Articles

Harnessing diversity in durum wheat (Triticum turgidum L.) to enhance climate resilience and micronutrient concentration through genetic and agronomic biofortification

Published:
December 6, 2022
Authors
View
Keywords
License

Copyright (c) 2022 by the Author(s)

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

How To Cite
Selected Style: APA
Melash, A. A., Vad, A., Bytyqi, B., & Éva Babett Ábrahám. (2022). Harnessing diversity in durum wheat (Triticum turgidum L.) to enhance climate resilience and micronutrient concentration through genetic and agronomic biofortification. Acta Agraria Debreceniensis, 2, 9-20. https://doi.org/10.34101/actaagrar/2/11053
Received 2022-05-05
Accepted 2022-10-03
Published 2022-12-06
Abstract

Huge consumption of wheat-driven food products with low bioavailability and small concentrations of zinc is responsible for zinc-induced malnutrition and associated health complications. The contemporary durum wheat varieties have inherently tiny zinc concentrations in developing grain, which cannot meet the daily human zinc demand. Despite the fact that over two billion people are suffering from iron and zinc-induced malnutrition, various intervention measures have been deployed to reverse the effect of zinc-induced malnutrition on humans. There are evidences that agronomic and genetic biofortification approaches can increase grain yield and nutritional quality (i.e. zinc, iron, protein, and vitamins) of durum wheat to a greater extent. However, there is a lack of direct empirical evidence for which the influence of both biofortification approaches on improving human health. Application of micronutrient-containing fertilizers either in the soil or foliarly is effective in combination with NPK, organic fertilizers coupled with efficient durum wheat varieties, emphasizing the need for integrated soil fertility management (ISFM). Although genetic biofortification is a cost-effective and sustainable approach, agronomic biofortification provides an immediate and effective route to enhancing micronutrient concentrations in durum wheat grain. The application of zinc-containing fertilizers is more effective under drought conditions than in normal growing situations. Hence, this article provides a key information for agronomists and breeders about the potential of biofortification interventions to improve durum wheat yield and enrich the grain qualitative traits to ensure food and nutritional security of the ever-increasing world population.

References
  1. Abdoli, M.–Esfandiari, E.−Mousavi, S.B.−Sadeghzadeh, B. (2014): Effects of foliar application of zinc sulfate at different phenological stages on yield formation and grain zinc content of bread wheat (cv. Kohdasht). Azarian Journal of Agriculture. 1: 11–16.
  2. Alloway, B. (2009): Soil Factors Associated with Zn Deficiency in Crops and Humans. Environmental Geochemistry and Health. 31: 537–548. http://dx.doi.org/10.1007/s10653-009-9255-4
  3. Ambuj, B.–Thomas, D. (2020): Biofortification of Pulse Crops: Status and Future Perspectives. Plants. 9: 73. doi:10.3390/plants9010073
  4. Badakhshan, H.–Moradi, N.–Mohammadzadeh, H.–Zakeri, M.R. (2013): Genetic variability analysis of grains Fe, Zn and beta-carotene concentration of prevalent wheat varieties in Iran. Int. J. Agric. Crop Sci. 2013, 6, 57.
  5. Bagci, S.A.–Ekiz, H.–Yilmaz, A.–Cakmak, I. (2007): Effects of Zinc Deficiency and Drought on Grain Yield of Field-grown Wheat Cultivars in Central Anatolia. Journal of Agronomy and Crop Science. 193: 198–206. https://doi.org/10.1111/j.1439-037X.2007.00256.x
  6. Bailey, R.–West, K.–Black, R. (2015): The epidemiology of global micronutrient deficiencies. Ann. Nutr. Metab. 66: 22–33.
  7. Blancquaert, D.–De Steur, H.–Gellynck, X.–Van Der Straeten, D. (2014): Present and future of folate biofortification of crop plants. J. Exp. Bot. 65: 895–906.
  8. Borrill, P.–Connorton, J.–Balk, J.–Miller, T.–Sanders, D.–Uauy, C. (2014): Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops. Frontiers in Plant Science. 5. https://doi.org/10.3389/fpls.2014.00053
  9. Bouis, H.–Hotz, C.–McClafferty, B.–Meenakshi, J.–Pfeiffer, W. (2011): Biofortification: A new tool to reduce micronutrient malnutrition. Food Nutr. Bull. 32: 31–40.
  10. Bouis, H.–Saltzman, A. (2017): Improving nutrition through biofortification: A review of evidence from HarvestPlus, 2003 through 2016. Glob. Food Sec. 12: 49–58. https://doi.org/10.1016/j.gfs.2017.01.009
  11. Bouis, H.–Welch, R. (2010): Biofortification—A Sustainable Agricultural Strategy for Reducing Micronutrient Malnutrition in the Global South. Crop Science. 50: 20–32.
  12. Cakmak, I. (2012): Zinc Fertilizer Strategy for Improving Yield. The Fluid Journal, 20, 4–7. https://fluidfertilizer.org/wp-content/uploads/2016/05/W12-A1.pdf
  13. Cakmak, I.–Kutman, U.B. (2018): Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci, 69: 172–180. https://doi.org/10.1111/ejss.12437
  14. Cakmak, I.–Pfeiffer, W.–McClafferty, B. (2010): Biofortification of Durum Wheat with Zinc and Iron. Cereal Chemistry. 87: 10–20. http://dx.doi.org/10.1094/CCHEM-87-1-0010
  15. Cakmak, I.–Torun, A.–Millet, E.–Feldman, M.–Fahima, T.–Korol A.–Nevo, E.–Braun H.–Ozkan, H. (2004): Triticum dicoccoides: An Important Genetic Resource for Increasing Zinc and Iron Concentration in Modern Cultivated Wheat. Soil Science and Plant Nutrition. 50: 1047–1054. http://dx.doi.org/10.1080/00380768.2004.10408573
  16. Calderini, D.–Ortiz-Monasterio, I. (2003): Are synthetic hexaploids a means of increasing grain element concentrations in wheat? Euphytica. 134:169–178.
  17. Carvalho, S.–Vasconcelos, M. (2013): Producing more with less: Strategies and novel technologies for plant-based food biofortification. Food Res. Int. 54: 961–971.
  18. Chizuru, N.–Ricardo, U.–Shiriki, K.–Prakash, S. (2003): The joint WHO/FAO expert consultation on diet, nutrition and the prevention of chronic diseases: process, product and policy implications. Public Health Nutr. 7:245–50. doi:10.1079/PHN2003592
  19. Collard, B.C.–Mackill, D.J. (2008): Marker assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond Ser B Biol Sci. 363: 557–572. https://doi.org/10.1098/rstb.2007.2170.
  20. Conti, M.–Cubadda, F.–Carcea, M. (2000): Trace Metals in Soft and Durum Wheat from Italy. Food Additives & Contaminants. 17: 45–53. http://dx.doi.org/10.1080/026520300283577
  21. De Valença, A.–Bake, A.–Brouwer, I.–Giller, K. (2017): Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa. Global Food Security. 12: 8–14. https://doi.org/10.1016/j.gfs.2016.12.001.
  22. Dhaliwal, S.S.–Sadana, U.S.–Manchanda, J.S.–Khurana, M.P.–Shukla, A.K. (2013): Differential response of maize cultivars to iron (Fe) applied through ferti-fortification. Indian J. Fertil. 9: 52–57.
  23. Dhaliwal, S.S.–Sharma, V.–Shukla, A.K.–Verma, V.–Kaur, M.–Shivay, Y.S.–Nisar, S.–Gaber, A.–Brestic, M.–Barek, V.–Skalicky, M.–Ondrisik, P.–Hossain, A. (2022): Biofortification–A Frontier Novel Approach to Enrich Micronutrients in Field Crops to Encounter the Nutritional Security. Molecules. 27: 1340. https://doi.org/10.3390/molecules27041340
  24. Erenoglu, E.B.−Kutman, U.B.−Ceylan, Y.−Yildiz, B.−Cakmak, I. (2011): Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytologist. 189: 438–448.
  25. FAO (2020): The State of Food Insecurity in the World: High Food Prices and Food Security-Threats and Opportunities. Rome. http://www.fao.org/publications/sofi/2020/en/
  26. Frison, E.A.–Cherfas, J.–Hodgkin, T. (2011): Agricultural Biodiversity Is Essential for a Sustainable Improvement in Food and Nutrition Security. Sustainability. 3: 238–253. https://doi.org/10.3390/su3010238
  27. Garg, M.–Sharma, N.–Sharma, S.–Kapoor, P.–Kumar, A.–Chunduri, V.–Arora, P. (2018): Biofortified Crops Generated by Breeding, Agronomy, and Transgenic Approaches Are Improving Lives of Millions of People around the World. Frontiers in Nutrition. 5: 12. DOI.10.3389/fnut.2018.00012
  28. Gómez-Galera, S.–Rojas, E.–Sudhakar, D.–Zhu, C.–Pelacho, A.M.–Capell, T.–Christou P. (2010): Critical evaluation of strategies for mineral fortification of staple food crops. Transgenic Res. 19:165–180.
  29. Gopalakrishnan, S.–Vadlamudi, S.–Samineni, S.–Kumar, C. (2016): Plant growth-promotion and biofortification of chickpea and pigeonpea through inoculation of biocontrol potential bacteria, isolated from organic soils. Springerplus. 5: 1882.
  30. Górniak, W.–Cholewińska, P.–Konkol, D. (2018): Feed additives produced on the basis of organic forms of micronutrients as a means of biofortification of food of animal origin. J. Chem. 8084127. https://doi.org/10.1155/2018/8084127
  31. Graham, R.–Senadhira, D.–Bebe, S.–Iglesias, C.–Monasterio, I. (1999): Breeding for micronutrient density in edible portions of staple food crops: conventional approaches. Field Crops Res. 60:57–80.
  32. Gupta, P.K.–Balyan, H.S.–Sharma, S.–Kumar, R. (2020): Biofortification and bioavailability of Zn, Fe and Se in wheat: Present status and future prospects. Theor. Appl. Genet. 2020: 1–35. https://doi.org/10.1007/s00122-020-03709-7
  33. Han, X. –Ding, S. –Lu, J. –Li, Y. (2022): Global, regional, and national burdens of common micronutrient deficiencies from 1990 to 2019: A secondary trend analysis based on the Global Burden of Disease 2019 study. eClinicalMedicine, 44, 101299. https://doi.org/10.1016/j.eclinm.2022.101299
  34. Hao, Y.–Zhang, Y.–He, Z. (2015): Progress in zinc biofortification of crops. Chin Bull Life Sci. 27:1047–54. doi: 10.13376/j.cbls/2015144
  35. Haslett, B.–Reid, R.–Rengel, Z. (2001): Zinc Mobility in Wheat: Uptake and Distribution of Zinc Applied to Leaves or Roots. Annals of Botany. 87: 379–386. http://dx.doi.org/10.1006/anbo.2000.1349.
  36. Hefferon, K. (2016): Can biofortified crops help attain food security? Curr. Mol. Biol. Rep. 2, 180–185.
  37. Hess, S.–King, J. (2009): Effects of Maternal Zinc Supplementation on Pregnancy and Lactation Outcomes. Food and Nutrition Bulletin. 30: 60–78. http://dx.doi.org/10.1177/15648265090301S105
  38. Hirschi, K. (2009): Nutrient biofortification of food crops. Annu Rev Nutr. 29:401–42
  39. Hotz, C. (2013): Biofortification, Editor(s): Benjamin Caballero, Encyclopedia of Human Nutrition (3rd Edition), Academic Press. Pp.175–181. https://doi.org/10.1016/B978-0-12-375083-9.00025-8.
  40. Huizar, M.–Arena, R.–Laddu, D. (2021): The global food syndemic: The impact of food insecurity, Malnutrition and obesity on the healthspan amid the COVID-19 pandemic. Progress in cardiovascular diseases. 64: 105–107. https://doi.org/10.1016/j.pcad.2020.07.002
  41. Impa, S.–Morete M.–Ismail, A.–Schulin, R.–Johnson-Beebout, S. (2013): Zn Uptake, Translocation, and Grain Zn Loading in Rice (Oryza sativa L.) Genotypes Selected for Zn Deficiency Tolerance and High Grain Zn. Journal of Experimental Botany. 64: 2739–2751. http://dx.doi.org/10.1093/jxb/ert118
  42. Kamaral, C.–Neate, S.M.–Gunasinghe, N.–Milham, P.J.–Paterson, D.J.–Kopittke, P.M. (2022): Genetic biofortification of wheat with zinc: Opportunities to fine-tune zinc uptake, transport and grain loading. Physiologia Plantarum. 174:1. e13612. https://doi.org/10.1111/ppl.13612
  43. Karim, M.R.–Zhang Y.Q.–Zhao, R.R.–Chen– X.P.–Zhang, F.S.–Zou, C.Q. (2012): Alleviation of drought stress in winter wheat by late foliar application of zinc, boron, and manganese. J. Plant Nutr. Soil Sci. 175: 142–151. https://doi.org/10.1002/jpln.201100141
  44. Khattak, S.G.–Dominy, P.J.–Ahmad, W. (2015): Effect of Zn as soil addition and foliar application on yield and protein content of wheat in alkaline soil. Journal of the National Science Foundation of Sri Lanka. 43:4, 303–312. DOI: http://doi.org/10.4038/jnsfsr.v43i4.7965
  45. Khokhar, J.S.–King, J.–King, I.P.–Young, S.D.–Foulkes, M.J.–DeSilva, J.–Weerasinghe, M.–Mossa, A.–Griffiths, S.–Riche, A.B. (2020): Novel sources of variation in grain Zinc (Zn) concentration in bread wheat germplasm derived from Watkins landraces. PLoS ONE 2020, 15, e0229107. https://doi.org/10.1371/journal.pone.0229107
  46. Khokhar, J.S.–Sareen, S.–Tyagi, B.S.–Singh, G.–Wilson, L.–King, I.P.–Young, S.D.–Broadley, M.R. (2018): Variation in grain Zn concentration, and the grain ionome, in field-grown Indian wheat. PLoS ONE. 13. e0192026. https://doi.org/10.1371/journal.pone.0192026
  47. Klikocka, H.–Marks, M. (2018): Sulphur and nitrogen fertilization as a potential means of agronomic biofortification to improve the content and uptake of microelements in spring wheat grain DM. J. Chem. 9326820. https://doi.org/10.1155/2018/9326820
  48. Kutman, U.B.–Yildiz, B.–Cakmak, I. (2011): Effect of nitrogen on uptake, remobilization and partitioning of zinc and iron throughout the development of durum wheat. Plant Soil. 342: 149–164. https://doi.org/10.1007/s11104-010-0679-5
  49. Lawson, P.–Daum, D.–Czauderna, R.–Meuser, H.–Härtling, J. (2015): Soil versus foliar iodine fertilization as a biofortification strategy for field-grown vegetables. Frontiers in Plant Science. 6: 450. https://www.frontiersin.org/article/10.3389/fpls.2015.00450
  50. Ma, D.–Sun, D.–Wang, C.–Ding, H.–Qin, H.–Hou, J.–Huang, X.–Xie, Y.–Guo, 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
  51. Malik, K.A.–Maqbool, A. (2020): Transgenic Crops for Biofortification. Front. Sustain. Food Syst. 4:571402. https://doi.org/10.3389/fsufs.2020.571402
  52. Mao, H.–Wang, J.–Zan, Y.–Lyons, G.–Zou, C. (2014): Using Agronomic Biofortification to Boost Zinc, Selenium, and Iodine Concentrations of Food Crops Grown on the Loess Plateau in China. Journal of Soil Science and Plant Nutrition. 14: 459–470. http://dx.doi.org/10.4067/s0718-95162014005000036
  53. Maralian, H. (2009): Effect of Foliar Application of Zn and Fe on Wheat Yield and Quality. African Journal of Biotechnology. 8: 6795–6798.
  54. Mathpal, B.–Srivastava, P.–Shankhdhar, D.–Shankhdhar, S. (2015): Zinc Enrichment in Wheat Genotypes under Various Methods of Zinc Application. Plant, Soil and Environment. 61: 171–175. http://dx.doi.org/10.17221/41/2015-PSE
  55. Mayer, J.E. –Pfeiffer, W.H. –Bouis, P. (2008): Biofortified crops to alleviate micronutrient malnutrition. Curr. Opin. Plant Biol. 11:166–170.
  56. Melash, A.A.–Dejene, K.M. (2020): Improving Grain Micronutrient Content of Durum Wheat (Triticum turgidum var. durum) through Agronomic Biofortification to Alleviate the Hidden Hunger. Advances in Agriculture. 2020: 6. https://doi.org/10.1155/2020/7825413
  57. Melash, A.A.–Dejene, K.M.–Dereje, A.A.–Alemtsehay, T. (2019): The influence of seeding rate and micronutrients foliar application on grain yield and quality traits and micronutrients of durum wheat. Journal of Cereal Science. 85:221–227.
  58. Melash, A.–Mengistu, D.–Aberra, D. (2016): Linking Agriculture with Health through Genetic and Agronomic Biofortification. Agricultural Sciences. 7: 295–307. doi: 10.4236/as.2016.75029.
  59. Mostafa, I.–Islam, S.–Mondal, P.–Faruque, A.–Ahmed T.–Hossain, M. (2019): Factors affecting low coverage of the vitamin A supplementation program among young children admitted in an urban diarrheal treatment facility in Bangladesh. Glob Health Action. 12:1588513. doi: 10.1080/16549716.2019.1588513.
  60. Naqvi, S.–Zhu, C.–Farre, G.–Ramessar, K.–Bassie, L.–Breitenbach, J.–Perez Conesa, D.–Ros, G.–Sandmann, G.–Capell, T. (2009): Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc. Natl. Acad. Sci. USA 2009. 106:7762–7767.
  61. Narwal, R.–Malik, R.–Dahiya, R. (2010): Addressing Variations in Status of a Few Nutritionally Important Micronutrients in Wheat Crop. 19th World Congress of Soil Science, Soil Solutions for a Changing World, Brisbane, 1-6 August 2010, 1–3.
  62. Nestel, P.–Bouis, H.–Meenakshi, J.–Pfeiffer, W. (2006): Biofortification of Staple Food Crops. Journal of Nutrition. 136: 1064–1067.
  63. Ozturk, L.–Yazici, M.A.–Yucel, C.–Torun, A.–Cekic, C.–Bagci, A. –Ozkan, H.–Braun, H.J.–Sayers Z.–Cakmak, I. (2006): Concentration and localization of zinc during seed development and germination in wheat. Physiol Plant. 128:144–152. https://doi.org/10.1111/j.1399-3054.2006.00737.x
  64. Paine, J.A.–Shipton, C.A.–Chaggar, S.–Howells, R.M.–Kennedy, M.J.–Vernon, G.–Wright, S.Y.–Hinchliffe, E.–Adams, J.L.–Silverstone, A.L. (2005b): Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat. Biotechnol. 23: 482–487.
  65. Paine, J.–Shipton, C.–Chaggar, S. (2005a): Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol. 23: 482–487. https://doi.org/10.1038/nbt1082
  66. Peleg, Z.–Saranga, Y.–Yazici, A.–Fahima, T.–Ozturk, L.–Cakmak, I. (2008): Grain zinc, iron and protein concentrations and zinc-efficiency in wild emmer wheat under contrasting irrigation regimes. Plant Soil, 306:57–67.
  67. Phattarakul, N.–Rerkasem, B.–Li, L.–Wu, L.–Zou, C.–Ram, H.–Sohu, V.–Kang, B.–Surek, H.–Kalayci, M.–Yazici, A.–Zhang, –Cakmak, I. (2012): Biofortification of rice grain with zinc through zinc fertilization in different countries. Plant Soil, 361: 131–141.
  68. Prasad R.–Yashbir S.S.–Dinesh, K. (2014): Chapter Two - Agronomic Biofortification of Cereal Grains with Iron and Zinc. Editor(s): Donald L. Sparks. Advances in Agronomy, Academic Press. 125: 55–91. https://doi.org/10.1016/B978-0-12-800137-0.00002-9.
  69. Ram, H.–Sohu, V.S.–Cakmak, I.–Singh, K.–Buttar, G.S.–Sodhi, G.P.–Gill, H.S.–Bhagat, I.–Singh, P.–Dhaliwal, S.S. (2015): Agronomic fortification of rice and wheat grains with zinc for nutritional security. Curr. Sci. 129: 1171–1176.
  70. Ramaswami, B. (2007): Biofortified Crops and Biotechnology: A Political Economy Landscape for India. AgBioForum, 10, 170-177.
  71. Rao, B.K.–Krishnappa, K.–Srinivasarao, S.P.–Wani, K.L.–Sahrawat, K.L.–Pardhasaradhi, G. (2012): Alleviation of multinutrient deficiency for productivity enhancement of rain-fed soybean and finger millet in semi-arid region of India. Commun. Soil Sci. Plant Anal. 43: 1427–1435.
  72. Rengel, Z.–Batten, G.–Crowley, D. (1999): Agronomic approaches for improving the micronutrient density in edible portions of field crops. Field Crop. Res, 60, 27–40.
  73. Ruel, M.T.–Alderman, H. (2013): Nutrition-sensitive interventions and programmes: How can they help to accelerate progress in improving maternal and child nutrition? Lancet. 382, 9891:536–551.
  74. Samuel, S.M.–Ryan, W.K.–Itai, K.–Antonella, Z. –Joel, S. (2015): Effect of increased concentrations of atmospheric carbon dioxide on the global threat of zinc deficiency: a modelling study. The Lancet Global Health. 10: 639–645. https://doi.org/10.1016/S2214-109X(15)00093-5.
  75. Sharma, V.–Choudhary, M.–Kumar, P.–Choudhary, J.R. –Khokhar, J.S. –Kaushik, P. –Goli, S. (2021): Harnessing the Wild Relatives and Landraces for Fe and Zn Biofortification in Wheat through Genetic Interventions—A Review. Sustainability. 13: 12975. https://doi.org/10.3390/su132312975
  76. Shewry, P.R. −Pellny, T.K. −Lovegrove, A. (2016): Is modern wheat bad for health? Nature Plants. 2: 1–3.
  77. Shunmugam, A.–Bock, C.–Arganosa, G.–Georges, F.–Gray, G.–Warkentin, T. (2015): Accumulation of phosphorus-containing compounds in developing seeds of low-phytate pea (Pisum sativum L.) mutants. Plants. 4: 1–26.
  78. Singh, U.–Praharaj, C.S.–Singh, S.S.–Bohra, A. (2016): Biofortification: Introduction, approaches, limitations, and challenges. In Biofortification of Food Crops; Springer: New Delhi, India, 2016; pp. 3–18.
  79. Smith, S. E.–Read, D.J. (2008): Mycorrhizal Symbiosis, 3rd Edn. New York, NY: Academic Press, 1–769. doi: 10.1016/B978-012370526-6.50002-7
  80. Steur, H.D.–Mehta, S.–Gellynck, X.–Finkelstein, J.L. (2017): GM biofortified crops: Potential effects on targeting the micronutrient intake gap in human populations. Curr. Opin. Biotechnol. 44: 181–188. https://doi.org/10.1016/j.copbio.2017.02.003.
  81. Storozhenko, S.–De Brouwer, V.–Volckaert, M.–Navarrete, O.–Blancquaert, D.–Zhang G.F.–Lambert, W.–Van Der Straeten, D. (2007): Folate fortification of rice by metabolic engineering. Nat. Biotechnol. 25: 1277–1279.
  82. Trethowan, R.M.–Turner, M.A.–Chattha, T.M. (2010): Breeding Strategies to Adapt Crops to a Changing Climate. Adv. Glob. Chang. Res. 37: 155–174.
  83. UNICEF. The State of the world’s children (2019): Children, food and nutrition: growing well in a changing world. UNICEF, New York, https://www.unicef.org/reports/state-of-worlds-children-2019
  84. Vasconcelos, M.–Datta, K.–Oliva, N.–Khalekuzzaman, M.–Torrizo, L.–Krishnan, S.–Oliveira, M.–Goto, F.–Datta, S.K. (2003): Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci. 164:371–378. https://doi.org/10.1016/S0168-9452(02)00421-1.
  85. Velu, G.–Ortiz-Monasterio, I.–Cakmak, I.–Hao, Y.–Signh, R. (2014): Biofortification Strategies to Increase Grain Zinc and Iron Concentrations in Wheat. Journal of Cereal Sciences. 59: 365–372. http://dx.doi.org/10.1016/j.jcs.2013.09.001
  86. Velu, G.–Singh, R.–Huerta-Espino, J.–PeÑa-Bautista, R.–Arun, B.–Mahendru-Singh, A.–Yaqub Mujahid, M.–Sohu, V.–Mavi, G.–Crossa, J. (2012): Performance of Biofortified Spring Wheat Genotypes in Target Environments for Grain Zinc and Iron Concentrations. Field Crops Research. 137: 261–267. http://dx.doi.org/10.1016/j.fcr.2012.07.018
  87. Wang H.–Jin J. Y. (2007): Effects of zinc deficiency and drought on plant growth and metabolism of reactive oxygen species in maize (Zea mays L.). Agric. Sci. China. 6: 988–995. https://doi.org/10.1016/S1671-2927(07)60138-2.
  88. Welch, R. (2002): The Impact of Mineral Nutrients in Food Crops on Global Human Health. Plant and Soil. 247: 83–90. http://dx.doi.org/10.1023/A:1021140122921
  89. Welch, R.M–Graham, R.D. (2004): Breeding for micronutrients in staple food crops from a human nutrition perspective. Journal of Experimental Botany. 55: 353–364. https://doi.org/10.1093/jxb/erh064
  90. White, J.–Broadley, M.R. (2005): Biofortifying crops with essential mineral elements. Trends Plant Sci. 10:586–93. doi:10.1016/j.tplants.2005.10.001
  91. White, P.J.–Broadley, M. (2009): Biofortification of crops with seven mineral elements often lacking in human diets-iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 182, 49–84.
  92. Yilmaz, A.–Ekiz, H.–Torun, B.–Gultekin, I.–Karanlik, S.–Bagci, S. –Cakmak, I. (1997): Effect of Different Zinc Application Methods on Grain Yield and Zinc Concentration in Wheat Grown on Zinc-Deficient Calcareous Soils in Central Anatolia. Journal of Plant Nutrition. 20: 461–471. http://dx.doi.org/10.1080/01904169709365267
  93. Younes, K.A.–Raouf, S.S.–Reza, Seyed, S. (2016): Bio fertilizers and zinc effects on some physiological parameters of triticale under water-limitation condition. Journal of Plant Interactions. 11:1, 167–177. https://doi.org/10.1080/17429145.2016.1262914
  94. Zhang, Y.–Shi, R.–Rezaul, K.M.–Zhang, F.–Zou, C. (2010): Iron and Zinc Concentrations in Grain and Flour of Winter Wheat as Affected by Foliar Application. Journal of Agriculture and Food Chemistry. 58: 12268–12274. http://dx.doi.org/10.1021/jf103039k
  95. Zhao, F.J.–Shewry, P.R. (2011): Recent developments in modifying crops and agronomic practice to improve human health. Food Policy. 36: 94–101.
  96. Zingore, S.–Delve, R.J.–Nyamangara, J.–Giller, K.E. (2008): Multiple benefits of manure: the key to maintenance of soil fertility and restoration of depleted sandy soils on African smallholder farms. Nutr. Cycl. Agroecosyst. 80: 267–282. https://doi.org/10.1007/s10705-007-9142-2.