Owens G, Naidu R (2010) Effect of root induced chemical changes on dynamics and plant uptake of heavy metals in rhizosphere soils. Pedosphere 20:494–504

    Article  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–448

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Ma D, Sun D, Wang C, Ding H, Qin H, Hou J, Huang X, Xie Y, Gou T (2017) Physiological responses and yield of wheat plants in zinc-mediated alleviation of drought stress. Front Plant Sci 8:860. https://doi.org/10.3389/fpls.2017.00860

    Article  PubMed  PubMed Central  Google Scholar 

  • Maqsood MA, Rahmatullah, Kanwal S, Aziz T, Ashraf M (2009) Evaluation of Zn distribution among grain and straw of twelve indigenous wheat (Triticum aestivum L) genotypes. Pak J Bot 41:225–231

    CAS  Google Scholar 

  • Maqsood MA, Hussain S, Aziz T, Ashraf M (2011) Wheat-exuded organic acids influence zinc release from calcareous soils. Pedosphere 21(5):657–665

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Mathpal B, Srivastava PC, Shankhdhar D, Shankhdhar SC (2015) Improving key enzyme activities and quality of rice under various methods of zinc application. Physiol Mol Biol Plants 21(4):567–572

    Article  CAS  Google Scholar 

  • Miller E, Tulyathan O, Isacoff E, Chang C (2007) Molecular imaging of hydrogen peroxide produced for cell signaling. Nat Chem Biol 3(5):263–267

    Article  CAS  Google Scholar 

  • Nazir Q, Arshad Q, Kanwal S, Mahmood S (2014) Zinc deficient cereals in developing world. Technol Times 05:37

    Google Scholar 

  • Nazir Q, Arshad M, Aziz T, Shahid M (2016) Influence of zinc impregnated urea on growth, yield and grain zinc in rice (Oryza sativa). Int J Agric Biol 18:1195–1200

    Article  CAS  Google Scholar 

  • O’Lgrainy MH (1982) Phosphoenolpyruvate carboxylase: an enzymologist’s view. Annu Rev Plant Physiol 33:297–315

    Article  Google Scholar 

  • Rengel Z (1995) Carbonic anhydrase activity in leaves of wheat genotypes differing in Zn efficiency. J Plant Physiol 147:251–256

    Article  CAS  Google Scholar 

  • Rengel Z (1999) Physiological mechanisms underlying differential nutrient efficiency of crop genotypes. In: Rengel Z (ed) Mineral nutrition of crops-fundamental mechanisms and implications. Food Products Press, New York, pp 227–265

    Google Scholar 

  • Rengel Z, Graham RD (1995) Importance of seed Zn content for wheat growth on Zn-deficient soil. Plant Soil 173:267–274

    Article  CAS  Google Scholar 

  • SAS Institute (2011) The SAS system for Windows, Release 9.2. SAS Inst., Cary

    Google Scholar 

  • Shukla AK (2014) Understanding the mechanism of variation in status of a few nutritionally important micronutrients in some important food crops and the mechanism of micronutrient enrichment in plant parts, NAIP Funded Research Project Report. AICRP on Micronutrients, IISS, Nabibagh, Berasia Road, Bhopal

  • Shukla AK, Pakhare A (2015) Trace elements in soil-plant-human continuum. In: Rattan RK et al (eds) Soil science: an introduction. ISSS, New Delhi

    Google Scholar 

  • Shukla AK, Tiwari PK (2016) Micro and secondary nutrients and pollutant elements research in India. Coordinators Report- AICRP on Micro- and Secondary Nutrients and Pollutant Elements in Soils and Plants, ICAR-IISS, Bhopal. pp 1–196

  • Shukla AK, Tiwari PK, Prakash C (2014) Micronutrients deficiencies vis-à-vis food and nutritional security of India. Indian J Fert 10(12):94–112

    Google Scholar 

  • Shukla AK, Tiwari PK, Pakhare A, Prakash C (2016) Zinc and Iron in soil, plant, animal and human health. Indian J Fert 12(11):133–149

    Google Scholar 

  • Singh B, Singh BK (2011) Effect of reduced seed and applied zinc on zinc efficiency of wheat genotypes under zinc deficiency in nutrient solution culture. J Plant Nutr 34:449–464

    Article  CAS  Google Scholar 

  • Velu G, Crossa J, Singh RP, Hao Y, Dreisigacker S, Perez-Rodriguez P, Joshi AK, Chatrath R, Gupta V, Balasubramaniam A, Tiwari C, Mishra VK, Sohu VS, Mavi GS (2016) Genomic prediction of grain zinc and iron concentrations in spring wheat. Theor Appl Genet 129:1595–1605. https://doi.org/10.1007/S00122-016-2726-y

    Article  CAS  PubMed  Google Scholar 

  • Walkley AJ, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    Article  CAS  Google Scholar 

  • Wasaya A, Shabir MS, Hussain M, Ansar M (2017) Foliar application of zinc and boron improved the productivity and net returns of maize grown under rainfed conditions of Pothwar plateau. J Soil Sci Plant Nutr 17(1):33–45

    CAS  Google Scholar 

  • Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364

    Article  CAS  Google Scholar 

  • Wilbur KM, Anderson GA (1948) Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 176:147–154

    CAS  PubMed  Google Scholar 

  • Xu X, Yu Z, Kong J, Yi M, Huan C, Jiang L (2017) Molecular cloning and expression analysis of cu/Zn SOD gene from Gynura bicolor DC. J Chemi Article ID 5987096. https://doi.org/10.1155/2017/5987096

  • Yang XW, Tian XH, Gale WJ, Cao YX, Lu XC, Zhao AQ (2011) Effect of soil and foliar zinc application on zinc concentration and bioavailability in wheat grain grown on potentially zinc-deficient soil. Cereal Res Commun 39(4):535–543

    Article  CAS  Google Scholar 

  • Yu Q, Rengel Z (1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Ann Bot 83:175–182

    Article  CAS  Google Scholar 

  • Zhang WH, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW (2007) Nutrient loading of developing seeds. Funct Plant Biol 34:314–331

    Article  CAS  Google Scholar 

  • Zhang F, Shen J, Zhang J, Zuo Y, Li L, Chen X (2010a) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Adv Agron 107:1–32

    Article  CAS  Google Scholar 

  • Zhang Y, Shi R, Rezaul KMD, Zhang F, Zou C (2010b) Iron and zinc concentrations in grain and flour of winter wheat as affected by foliar application. J Agric Food Chem 58:12268–12274

    Article  CAS  Google Scholar 

  • Zhao AQ, Tian XH, Cao YX, Lu XC, Liu T (2014) Comparison of soil and foliar zinc application for enhancing grain zinc content of wheat when grown on potentially zinc-deficient calcareous soils. J Sci Food Agric 94:2016–2022

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Director, ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India, for providing the facilities to carry out the research work. The authors also express their gratitude to the editor and the anonymous reviewers for their suggestions to improve the manuscript.

Funding

The study was funded through National Agricultural Innovation Project (NAIP) (sub-project code: 417801-08) of Indian Council of Agriculture Research (ICAR), New Delhi.

Author information

Authors and Affiliations

  1. Rajmata Vijayaraje Scindia Krishi Viswavidyalaya, Gwalior, Madhya Pradesh, 474002, India

    Pooja Singh

  2. ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, 462038, India

    Arvind Kumar Shukla, Sanjib Kumar Behera & Pankaj Kumar Tiwari

Authors
  1. Pooja Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arvind Kumar Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sanjib Kumar Behera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pankaj Kumar Tiwari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arvind Kumar Shukla.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

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

Singh, P., Shukla, A.K., Behera, S.K. et al. Zinc Application Enhances Superoxide Dismutase and Carbonic Anhydrase Activities in Zinc-Efficient and Zinc-Inefficient Wheat Genotypes. J Soil Sci Plant Nutr 19, 477–487 (2019). https://doi.org/10.1007/s42729-019-00038-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42729-019-00038-7

Keywords

Search

Navigation