Transgenic Research

, Volume 19, Issue 2, pp 165–180 | Cite as

Critical evaluation of strategies for mineral fortification of staple food crops

  • Sonia Gómez-Galera
  • Eduard Rojas
  • Duraialagaraja Sudhakar
  • Changfu Zhu
  • Ana M. Pelacho
  • Teresa Capell
  • Paul Christou
Review

Abstract

Staple food crops, in particular cereal grains, are poor sources of key mineral nutrients. As a result, the world’s poorest people, generally those subsisting on a monotonous cereal diet, are also those most vulnerable to mineral deficiency diseases. Various strategies have been proposed to deal with micronutrient deficiencies including the provision of mineral supplements, the fortification of processed food, the biofortification of crop plants at source with mineral-rich fertilizers and the implementation of breeding programs and genetic engineering approaches to generate mineral-rich varieties of staple crops. This review provides a critical comparison of the strategies that have been developed to address deficiencies in five key mineral nutrients—iodine, iron, zinc, calcium and selenium—and discusses the most recent advances in genetic engineering to increase mineral levels and bioavailability in our most important staple food crops.

Keywords

Mineral Malnutrition Supplement Fortification Biofortification Poverty 

Notes

Acknowledgments

S.G.-G. is recipient of a fellowship from the Catalan Regional Government (DIUE and “Fons Social Europeu 2008FIC 00196) Spain. T.C. is supported by the Ramon y Cajal (RyC) program, Spain. PC is grateful for financial support to the Ministry of Science and Innovation, Spain (Grant number BFU2007-61413) and to the European Research Council for advanced grant, BIOFORCE.

References

  1. Alavi S, Bugusu B, Cramer G et al (2008) Rice fortification in developing countries: A critical review of the technical and economic feasibility. Institute of Food Technologists, Washington DCGoogle Scholar
  2. Allen LH (2002) Iron supplements: scientific issues concerning efficacy and implications of research and programs. J Nutr 132:S813–S819Google Scholar
  3. Anzai H, Takaiwa F, Katsumata K (2000) Production of human lactoferrin in transgenic plants. In: Shimazaki K, Tsuda H, Tomita M, Kuwata T, Perraudin J (eds) Lactoferrin: structure, function and application. Elsevier, Amsterdam, pp 265–271Google Scholar
  4. Bauer P, Bereczky Z (2003) Gene networks involved in iron acquisition strategies in plants. Agronomie 23:447–454Google Scholar
  5. Bethell DR, Huang J (2004) Recombinant human lactoferrin treatment for global health issues: iron deficiency and acute diarrhea. Biometals 17:337–342PubMedGoogle Scholar
  6. Black MM (2003a) The evidence linking zinc deficiency with children’s cognitive and motor functioning. J Nutr 133:S1473–S1476Google Scholar
  7. Black RE (2003b) Zinc deficiency, infectious disease and mortality in the developing world. J Nutr 133:S1485–S1489Google Scholar
  8. Blasco B, Rios JJ, Cervilla LM et al (2008) Iodine biofortification and antioxidant capacity of lettuce: potential benefits for cultivation and human health. Ann Appl Biol 152:289–299Google Scholar
  9. Brinch-Pedersen H, Hatzack F, Sørensen LD et al (2003) Concerted action of endogenous and heterologous phytase on phytic acid degradation in seed of transgenic wheat (Triticum aestivum L.). Transgenic Res 12:649–659PubMedGoogle Scholar
  10. Brinch-Pedersen H, Hatzack F, Stöger E et al (2006) Heat-stable phytases in transgenic wheat (Triticum aestivum L.): deposition pattern, thermostability, and phytate hydroslysis. J Agric Food Chem 54:4624–4632PubMedGoogle Scholar
  11. Broadley MR, White PJ, Bryson RJ et al (2006) Biofortification of UK food crops with selenium. Proc Nutr Soc 65:169–181PubMedGoogle Scholar
  12. Buois HE (2002) Plant breeding: a new tool for fighting micronutrient malnutrition. J Nutr 132:491S–494SGoogle Scholar
  13. Buois HE, Chassy BM, Ochanda JO (2003) Genetically modified food crops and their contribution to human nutrition and food quality. Trends Food Sci Technol 14:191–209Google Scholar
  14. Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17Google Scholar
  15. Campos-Bowers MH, Wittenmyer BF (2007) Biofortification in China: policy and practice. Health Res Policy Sys 5:10–16Google Scholar
  16. Carvalho KM, Gallardo-Williams MT, Benson RF, Martin DF (2003) Effects of selenium supplementation on four agricultural crops. J Agric Food Chem 51:704–709PubMedGoogle Scholar
  17. CDCP (Centers for Disease Control and Prevention) (2008) Trends in wheat-flour fortification with folic acid, iron. Worldwide, 2004 and 2007. MMWR 57:8–10Google Scholar
  18. Chen L, Yang F, Xu J et al (2002) Determination of selenium concentration of rice in China and effect of fertilization of selenite and selenate on selenium content of rice. J Agric Food Chem 50:5128–5130PubMedGoogle Scholar
  19. Chen R, Xue G, Chen P et al (2008) Transgenic maize plants expressing a fungal phytase gene. Transgenic Res 17:633–643PubMedGoogle Scholar
  20. Chong DK, Langridge WH (2000) Expression of full-length bioactive antimicrobial human lactoferrin in potato plants. Transgenic Res 9:71–78PubMedGoogle Scholar
  21. Christou P, Twyman RM (2004) The potential of genetically enhanced plants to address food insecurity. Nutr Res Rev 17:23–42PubMedGoogle Scholar
  22. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719PubMedGoogle Scholar
  23. Combs GF (2001) Selenium in global food system. Br J Nutr 85:517–547PubMedGoogle Scholar
  24. Connolly EL (2008) Raising the bar for biofortification: enhanced levels of bioavailable calcium in carrots. Trends Biotechnol 26:401–403PubMedGoogle Scholar
  25. Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357PubMedGoogle Scholar
  26. Dai JL, Zhu YG, Zhang M, Huang YZ (2004) Selecting iodine-enriched vegetables and the residual effect of iodate application to soil. Biol Trace Element Res 101:265–276Google Scholar
  27. Darnton-Hill I, Nalubola R (2002) Fortification strategies to meet micronutrient needs: successes and failures. Proc Nutr Soc 61:231–241PubMedGoogle Scholar
  28. De Lorgeril M, Salen P (2006) Selenium and antioxidant defenses as major mediators in the development of chronic heart failure. Heart Fail Rev 11:13–17PubMedGoogle Scholar
  29. Douchkov D, Gryczka C, Stephan UW et al (2005) Ectopic expression of nicotianamine synthase genes results in improved iron accumulation and increased nickel tolerance in transgenic tobacco. Plant Cell Environ 28:365–374Google Scholar
  30. Drakakaki G, Marcel S, Glahn RP et al (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol 59:869–880PubMedGoogle Scholar
  31. Dunn JT (2003) Iodine should be routinely added to complementary foods. J Nut 133:3008S–3010SGoogle Scholar
  32. Eide DJ (2006) Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763:711–722PubMedGoogle Scholar
  33. FAO (1997) Preventing micronutrient malnutrition. A guide to food-based approaches. International Life Science Institute, Washington DCGoogle Scholar
  34. FAO (2000) Biotechnology in food and agriculture. FAO, RomeGoogle Scholar
  35. Frossard E, Bucher M, Machler F et al (2000) Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition. J Sci Food Agr 80:861–879Google Scholar
  36. Genc Y, Humphries JM, Lyons GH, Graham RD (2005) Exploiting genotypic variation in plant nutrient accumulation to alleviate micronutrient deficiency in populations. J Trace Element Med Biol 18:319–324Google Scholar
  37. Ghandilyan A, Vreugdenhil D, Aarts MGM (2006) Progress in the genetic understanding of plant iron and zinc nutrition. Physiol Plant 126:407–417Google Scholar
  38. Goto F, Yoshihara T, Shigemoto N et al (1999) Iron fortification of rice seeds by the soybean ferritin gene. Nature Biotechnol 17:282–286Google Scholar
  39. Graham RD (2003) Biofortification: a global challenge program. Int Rice Res Notes 28:4–8Google Scholar
  40. Graham R, Senadhira D, Beebe S et al (1999) Breeding for micronutrient density in edible portions of staple food crops: conventional approaches. Field Crops Res 60:57–80Google Scholar
  41. Graham RD, Welch RM, Bouis HE (2001) Addressing micornutrient malnutrition through enhancing the nutritional quality of staple foods: principles, perspectives and knowledge gaps. Adv Agron 70:77–142Google Scholar
  42. Gregorio GB (2002) Progress in breeding for trace minerals in staple crops. J Nutr 132:500S–502SPubMedGoogle Scholar
  43. Haas JD, Beard JL, Murray-Kolb LE et al (2005) Iron-biofortified rice improves the iron stores of nonanemic Filipino women. J Nutr 135:2823–2830PubMedGoogle Scholar
  44. Hong CL, Weng HX, Qin YC et al (2008) Transfer of iodine from soil to vegetables by applying exogenous iodine. Agron Sustain Dev 28:575–583Google Scholar
  45. Hong-Xia Y, Mei L, Ze-Jian G et al (2008) Evaluation and application of two high-iron transgenic rice lines expressing a pea ferritin gene. Rice Sci 15:51–56Google Scholar
  46. Horton S (2006) The economics of food fortification. J Nutr 136:1068–1071PubMedGoogle Scholar
  47. Hotz C, Brown KH (2004) International Zinc Nutrition Consultative Group (IZiNCG). Assessment of the risk of zinc deficiency in populations and options for its control. Food Nutr Bull 25:S91–S204Google Scholar
  48. Hunt JM (2002) Reversing productivity losses from iron deficiency: the economic case. J Nutr 132:S794Google Scholar
  49. Ishimaru Y, Suzuki M, Tsukamoto T et al (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346PubMedGoogle Scholar
  50. IZINCG (2007) Technical Brief no 4: zinc fortification. Available at http://www.izincg.org/index.php. Accessed 30 Nov 2008
  51. Jeong J, Guerinot ML (2008) Biofortified and bioavailable: the gold standard for plant-based diets. Proc Natl Acad Sci USA 105:1777–1778PubMedGoogle Scholar
  52. Kobayashi T, Nakanishi H, Takahashi M, et al (2008) Generation and field trials of transgenic rice tolerant to iron deficiency. Rice 1:144–153Google Scholar
  53. Lee MH, Hettiarachchy NS, McNew RW, Gnanasambandam R (1995) Physicochemical properties of calcium-fortified rice. Cereal Chem 72:352–355Google Scholar
  54. Liu QL, Xu XH, Ren XL et al (2007) Generation and characterization of low phytic acid germplasm in rice (Oryza sativa L.). Theor Appl Genet 114:803–814PubMedGoogle Scholar
  55. Lucca P, Hurrell R, Potrykus I (2002) Fighting iron deficiency anemia with iron-rich rice. J Am Coll Nutr 21:184S–190SPubMedGoogle Scholar
  56. Lyons GH, Lewis J, Lorimer MF et al (2004a) High-selenium wheat: agronomic biofortification strategies to improve human nutrition. Food Agric Environ 2:171–178Google Scholar
  57. Lyons GH, Stangoulis JCR, Graham RD (2004b) Exploiting micronutrient interaction to optimize biofortification programs: the case for inclusion of selenium and iodine in the HarvestPlus program. Nutr Rev 62:247–252PubMedGoogle Scholar
  58. Lyons GH, Judson GJ, Ortiz-Monasterio I et al (2005) Selenium in Australia: selenium status and biofortification of wheat for better health. J Trace Element Med Biol 19:75–82Google Scholar
  59. Maier KJ, Nelson CR, Bailey FC et al (1998) Accumulation of selenium in aquatic biota of a watershed treated with seleniferous fertilizer. Bull Env Contam Tox 60:409–416Google Scholar
  60. Maret W, Sandstead H (2006) Zinc requirements and the risk and benefits of zinc supplementation. J Trace Element Med Biol 20:3–18Google Scholar
  61. Mason J, Deitchler M, Soekirman, Martorell R (2004) Successful micronutrient programs. Food Nutr Bull 25:1–102Google Scholar
  62. Mehansho H (2006) Iron fortification technology development: new approaches. J Nutr 136:1059PubMedGoogle Scholar
  63. Mei H, Zhao J, Pittman JK et al (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427PubMedGoogle Scholar
  64. Mori S (1999) Iron acquisition by plants. Curr Opin Plant Biol 2:250–253PubMedGoogle Scholar
  65. Morris J, Nakata PA, McConn M et al (2007) Increased calcium bioavailability in mice fed genetically engineered plants lacking calcium oxalate. Plant Mol Biol 64:613–618PubMedGoogle Scholar
  66. Muller O, Krawinkel M (2005) Malnutrition and health in developing countries. CMAJ 173:279–286PubMedGoogle Scholar
  67. Murray-Kolb LE, Takaiwa F, Goto F et al (2002) Transgenic rice is a source of iron for iron-depleted rats. J Nutr 132:957–960PubMedGoogle Scholar
  68. Nandi S, Suzuki YA, Huang J et al (2002) Expression of human lactoferrin in transgenic rice grains for the application in infant formula. Plant Sci 163:713–722Google Scholar
  69. Nantel G, Tontisirin K (2002) Policy and sustainability issues. J Nutr 132:S839–S844Google Scholar
  70. Nestel P, Buois HE, Meenakshi JV, Pfeiffer W (2006) Biofortification of staple food crops. J Nutr 136:1064–1067PubMedGoogle Scholar
  71. Park S, Kim CK, Pike LM et al (2004) Increased calcium in carrots by expression of an Arabidopsis H+/Ca2+ transporter. Mol Breeding 14:275–282Google Scholar
  72. Park S, Kang TS, Kim CK et al (2005) Genetic manipulation for enhancing calcium content in potato tuber. J Agr Food Chem 53:5598–5603Google Scholar
  73. Park S, Elless MP, Park J, et al (2009) Sensory analysis of calcium-biofortified lettuce. Plant Biotechnol J 7(1):106–117Google Scholar
  74. Peleg Z, Saranga Y, Yazici A, et al (2008) Grain zinc, iron and protein concentrations and zinc-efficiency in wild emmer wheat under contrasting irrigation regimes. Plant Soil 306:57–67Google Scholar
  75. Pilon-Smits EAH, Hwang S, Lytle CM et al (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction and tolerance. Plant Physiol 119:123–132PubMedGoogle Scholar
  76. Qu LQ, Yoshihara T, Ooyama A et al (2005) Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta 222:225–233Google Scholar
  77. Raboy V (2002) Progress in breeding low phytate crops. J Nutr 132:503S–505SPubMedGoogle Scholar
  78. Ramessar K, Capell T, Twyman RM et al (2008a) Calling the tunes on transgenic crops—the case for regulatory harmony. Mol Breeding 23:99–112Google Scholar
  79. Ramessar K, Capell T, Twyman RM et al (2008b) Trace and traceability—a call for regulatory harmony. Nature Biotechnol 26:975–978Google Scholar
  80. Rayman MP (2002) The argument for increasing selenium intake. Proc Nutr Soc 61:203–215PubMedGoogle Scholar
  81. Rengel Z, Batten GD, Crowley DE (1999) Agronomic approaches for improving the micronutrient density in edible portions of field crops. Field Crops Res. 60:27–40Google Scholar
  82. Romanchik-Cerpovicz JE, McKemie RJ (2007) Fortification of all-purpose wheat-flour tortillas with calcium lactate, calcium carbonate, or calcium citrate is acceptable. J Am Dietetic Assoc 107:506–509Google Scholar
  83. Salmon V, Legrand D, Slomianny MC et al (1998) Production of human lactoferrin in transgenic tobacco plants. Protein Expr Purif 13:127–135PubMedGoogle Scholar
  84. Schachtman DP, Barker SJ (1999) Molecular approaches for increasing the micronutrient density in edible portions of food crops. Field Crop Res 60:81–92Google Scholar
  85. Sheikholeslam R, Abdollahi Z, Haghighi FN (2004) Managing nutritional programmes in developing countries. Eastern Mediterr Health J 10:737–746Google Scholar
  86. Shrimpton R, Schultink W (2002) Can supplements help meet the micronutrient needs of the developing world? Proc Nutr Soc 61:223–229PubMedGoogle Scholar
  87. Shrimpton R, Gross R, Darnton-Hill I, Young M (2005) Zinc deficiency: what are the most appropriate interventions? BMJ 330:347–349PubMedGoogle Scholar
  88. Sivakumar B, Brahmam GNV, Madhavan Nair K et al (2001) Prospects of fortification of salt with iron and iodine. Br J Nutr 85:S167–S173PubMedGoogle Scholar
  89. Sivakumar B, Nair KM, Sreeramulu D et al (2006) Effect of micronutrient supplement on health and nutritional status of schoolchildren: biochemical status. Nutrition 22:15S–25SGoogle Scholar
  90. Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389PubMedGoogle Scholar
  91. Stein AJ, Meenakshi JV, Qaim M et al (2008) Potential impacts of iron biofortification in India. Social Sci Med 66:1797–1808Google Scholar
  92. Suzuki M, Takahashi M, Tsukamoto T et al (2006) Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. Plant J 48:85–97PubMedGoogle Scholar
  93. Takahashi M (2003) Overcoming Fe deficiency by a transgenic approach in rice. Plant Cell Tiss Org Cult 72:211–220Google Scholar
  94. Takahashi M, Nakanishi H, Kawasaki S et al (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nature Biotechnol 19:466–469Google Scholar
  95. Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51:401–432PubMedGoogle Scholar
  96. Theil EC, Briat JF (2004) Plant ferritin and non-heme iron nutrition in humans. In: HarvestPlus technical monographs 1. International Food Policy Research Institute and International Center for Tropical Agriculture (CIAT), Washington, DC and CaliGoogle Scholar
  97. Timmer CP (2003) Biotechnology and food systems in developing countries. J Nutr 133:3319–3322PubMedGoogle Scholar
  98. Underwood BA, Smitasiri S (1999) Micronutrient malnutrition: policies and programs for control and their implications. Annu Rev Nutr 19:303–324PubMedGoogle Scholar
  99. UNICEF (2008) Sustainable elimination of iodine deficiency. UNICEF, New YorkGoogle Scholar
  100. van der Zaal BJ, Neuteboom LW, Pinas JE et al (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055PubMedGoogle Scholar
  101. Vasconcelos M, Datta K, Oliva N et al (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164:371–378Google Scholar
  102. Vert G, Grotz N, Dédaldéchamp F et al (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233PubMedGoogle Scholar
  103. Weaver CM (1998) Calcium in food fortification strategies. Int Dairy J 8:443–449Google Scholar
  104. Welch RM, Graham RD (2005) Agriculture: the real nexus for enhancing bioavailable micronutrients in food crops. J Trace Elements Med Biol 18:299–307Google Scholar
  105. Welch RM, House WA, Ortiz-Monasterio I, Cheng Z (2005) Potential for improving bioavailable zinc in wheat grain (Triticum species) through plant breeding. J Agirc Food Chem 53:2176–2180Google Scholar
  106. White PJ, Broadley MR (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci 10:586–593PubMedGoogle Scholar
  107. WHO (2004) Iodine status worldwide : WHO global database on iodine deficiency. WHO, GenevaGoogle Scholar
  108. WHO/FAO (1998) Vitamin and mineral requirements in human nutrition: report of a joint FAO/WHO expert consultation, 2nd edn. Bangkok, Thailand. 21–30 Sept 1998Google Scholar
  109. WHO/UNICEF (2004) Joint statement: clinical management of acute diarrhea. Available at http://www.izincg.org/pdf/WHOUnicefdiarrheaStatementENGL.pdf. Accessed 30 Nov 2008
  110. WHO/WFP/UNICEF (2007) Preventing and controlling micronutrient deficiencies in populations affected by an emergency. Joint statement by the World Health Organization, the World Food Programme and the United Nations Children’s FundGoogle Scholar
  111. Zhu C, Naqvi S, Gomez-Galera S et al (2007) Transgenic strategies for the nutritional enhancement of plants. Trends Plant Sci 12:548–555PubMedGoogle Scholar
  112. Zhu C, Naqvi S, Breitenbach J et al (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci USA 105:18232–18237PubMedGoogle Scholar
  113. Zimmermann MB, Wegmueller R, Zeder C et al (2004) Triple fortification of salt with microcapsules of iodine, iron, and vitamin A. Am J Clin Nutr 80:1283–1290PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Sonia Gómez-Galera
    • 1
  • Eduard Rojas
    • 1
  • Duraialagaraja Sudhakar
    • 2
  • Changfu Zhu
    • 1
  • Ana M. Pelacho
    • 3
  • Teresa Capell
    • 1
  • Paul Christou
    • 1
    • 4
  1. 1.Department of Vegetal Production and Forestry Science, ETSEAUniversity of LleidaLleidaSpain
  2. 2.Department of Plant Molecular Biology and Biotechnology, Centre for Plant Molecular BiologyTamil Nadu Agricultural UniversityCoimbatoreIndia
  3. 3.Department of Hortofruticulture, Botany and Gardening, ETSEAUniversity of LleidaLleidaSpain
  4. 4.Institució Catalana de Reserca i Estudis AvançatsBarcelonaSpain

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