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

  • Pooja Singh
  • Arvind Kumar ShuklaEmail author
  • Sanjib Kumar Behera
  • Pankaj Kumar Tiwari
Original Paper
  • 6 Downloads

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.

Keywords

Zn biofortification Super oxide dismutase Carbonic anhydrase Zn efficiency Wheat genotypes 

Notes

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.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Alloway BJ (2008) Zinc in soils and crop nutrition. Second edition, published by IZA and IFA, North American Version. International Plant Nutrition Institute, NorcrossGoogle Scholar
  2. Alloway BJ (2009) Soil factors associated with zinc deficiencies in crops and humans. Environ Geochem Health 31(5):537–548CrossRefGoogle Scholar
  3. 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 50:601–639CrossRefGoogle Scholar
  4. Bar-Akiva A, Lavon R (1969) Carbonic anhydrase activity as an indicator of zinc deficiency in citrus leaves. J Hortic Sci 44:359–362CrossRefGoogle Scholar
  5. Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287CrossRefGoogle Scholar
  6. 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):41–48CrossRefGoogle Scholar
  7. Bouis HE, Welch RM (2010) Biofortification—a sustainable agricultural strategy for reducing micronutrient malnutrition in the Global South. Crop Sci 50:S20–S32CrossRefGoogle Scholar
  8. Cakmak I (2002) Plant nutrition research priorities to meet human needs for food in sustainable ways. Plant Sci 247:3–24Google Scholar
  9. Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17CrossRefGoogle Scholar
  10. Cakmak I (2012) Harvest plus zinc fertilizer project: harvest zinc. Better Crops 96:17–19Google Scholar
  11. 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 188:1–10CrossRefGoogle Scholar
  12. 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 151:91–95CrossRefGoogle Scholar
  13. Cakmak I, Pfeiffer WH, Mc Clafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87(1):10–20CrossRefGoogle Scholar
  14. Cochran WG, Cox GM (1957) Experimental designs. Wiley, New YorkGoogle Scholar
  15. Coleman JE (1998) Zinc enzymes. Curr Opin Chem Biol 2:222–234CrossRefGoogle Scholar
  16. Fageria NK, Baligar VC, Clark RB (2002) Micronutrients in crop production. Adv Agron 77:185–250CrossRefGoogle Scholar
  17. Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11CrossRefGoogle Scholar
  18. Furlani AMC, Furlani PR, Meda AR, Duarte AP (2005) Efficiency of maize cultivars for zinc uptake and use. Sci Agric 62:264–273CrossRefGoogle Scholar
  19. Genc Y, McDonald GK, Graham RD (2006) Contribution of different mechanisms to zinc efficiency in bread wheat during early vegetative stage. Plant Soil 281:353–367CrossRefGoogle Scholar
  20. 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):14–23Google Scholar
  21. 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 401:331–346CrossRefGoogle Scholar
  22. 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 107–114CrossRefGoogle Scholar
  23. Graham RD, Ascher JS, Hynes SC (1992) Selecting zinc efficient cereal genotypes for soils of low zinc status. Plant Soil 146:241–250CrossRefGoogle Scholar
  24. 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 92:1–74CrossRefGoogle Scholar
  25. Hacisalihoglu G, Kochian LV (2003) How do some plants tolerate low levels of soil zinc? Mechanisms of zinc efficiency in crop plants. New Phytol 159:341–350CrossRefGoogle Scholar
  26. 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 131:595–602CrossRefGoogle Scholar
  27. 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):72–75Google Scholar
  28. Haslett BS, Reid RJ, Rengel Z (2001) Zinc mobility in wheat: uptake and distribution of zinc applied to leaves or roots. Ann Bot 87:379–386CrossRefGoogle Scholar
  29. 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):3775–3781Google Scholar
  30. 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):112–126Google Scholar
  31. 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 361:279–290CrossRefGoogle Scholar
  32. Jackson ML (1973) Soil Chemical Analysis. Prentice Hall of India Pvt. Ltd, New DelhiGoogle Scholar
  33. 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):571–577CrossRefGoogle Scholar
  34. 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 313–348CrossRefGoogle Scholar
  35. 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 20:494–504CrossRefGoogle Scholar
  36. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–448CrossRefGoogle Scholar
  37. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 41:225–231Google Scholar
  40. Maqsood MA, Hussain S, Aziz T, Ashraf M (2011) Wheat-exuded organic acids influence zinc release from calcareous soils. Pedosphere 21(5):657–665CrossRefGoogle Scholar
  41. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, LondonGoogle Scholar
  42. 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):567–572CrossRefGoogle Scholar
  43. Miller E, Tulyathan O, Isacoff E, Chang C (2007) Molecular imaging of hydrogen peroxide produced for cell signaling. Nat Chem Biol 3(5):263–267CrossRefGoogle Scholar
  44. Nazir Q, Arshad Q, Kanwal S, Mahmood S (2014) Zinc deficient cereals in developing world. Technol Times 05:37Google Scholar
  45. 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 18:1195–1200CrossRefGoogle Scholar
  46. O’Lgrainy MH (1982) Phosphoenolpyruvate carboxylase: an enzymologist’s view. Annu Rev Plant Physiol 33:297–315CrossRefGoogle Scholar
  47. Rengel Z (1995) Carbonic anhydrase activity in leaves of wheat genotypes differing in Zn efficiency. J Plant Physiol 147:251–256CrossRefGoogle Scholar
  48. 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 227–265Google Scholar
  49. Rengel Z, Graham RD (1995) Importance of seed Zn content for wheat growth on Zn-deficient soil. Plant Soil 173:267–274CrossRefGoogle Scholar
  50. SAS Institute (2011) The SAS system for Windows, Release 9.2. SAS Inst., CaryGoogle Scholar
  51. 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, BhopalGoogle Scholar
  52. Shukla AK, Pakhare A (2015) Trace elements in soil-plant-human continuum. In: Rattan RK et al (eds) Soil science: an introduction. ISSS, New DelhiGoogle Scholar
  53. 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 1–196Google Scholar
  54. Shukla AK, Tiwari PK, Prakash C (2014) Micronutrients deficiencies vis-à-vis food and nutritional security of India. Indian J Fert 10(12):94–112Google Scholar
  55. Shukla AK, Tiwari PK, Pakhare A, Prakash C (2016) Zinc and Iron in soil, plant, animal and human health. Indian J Fert 12(11):133–149Google Scholar
  56. 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 34:449–464CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 37:29–38CrossRefGoogle Scholar
  59. 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):33–45Google Scholar
  60. Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364CrossRefGoogle Scholar
  61. Wilbur KM, Anderson GA (1948) Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 176:147–154Google Scholar
  62. 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
  63. 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):535–543CrossRefGoogle Scholar
  64. Yu Q, Rengel Z (1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Ann Bot 83:175–182CrossRefGoogle Scholar
  65. Zhang WH, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW (2007) Nutrient loading of developing seeds. Funct Plant Biol 34:314–331CrossRefGoogle Scholar
  66. 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 107:1–32CrossRefGoogle Scholar
  67. 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 58:12268–12274CrossRefGoogle Scholar
  68. 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 94:2016–2022CrossRefGoogle Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  1. 1.Rajmata Vijayaraje Scindia Krishi ViswavidyalayaGwaliorIndia
  2. 2.ICAR-Indian Institute of Soil ScienceBhopalIndia

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