Plant and Soil

, Volume 349, Issue 1–2, pp 215–225 | Cite as

Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers

  • Seher Bahar Aciksoz
  • Atilla Yazici
  • Levent Ozturk
  • Ismail Cakmak
Regular Article


Increasing iron (Fe) concentration in food crops is an important global challenge due to high incidence of Fe deficiency in human populations. Evidence is available showing that nitrogen (N) fertilization increases Fe concentration in wheat grain. This positive impact of N on grain Fe was, however, not studied under varied soil and foliar applications of Fe. Greenhouse experiments were conducted to investigate a role of soil- and foliar-applied Fe fertilizers in improving shoot and grain Fe concentration in durum wheat (Triticum durum) grown under increasing N supply as Ca-nitrate. Additionally, an effect of foliar Fe fertilizers on grain Fe was tested with and without urea in the spray solution. Application of various soil or foliar Fe fertilizers had either a little positive effect or remained ineffective on shoot or grain Fe. By contrast, at a given Fe treatment, raising N supply substantially enhanced shoot and grain concentrations of Fe and Zn. Improving N status of plants from low to sufficient resulted in a 3-fold increase in shoot Fe content (e.g., total Fe accumulated), whereas this increase was only 42% for total shoot dry weight. Inclusion of urea in foliar Fe fertilizers had a positive impact on grain Fe concentration. Nitrogen fertilization represents an important agronomic practice in increasing grain Fe. Therefore, the plant N status deserves special attention in biofortification of food crops with Fe.


Biofortification Iron Nitrogen Wheat Zinc 



The authors are grateful to Professor Zed Rengel for constructive comments on the manuscript and correction of the English text. This study was financially supported by the HarvestPlus Program ( and the sponsors of the HarvestPlus Global Zinc Fertilizer Project (e.g., Mosaic Company, K+S Kali, International Zinc Association, Omex Agrifluids, International Fertilizer Industry Association and International Plant Nutrition Institute).


  1. Abadia A, Sanz M, de las Rivas J, Abadia J (2002) Correction of iron chlorosis by foliar sprays. Acta Hortic 594:115–121Google Scholar
  2. Aciksoz SB, Ozturk L, Gokmen OO, Roemheld V. Cakmak I (2011) Effect of nitrogen on root release of phytosiderophores and root uptake of Fe(III)-phytosiderophore in Fe-deficient wheat plants. Physiol Plant. doi: 10.1111/j.1399-3054.2011.01460.x, in press
  3. Borg S, Brinch-Pedersen H, Tauris B, Holm PB (2009) Iron transport, deposition and bioavailability in the wheat and barley grain. Plant Soil 325:15–24CrossRefGoogle Scholar
  4. Bouis HE, Welch RM (2010) Biofortification - a sustainable agricultural strategy for reducing micronutrient malnutrition in the global south. Crop Sci 50:20–32CrossRefGoogle Scholar
  5. Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17CrossRefGoogle Scholar
  6. Cakmak I, Gulut KY, Marschner H, Graham RD (1994) Effects of zinc and iron deficiency on phytosiderophore release in wheat genotypes differing in zinc efficiency. J Plant Nutr 17:1–17CrossRefGoogle Scholar
  7. Cakmak I, Yilmaz A, Ekiz H, Torun B, Erenoglu B, Braun HJ (1996) Zinc deficiency as a critical nutritional problem in wheat production in Central Anatolia. Plant Soil 180:165–172CrossRefGoogle Scholar
  8. Cakmak I, Torun A, Millet E, Feldman M, Fahima T, Korol A, Nevo E, Braun HJ, Özkan H (2004) Triticum dicoccoides: an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Sci Plant Nutr 50:1047–1054CrossRefGoogle Scholar
  9. Cakmak I, Pfeiffer WH, McClafferty B (2010a) Biofortification of durum wheat with zinc and iron. Cereal Chem 87:10–20CrossRefGoogle Scholar
  10. Cakmak I, Kalayci M, Kaya Y, Torun AA, Aydin N, Wang Y, Arisoy Z, Erdem H, Gokmen O, Ozturk L, Horst WJ (2010b) Biofortification and localization of zinc in wheat grain. J Agr Food Chem 58:9092–9102Google Scholar
  11. Carter RC, Jacobson JL, Burden MJ, Armony-Sivan R, Dodge NC, Angelilli ML, Lozoff B, Jacobson SW (2010) Iron deficiency anemia and cognitive function in infancy. Pediatrics 126:427–434CrossRefGoogle Scholar
  12. Curie C, Cassin G, Couch D, Divol F, Higuchi K, Jean ML, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11PubMedCrossRefGoogle Scholar
  13. Distelfeld A, Cakmak I, Peleg Z, Ozturk L, Yazici AM, Budak H, Saranga Y, Fahima T (2007) Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Physiol Plant 129:635–643CrossRefGoogle Scholar
  14. Erenoglu EB, Kutman UB, 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 Phytol 189:438–448PubMedCrossRefGoogle Scholar
  15. Fageria NK, dos Santos AB, de Moraes MF (2010) Yield, potassium uptake and use efficiency in upland rice genotypes. Commun Soil Sci Plant Anal 41:2676–2684CrossRefGoogle Scholar
  16. Fernandez V, Ebert G (2005) Foliar iron fertilization: a critical review. J Plant Nutr 28:2113–2124CrossRefGoogle Scholar
  17. Fernandez V, Rio V, Abadia J, Abadia A (2006) Foliar iron fertilization of peach (Prunus persica (L.) Batsch): effects of iron compounds, surfactants and other adjuvants. Plant Soil 289:239–252CrossRefGoogle Scholar
  18. Fernandez V, Orera I, Abadia J, Abadia A (2009) Foliar iron-fertilisation of fruit trees: present knowledge and future perspectives - a review. J Hort Sci Biotech 84:1–6Google Scholar
  19. Gibson RS, Bailey KB, Gibbs M, Ferguson EL (2010) A review of phytate, iron, zinc, and calcium concentrations in plant-based complementary foods used in low-income countries and implications for bioavailability. Food Nutr Bull 31:134–146Google Scholar
  20. Gomez-Becerra HF, Erdem H, Yazici A, Tutus Y, Torun B, Ozturk L, Cakmak I (2010) Grain concentrations of protein and mineral nutrients in a large collection of spelt wheat grown under different environments. J Cereal Sci 52:342–349CrossRefGoogle Scholar
  21. Grusak MA, Pearson JN, Marentes E (1999) The physiology of micronutrient homeostasis in field crops. Field Crops Res 60:41–56CrossRefGoogle Scholar
  22. Gupta UC (1991) Iron statues of crops in Prince-Edward-Island and effect of soil-pH on plant iron concentration. Can J Soil Sci 71:197–202CrossRefGoogle Scholar
  23. Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506PubMedCrossRefGoogle Scholar
  24. Hunt JR (2005) Dietary and physiological factors that affect the absorption and bioavailability of iron. Int J Vitam Nutr Res 75:375–84PubMedCrossRefGoogle Scholar
  25. Hurrell RF, Lynch S, Bothwell T, Cori H, Glahn R, Hertrampf E, Kratky Z, Miller D, Rodenstein M, Streekstra H, Teucher B, Turner E, Yeung CK, Zimmerman MB (2004) Enhancing the absorption of fortification iron - a sustain task force report. Int J Vitam Nutr Res 74:387–401PubMedCrossRefGoogle Scholar
  26. Kirkby EA, Knight AH (1977) Influence of the level of nitrate nutrition on ion uptake and assimilation, organic acid accumulation, and cation-anion balance in whole tomato plants. Plant Physiol 60:349–353PubMedCrossRefGoogle Scholar
  27. Kutman UB, Yildiz B, Ozturk L, Cakmak I (2010) Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen. Cereal Chem 87:1–9CrossRefGoogle Scholar
  28. Kutman UB, 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 342:149–164CrossRefGoogle Scholar
  29. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428CrossRefGoogle Scholar
  30. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  31. Marschner H, Romheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9:695–713CrossRefGoogle Scholar
  32. McLeon E, Cogswell M, Egli I, Wojdyla D, de Benoist B (2009) Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Pub Health Nutr 12:444–454CrossRefGoogle Scholar
  33. Monsant AC, Wang Y, Tang C (2010) Nitrate nutrition enhances zinc hyperaccumulation in Noccaea caerulescens (Prayon). Plant Soil 336:391–404CrossRefGoogle Scholar
  34. Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in Graminaceae plants. Plant Cell Physiol 28:1081–1092Google Scholar
  35. Murata Y, Harada E, Sugase K, Namba K, Horikawa M, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T, Kusumoto S (2008) Specific transporter for iron(III)-phytosiderophore complex involved in iron uptake by barley roots. Pure Appl Chem 80:2689–2697CrossRefGoogle Scholar
  36. Pahlavan-Rad M, Pessarakli M (2009) Response of wheat plants to zinc, iron and manganese applications and uptake and concentration of zinc, iron and manganese in wheat grains. Commun Soil Sci Plant Anal 40:1322–1332CrossRefGoogle Scholar
  37. Peck AW, McDonald GK, Graham RD (2008) Zinc nutrition influences the protein composition of flour in bread wheat (Triticum aestivum L.). J Cereal Sci 47:266–274CrossRefGoogle Scholar
  38. Peterson CJ, Johnson VA, Mattern PJ (1986) Influence of cultivar and environment on mineral and protein concentrations of wheat flour, bran and grain. Cereal Chem 63:183–186Google Scholar
  39. Pfeiffer WH, McClafferty B (2007) Biofortification: breeding micronutrient-dense crops. In: Kang MS, Priyadarshan PM (eds) Breeding major food staples. Blackwell Science, New York, pp 61–91CrossRefGoogle Scholar
  40. Rengel Z, Batten GD, Crowley DE (1999) Agronomic approaches for improving teh micronutrient density inedible portions of field crops. Field Crop Res 60:27–40CrossRefGoogle Scholar
  41. Rodriguez-Lucena P, Apaolaza-Hernandez L, Lucena JJ (2010a) Comparison of iron chelates and complexes supplied as foliar sprays and in nutrient solution to correct iron chlorosis of soybean. J Plant Soil Sci 173:120–126CrossRefGoogle Scholar
  42. Rodriguez-Lucena P, Ropero E, Apaolaza-Hernandez L, Lucena JJ (2010b) Iron supply to soybean plants through the foliar application of IDHA/Fe3+: effect of plant nutritional status and adjuvants. J Sci Food Agric 90:2633–2640CrossRefGoogle Scholar
  43. Römheld V (1991) The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: an ecological approach. Plant Soil 130:127–134CrossRefGoogle Scholar
  44. Schonherr J, Fernandez V, Schreiber L (2005) Rates of cuticular penetration of chelated Fe-III: role of humidity, concentration, adjuvants, temperature, and type of chelate. J Agr Food Chem 53:4484–4492CrossRefGoogle Scholar
  45. Shi R, Zhang Y, Chen X, Sun Q, Zhang F, Romheld V, Zou C (2010) Influence of long term nitrogen fertilization on micronutrient density in grain of winter wheat (Triticum aestivum). J Cereal Sci 51:165–170CrossRefGoogle Scholar
  46. Swietlik D, Faust M (1984) Foliar nutrition of fruit crops. Hort Rev 6:287–356Google Scholar
  47. Tagliavini M, Abadia J, Rombola AD, Abadia A, Tsipouridis C, Marangoni B (2000) Agronomic means for the control of iron deficiency chlorosis in deciduous fruit trees. J Plant Nutr 23:2007–2022CrossRefGoogle Scholar
  48. Takagi S, Kamei S, Ming-Ho Y (1988) Efficiency of iron extraction from soil by mugineic acid family phytosiderophores. J Plant Nutr 11:643–651CrossRefGoogle Scholar
  49. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301PubMedCrossRefGoogle Scholar
  50. Waters BM, Uauy C, Dubcovsky J, Grusak MA (2009) Wheat (Triticum aestivum) proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J Exp Bot 60:4263–4274PubMedCrossRefGoogle Scholar
  51. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets - iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84PubMedCrossRefGoogle Scholar
  52. Wittwer SH, Bukovac MJ, Jyung WH, Yamada Y, Rasmussen HP, Marian SH, Kannan S (1967) Foliar absorption – penetration of the cuticular membrane and nutrient uptake by isolated leaf cells. Qual Plant 14:105–120CrossRefGoogle Scholar
  53. Yamada Y, Jyung WH, Wittwer SH, Bukovac MJ (1965) Effect of urea on ion penetration through isolated cuticular membranes. Plant Physiol 39:978–982CrossRefGoogle Scholar
  54. Yilmaz A, Ekiz H, Torun B, Gültekin I, Karanlik S, Bagci SA, Cakmak I (1998) Effect of different zinc application methods on grain yield and zinc concentration in wheat grown on zinc-deficient calcareous soils in Central Anatolia. J Plant Nutr 20:461–471CrossRefGoogle Scholar
  55. Ylivainio K, Jaakkola A, Aksela R (2004) Effects of Fe compounds on nutrient uptake by plants grown in sand media with different pH. J Plant Nutr Soil Sci 167:602–608CrossRefGoogle Scholar
  56. Zebarth BJ, Warren CJ, Sheard RW (1992) Influence of the rate of nitrogen fertilization on mineral content of winter wheat in Ontario. J Agric Food Chem 40:1528–1530CrossRefGoogle Scholar
  57. Zhang Y, Shi R, Md. Rezaul K, Zhang F, Zou C (2010) Iron and zinc concentrations in grain and flour of winter wheat as affected by foliar application. J Agric Food Chem 58:12268–12274CrossRefGoogle Scholar
  58. Zhao FJ, Su YH, Dunham SJ, Rakszegi M, Bedo Z, McGrath SP, Shewry PR (2009) Variation in mineral micronutrient concentrations in grain of wheat lines of diverse origin. J Cereal Sci 49:290–295CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Seher Bahar Aciksoz
    • 1
  • Atilla Yazici
    • 1
  • Levent Ozturk
    • 1
  • Ismail Cakmak
    • 1
  1. 1.Faculty of Engineering and Natural SciencesSabanci UniversityIstanbulTurkey

Personalised recommendations