Genes & Nutrition

, Volume 8, Issue 1, pp 29–41 | Cite as

The contribution of transgenic plants to better health through improved nutrition: opportunities and constraints

  • Eduard Pérez-Massot
  • Raviraj Banakar
  • Sonia Gómez-Galera
  • Uxue Zorrilla-López
  • Georgina Sanahuja
  • Gemma Arjó
  • Bruna Miralpeix
  • Evangelia Vamvaka
  • Gemma Farré
  • Sol Maiam Rivera
  • Svetlana Dashevskaya
  • Judit Berman
  • Maite Sabalza
  • Dawei Yuan
  • Chao Bai
  • Ludovic Bassie
  • Richard M. Twyman
  • Teresa Capell
  • Paul Christou
  • Changfu Zhu
Review

Abstract

Malnutrition is a prevalent and entrenched global socioeconomic challenge that reflects the combined impact of poverty, poor access to food, inefficient food distribution infrastructure, and an over-reliance on subsistence mono-agriculture. The dependence on staple cereals lacking many essential nutrients means that malnutrition is endemic in developing countries. Most individuals lack diverse diets and are therefore exposed to nutrient deficiencies. Plant biotechnology could play a major role in combating malnutrition through the engineering of nutritionally enhanced crops. In this article, we discuss different approaches that can enhance the nutritional content of staple crops by genetic engineering (GE) as well as the functionality and safety assessments required before nutritionally enhanced GE crops can be deployed in the field. We also consider major constraints that hinder the adoption of GE technology at different levels and suggest policies that could be adopted to accelerate the deployment of nutritionally enhanced GE crops within a multicomponent strategy to combat malnutrition.

Keywords

Transgenic crops Micronutrients Food security Vitamins Minerals Genetic engineering 

Supplementary material

12263_2012_315_MOESM1_ESM.doc (1.4 mb)
Supplementary material 1 (DOC 1392 kb)

References

  1. Abbadi A, Domergue F, Bauer J, Napier JA, Welti R, Zähringer U, Cirpus P, Heinz E (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. Plant Cell 16:2734–2748PubMedGoogle Scholar
  2. Aluru M, Xu Y, Guo R et al (2008) Generation of transgenic maize with enhanced provitamin A content. J Exp Bot 59:3551–3562PubMedGoogle Scholar
  3. Apel A (2010) The costly benefits of opposing agricultural biotechnology. New Biotechnol 27:635–640Google Scholar
  4. Bai C, Twyman RM, Farré G, Sanahuja G, Christou P, Capell T, Zhu C (2011) A golden era—pro-vitamin A enhancement in diverse crops. In Vitro Cell Dev Biol Plant 47:205–221Google Scholar
  5. Bartholomew M (2002) James Lind’s treatise of the scurvy (1753). Postgrad Med J 78:695–696PubMedGoogle Scholar
  6. Benoist B, McLean M, Egli I, Cogswell M (2008) Worldwide prevalence of anaemia 1993–2005. WHO Global database on AnaemiaGoogle Scholar
  7. Bicar E, Woodman-Clikeman W, Sangtong V, Peterson J, Yang S, Lee M, Scott M (2008) Transgenic maize endosperm containing a milk protein has improved amino acid balance. Transgenic Res 17:59–71PubMedGoogle Scholar
  8. Botella-Pavía P, Rodríguez-Concepción M (2006) Carotenoid biotechnology in plants for nutritionally improved foods. Physiol Plantarum 126:369–381Google Scholar
  9. Brinch-Pedersen H, Hatzack F, Stöger E, Arcalis E, Pontopidan K, Holm PB (2006) Heat-stable phytases in transgenic wheat (Triticum aestivum L.): deposition pattern, thermostability, and phytate hydroslysis. J Agric Food Chem 54:4624–4632PubMedGoogle Scholar
  10. Brookes G, Barfoot P (2006) GM crops: the first ten years—global socio-economic and environmental impacts. ISAAA Brief 36, ISAAA, IthacaGoogle Scholar
  11. Bulley S, Wright M, Rommens C, Yan H et al (2011) Enhancing ascorbate in fruits and tubers through over-expression of the L-galactose pathway gene GDP-L-galactose phosphorylase. Plant Biotechnol J 10:390–397PubMedGoogle Scholar
  12. Chakraborty S, Chakraborty N, Datta A (2000) Increased nutritive value of transgenic potato by expressing a nonallergenic seed albumin gene from Amaranthus hypochondriacus. Proc Natl Acad Sci USA 97:3724–3729PubMedGoogle Scholar
  13. Chen R, Xue G, Chen P, Yao B, Yang W, Ma Q, Fan Y, Zhao Z, Tarczynski MC, Shi J (2008) Transgenic maize plants expressing a fungal phytase gene. Transgenic Res 17:633–643PubMedGoogle Scholar
  14. Cho EA, Lee CA, Kim YA, Baek SH, Reyes BG, Yun SJ (2005) Expression of γ-tocopherol methyltransferase transgene improves tocopherol composition in lettuce (Latuca sativa L.). Mol Cells 19:16–22PubMedGoogle Scholar
  15. Chong MYK (2011) Risk perception and communication about agricultural biotechnology in developing countries: the case of Bt eggplant in India. Cornwell University, DissertationGoogle Scholar
  16. Christou P, Twyman RM (2004) The potential of genetically enhanced plants to address food insecurity. Nutr Res Rev 17:23–42PubMedGoogle Scholar
  17. Combs GF Jr (2001) Selenium in global food systems. Br J Nutr 85:517–547PubMedGoogle Scholar
  18. Cong L, Wang C, Chen L, Liu H, Yang G, He G (2009) Expression of phytoene synthase1 and carotene desaturase crtI genes result in an increase in the total carotenoids content in transgenic elite wheat (Triticum aestivum L.). J Agric Food Chem 57:8652–8660PubMedGoogle Scholar
  19. Connolly EL (2008) Raising the bar for biofortification: enhanced levels of bioavailable calcium in carrots. Trends Biotechnol 26:401–403PubMedGoogle Scholar
  20. Dayod M, Tyerman SD, Leigh RA, Gilliham M (2010) Calcium storage in plants and the implications for calcium biofortification. Protoplasma 247:215–231PubMedGoogle Scholar
  21. DellaPenna D, Pogson B (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Ann Rev Plant Biol 57:711–773Google Scholar
  22. Díaz de la Garza R, Gregory JF, Hanson AD (2007) Folate biofortification of tomato fruit. Proc Natl Acad Sci USA 104:4218–4222PubMedGoogle Scholar
  23. Diretto G, Al-Babili S, Tavazza R, Papacchioli V, Beyer P, Giuliano G (2007) Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoSONE 2:e350Google Scholar
  24. Djoussé L, Biggs ML, Lemaitre RN, King IB, Song X, Ix JH, Mukamal KJ, Siscovick DS, Mozaffarian D (2011) Plasma omega-3 fatty acids and incident diabetes in older adults. Am J Clin Nutr 94:527–533PubMedGoogle Scholar
  25. Domergue F, Abbadi A, Heinz E (2005) Relief for fish stocks: oceanic fatty acids in transgenic oilseeds. Trends Plant Sci 10:112–116PubMedGoogle Scholar
  26. Drakakaki G, Marcell S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (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
  27. Ducreux LJ, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein. J Exp Bot 56:81–89PubMedGoogle Scholar
  28. EFSA Panel on Genetically Modified Organisms (GMO) (2010) Guidance on the environmental risk assessment of genetically modified plants. EFSA J 2010(8):1879–1989Google Scholar
  29. EFSA Panel on Genetically Modified Organisms (GMO) (2011) Guidance for risk assessment of food and feed from genetically modified plants. EFSA J 2011(9):2150–2186Google Scholar
  30. EFSA Panel on Genetically Modified Organisms (GMO) and Panel on Biological Hazards (BIOHAZ) (2009) Scientific opinion on a request from the European Commission on the use of antibiotic resistance genes as marker genes in genetically modified plants. EFSA J 2009(1034):1–81Google Scholar
  31. Enfissi EMA, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3:17–27PubMedGoogle Scholar
  32. FAO (2009) 2050: A third more mouths to feed: food production will have to increase by 70 percent—FAO convenes high-level expert forum. FAO Media centre, RomeGoogle Scholar
  33. Farré G, Ramessar K, Twyman RM, Capell T, Christou P (2010a) The humanitarian impact of plant biotechnology: recent breakthroughs vs bottlenecks for adoption. Curr Opin Plant Biol 13:219–225PubMedGoogle Scholar
  34. Farré G, Sanahuja G, Naqvi S, Bai C, Capell T, Zhu C, Christou P (2010b) Travel advice on the road to carotenoids in plants. Plant Sci 179:28–48Google Scholar
  35. Farré G, Bai C, Twyman RM, Capell T, Christou P, Zhu C (2011a) Nutritious crops producing multiple carotenoids—a metabolic balancing act. Trends Plant Sci 16:532–540PubMedGoogle Scholar
  36. Farré G, Twyman RM, Changfu Z, Capell T, Christou P (2011b) Nutritionally enhanced crops and food security: scientific achievements versus political expediency. Curr Opin Biotechnol 22:245–251PubMedGoogle Scholar
  37. Farré G, Sudhakar D, Naqvi S, Sandmann G, Christou P, Capell T, Zhu C (in press) Transgenic rice grains expressing a heterologous ρ-hydroxyphenylpyruvate dioxygenase shift tocopherol synthesis from the gamma to the alpha isoform without increasing absolute tocopherol levels. Trans Res. doi:10.1007/s11248-012-9601-7
  38. Frizzi A, Huang S, Gilberton LA, Armstrong TA, Luethy MH, Malvar TM (2008) Modifying lysine biosynthesis and catabolism in corn with a single bifuncitonal expression/silencing transgene cassette. Plant Biotechnol J 6:13–21PubMedGoogle Scholar
  39. García-Casal MN, Leets I, Layrisse M (2000) β-carotene and inhibitors of iron absorption modify iron uptake by Caco-2 cells. J Nutr 130:5–9PubMedGoogle Scholar
  40. Gibson RS (2007) The role of diet- and host-related factors in nutrient bioavailability and thus in nutrient-based dietary requirement estimates. Food Nutr Bull 28:77–100Google Scholar
  41. Gómez-Galera S, Rojas E, Sudhakar D, Zhu C, Pelacho AM, Capell T, Christou P (2010) Critical evaluation of strategies for mineral fortification of staple crops. Transgenic Res 19:165–180PubMedGoogle Scholar
  42. Gómez-Galera S, Sudhakar D, Pelacho AM, Capell T, Christou P (2012a) Constitutive expression of a barley Fe phytosiderophore transporter increases alkaline soil tolerance and results in iron partitioning between vegetative and storage tissues under stress. Plant Physiol Biochem 53:46–53PubMedGoogle Scholar
  43. Gómez-Galera S, Twyman RM, Sparrow PAC, Van Droogenbroeck B, Custers R, Capell T, Christou P (2012b) Field trials and tribulations—making sense of the regulations for experimental field trials of transgenic crops in Europe. Plant Biotechnol J 10:511–523Google Scholar
  44. Graham RD, Welch RM, Bouis HE (2001) Addressing micronutrient malnutrition through enhancing the nutritional quality of staple foods: principles, perspectives and knowledge gaps. Adv Agron 70:77–142Google Scholar
  45. Hambidge MK, Krebs NF (2007) Zinc deficiency: a special challenge. J Nutr 137:1101–1105PubMedGoogle Scholar
  46. Harrison EA (2005) Mechanisms of digestion and absorption of dietary vitamin A. Annu Rev Nutr 25:87–103PubMedGoogle Scholar
  47. Hemavathi UpadhyayaCP, Akula N, Young KE, Chun SC, Hwan Kim D, Park SW (2010) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol Lett 32:321–330PubMedGoogle Scholar
  48. Hirschi K (2008) Nutritional improvements in plants: time to bite on biofortified foods. Trends Plant Sci 13:459–463PubMedGoogle Scholar
  49. Hoddinott J, Maluccio JA, Behrman JR, Flores R, Martorell R (2008) Effect of a nutrition intervention during early childhood on economic productivity in Guatemalan adults. Lancet 371:411–416PubMedGoogle Scholar
  50. Hotz C, Brown KH (2004) Assessment of the risk of zinc deficiency in population and options for its control. Food Nutr Bull 25:99–203Google Scholar
  51. Hotz C, Gibson RS (2007) Traditional food-processing and preparation practices to enhance the bioavailability of micronutrients in plant-based diets. J Nutr 137:1097–1100PubMedGoogle Scholar
  52. Ishimoto M, Rahman SM, Hanafy MS, Khalafalla MM, El-Shemy HA, Nakamoto Y, Kita Y, Takanashi K, Matsuda F, Murano Y, Funabashi T, Miyagawa H, Wakasa K (2010) Evaluation of amino acid content and nutritional quality of transgenic soybean seeds with high-level tryptophan accumulation. Mol Breed 25:313–326Google Scholar
  53. Jain AK, Nessler CL (2000) Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol Breed 6:73–78Google Scholar
  54. Jeong J, Guerinot ML (2008) Biofortified and bioavailable: the gold standard for plant-based diets. Proc Nac Acad Sci USA 105:1777–1778Google Scholar
  55. Johnson AAT, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLOSone 6:e24476Google Scholar
  56. Jørgensen K, Bak S, Kamp Busk P, Sørensen C, Olsen CE, Puonti-Kaerlas J, Lindberg Møller B (2005) Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology. Plant Physiol 139:363–374PubMedGoogle Scholar
  57. Jung R, Carl F (2000) Transgenic corn with an improved amino acid composition. In: Müntz K, Ulrich W (eds) The 8th international symposium on plant seeds. Institute of Plant Genetics and Crop Plant Research, GaterslebenGoogle Scholar
  58. Kalaitzandonakes N, Alston JM, Bradford KJ (2007) Compliance costs for regulatory approval of new biotech crops. Nature Biotecnol 25:509–511Google Scholar
  59. Khalili H, Soudbakhsh A, Hajiabdolbaghi M, Dashti-Khavidaki S, Poorzare A, Saeedi AA, Sharififar R (2008) Nutritional status and serum zinc and selenium levels in Iranian HIV infected individuals. J Infect Dis 8:165–172Google Scholar
  60. Kim CK, Han JS, Lee HS, Oh JY et al (2006) Expression of an Arabidopsis CAX2 variant in potato tubers increases calcium levels with no accumulation of manganese. Plant Cell Rep 25:1226–1232PubMedGoogle Scholar
  61. Kinney AJ, Cahoon EB, Damude HG, Hitz WD, Kolar CW, Liu ZB (2004) Production of very long chain polyunsaturated fatty acids in oilseed plants. Patent WO 071467 A2Google Scholar
  62. König A, Cockburn A, Crevel RWR, Debruyne E, Grafstroem R, Hammerling U, Kimber I, Knudsen I, Kuiper HA, Peijnenburg AACM, Penninks AH, Poulsen M, Schauzu M, Wal JM (2004) Assessment of the safety of food derived from genetically modified GM crops. Food Chem Toxicol 42:1047–1088PubMedGoogle Scholar
  63. Kouser S, Qiam M (2011) Impact of Bt cotton on pesticide poisoning in smallholder agriculture: a panel data analysis. Ecol Econom 70:2105–2113Google Scholar
  64. Kowalski S (2007) Rational risk/benefit analysis of genetically modified crops. J Intellect Prop Rights 12:92–103Google Scholar
  65. Kuwano M, Mimura T, Takaiwa F, Yoshida KT (2009) Generation of stable ‘low phytic acid’ transgenic rice through antisense repression of the 1D-myo-inositol 3-phosphate synthase gene (RINO1) using the 18-kDa oleosin promoter. Plant Biotechnol J 7:96–105PubMedGoogle Scholar
  66. LeDuc DL, Tarun AS, Montes-Bayon M, Meija J et al (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383PubMedGoogle Scholar
  67. Lee S, Jeon US, Lee SJ, Kim YK, Persson DP et al (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc Natl Acad Sci USA 106:22014–22019PubMedGoogle Scholar
  68. Lee S, Persson DP, Hansen TH, Husted S, Schjoerring JK, Kim YS, Jeon US, Kim YK, Kakei Y, Masuda H, Nishizhawa NK, An G (2011) Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnol J 9:865–873PubMedGoogle Scholar
  69. Lemaux PG (2009) Genetically engineered plants and food: scientist’s analysis of the issues (part II). Ann Rev Plant Biol 60:511–599Google Scholar
  70. Lopez HW, Leenhardt F, Coudray C, Remesy C (2002) Minerals and phytic acid interactions: is it a real problem for human nutrition? Int J Food Sci Technol 37:727–739Google Scholar
  71. Lopez AB, Eck JV, Conlin BJ, Paolillo DJ, O’Neill J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59:213–223PubMedGoogle Scholar
  72. Lyons G, Stangoulis J, Graham R (2003) High-selenium wheat: biofortification for better health. Nutr Res Rev 16:45–60PubMedGoogle Scholar
  73. Martin C, Butelli E, Petroni K, Tonelli C (2011) How can research on plants contribute to promoting human health? Plant Cell 23:1685–1699PubMedGoogle Scholar
  74. Monsen ER, Balintfy J (1982) Calculating dietary iron bioavailability: refinement and computerization. J Am Diet Assoc 80:307–311PubMedGoogle Scholar
  75. Morris S, Spillane C (2010) EU GM crop regulation: a road to resolution or a regulatory roundabout? EJRR 4:359Google Scholar
  76. Naqvi S, Farre G, Sanahuja G, Capell T, Zhu C, Christou P (2009a) When more is better: multigene engineering in plants. Trends Plant Sci 15:49–56Google Scholar
  77. Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J, Conesa D, Ros G, Sandmann G, Capell T, Christou P (2009b) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106:7762–7767PubMedGoogle Scholar
  78. Naqvi S, Zhu C, Farre G, Sandmann G, Capell T, Christou P (2010) Synergistic metabolism in hybrid corn indicates bottlenecks in the carotenoid pathway and leads to the accumulation of extraordinary levels of the nutritionally important carotenoid zeaxanthin. Plant Biotechnol J 9:384–393PubMedGoogle Scholar
  79. Naqvi S, Farré G, Zhu C, Sandmann G, Capell T, Christou P (2011) Simultaneous expression of Arabidopsis ρ-hydroxyphenylpyruvate dioxygenase and MPBQ methyltransferase in transgenic corn kernels triples the tocopherol content. Transgenic Res 20:177–181PubMedGoogle Scholar
  80. Naylor RL, Falcon WP, Goodman RM, Jahn MM, Sengooba T, Tefera H, Nelson RJ (2004) Biotechnology in the developing world: a case for increased investments in orphan crops. Food Policy 29:15–44Google Scholar
  81. Nunes ACS, Vianna GR, Cuneo F, Amaya-Farfán J, de Capdeville G, Rech EL, Aragao FJL (2006) RNAi-mediated silencing of the myo-inositol-1-phosphate synthase gene (GmMIPS1) in transgenic soybean inhibited seed development and reduced phytate content. Planta 224:125–132PubMedGoogle Scholar
  82. Paine J, Shipton C, Chaggar S, Howells R, Kennedy M, Vernon G, Wright S, Hinchliffe E, Adams J, Silverstone A, Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487PubMedGoogle Scholar
  83. Palmgren MG, Clemens S, Williams LE, Krämer U, Borg SUK, Schjørring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473PubMedGoogle Scholar
  84. Park SH, Kim C-K, Pike LM et al (2004) Increased calcium in carrots by expression of an Arabidopsis H+/Ca2+ transporter. Mol Breed 14:275–282Google Scholar
  85. Park S, King TS, Kim CK, Han JS, Kim S, Smith RH, Pike LM, Hirschi KD (2005) Genetic manipulation for enhancing calcium content in potato tuber. J Agric Food Chem 53:5598–5603PubMedGoogle Scholar
  86. Park S, Elless MP, Park J et al (2009) Sensory analysis of calciumbiofortified lettuce. Plant Biotechnol J 7:106–117PubMedGoogle Scholar
  87. Perseley G (2000) Agricultural biotechnology and the poor: Promethean science. In: Perseley GJ, Lantin MM (eds) Agricultural biotechnology and the poor: proceedings of an international conference, Washington, DC, 21–22 October 1999. Consultative Group on International Agricultural Research, Washington, DC, pp 1–36Google Scholar
  88. Pilion-Smits EAH, Hwang S, Lytle CM, Zhu Y, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Over expression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction and tolerance. Plant Physiol 119:123–132Google Scholar
  89. Qaim M (2009) Economics of GM Crops. Ann Rev Resour Econ 1:665–693Google Scholar
  90. Qaim M, Stein AJ, Meenakshi JV (2007) Economics of biofortification. Agric Econ 37:119–133Google Scholar
  91. Ramaswami B (2007) Biofortified crops and biotechnology: a political economy landscape for India. AgBioForum 10:170–177Google Scholar
  92. Ramessar K, Peremarti A, Gómez-Galera S, Naqvi S, Moralejo M, Muñoz P, Capell T, Christou P (2007) Biosafety and risk assessment framework for selectable marker genes in transgenic crop plants: a case of the science not supporting the politics. Transgenic Res 16:261–280PubMedGoogle Scholar
  93. Ramessar K, Capell T, Twyman RM, Quemada H, Christou P (2009) Calling the tunes on transgenic crops: the case for regulatory harmony. Mol Breeding 23:99–112Google Scholar
  94. Ramessar K, Capell T, Twyman RM, Christou P (2010) Going to ridiculous lengths—European coexistence regulations for GM crops. Nat Biotechnol 28:133–136PubMedGoogle Scholar
  95. Rascón-Cruz Q, Sinagawa-García S, Osuna-Castro JA, Bohorova N, Paredes-Lopez O (2004) Accumulation, assembly, and digestibility of amarantin expressed in transgenic tropical maize. Theor Appl Genet 108:335–342PubMedGoogle Scholar
  96. Raybould A, Quemada H (2010) Bt crops and food security in developing countries: realized benefits, sustainable use and lowering barriers to adoption. Food Sec 2:247–259Google Scholar
  97. Romer S, Lubeck J, Kauder F et al (2002) Genetic engineering of a zeaxanthin-rich potato by antisense inactivation and co-suppression of carotenoid epoxidation. Metab Eng 4:263–272PubMedGoogle Scholar
  98. Rosenberg IH (2005) Science-based micronutrient fortification: which nutrients, how much, and how to know? Am J Clin Nutr 280:279–280Google Scholar
  99. Sabalza M, Miralpeix B, Twyman RM, Capell T, Christou P (2011) EU legitimizes GM crop exclusion zones. Nature Biotechnol 29:315–317Google Scholar
  100. Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J 9:283–300PubMedGoogle Scholar
  101. Sayre R, Beeching JR, Cahoon EB, Egesi C et al (2011) The BioCassava plus program: biofortification of cassava for sub-Saharan Africa. Ann Rev Plant Biol 62:251–272Google Scholar
  102. Scholl TO, Johnson GW (2000) Folic acid: influence on the outcome of pregnancy. Am J Clin Nutr 71:1295S–1303SPubMedGoogle Scholar
  103. Segal G, Song R, Messing J (2003) A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165:387–397PubMedGoogle Scholar
  104. Sindhu AS, Zheng ZW, Murai N (1997) The pea seed storage protein legumin was synthesized, processed and accumulated stably in transgenic rice endosperm. Plant Sci 130:189–196Google Scholar
  105. Siritunga D, Sayre RT (2003) Generation of cyanogens-free transgenic cassava. Planta 217:367–373PubMedGoogle Scholar
  106. Stöger E, Parker M, Christou P, Casey R (2001) Pea legumin overexpressed in wheat endosperm assembles into an ordered paracrystalline matrix. Plant Physiol 125:1732–1742PubMedGoogle Scholar
  107. Storozhenko S, De Brouwer V, Volckaert M, Navarrete O, Blancquaert D, Zhang GF, Lambert W, Van Der Straeten D (2007) Folate fortification of rice by metabolic engineering. Nat Biotechnol 25:1277–1279PubMedGoogle Scholar
  108. Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37:517–527PubMedGoogle Scholar
  109. Tadele Z (2009) New approaches to plant breeding of orphan crops in Africa. In: Proceedings of an international conference, 19–21 September 2007, Bern, SwitzerlandGoogle Scholar
  110. Tamás C, Kisgyörgy BN, Rakszegi M, Wilkinson MD, Yang M, Láng L, Tamás L, Bedo Z (2009) Transgenic approach to improve wheat (Triticum aestivum L.) nutritional quality. Plant Cell Rep 28:1085–1094PubMedGoogle Scholar
  111. Tang G, Qin J, Dolnikowski GG, Russell RM, Grusak MA (2009) Golden rice is an effective source of vitamin A. Am J Clin Nutr 89:1776–1783PubMedGoogle Scholar
  112. Tavya V, Kim Y, Kagan I, Dinkins R, Kim K, Collins G (2007) Increased α-tocopherol content in soybean seed overexpressing the Perilla frutescens γ-tocopherol methyltransferase gene. Plant Cell Rep 26:61–70Google Scholar
  113. United States Food and Drug Administration (1992) Statement of policy—foods derived from new plant varieties. FDA federal register 57Google Scholar
  114. Wakasa K, Hasegawa H, Nemoto H, Matsuda F, Miyazawa H, Tozawa Y, Morino K, Komatsu A, Yamada T, Terakawa T, Miyagawa H (2006) High-level tryptophan accumulation in seeds of transgenic rice and its limited effects on agronomic traits and seed metabolite profile. J Expt Bot 57:3069–3078Google Scholar
  115. Welch RM, Graham RD (2005) Agriculture: the real nexus for enhancing bioavailable micronutrients in food crops. J Trace Element Med Biol 18:299–307Google Scholar
  116. Welsch R, Arango J, Bar C, Salazar B, Al-Babili S, Beltran J, Chavarriaga P, Ceballos H, Tohme J, Beyer P (2010) Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. Plant Cell 22:3348–3356PubMedGoogle Scholar
  117. Wirth J, Poletti S, Aeschlimann B, Yakandawala N, Drosse B, Osorio S, Tohge T, Fernie AR, Günther D, Gruissem W, Sautter C (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol J 7:631–644PubMedGoogle Scholar
  118. Wu F (2006) Mycotoxin reduction in Bt corn: potential economic, health, and regulatory impacts. Transgenic Res 15:277–289PubMedGoogle Scholar
  119. Wu G, Truksa M, Datla N, Vrinten P, Bauer J, Zank T, Cirpus P, Qiu X (2005) Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants. Nat Biotechnol 23:1013–1017PubMedGoogle Scholar
  120. Wu XR, Kenzior A, Willmot D, Scanlon S, Chen Z, Topin A, He SH, Acevedo A, Folk WR (2007) Altered expression of plant lysyl tRNA synthetase promotes tRNA misacylation and translation recoding of lysine. Plant J 50:627–663PubMedGoogle Scholar
  121. Yamada T, Tozawa Y, Hasegawa H, Terakawa T, Ohkawa Y, Wakasa K (2004) Use of a feedback-insensitive a subunit of anthranilate synthase as a selectable marker for transformation of rice and potato. Mol Breed 14:363–373Google Scholar
  122. Yang RY, Tsou SCS (2006) Enhancing iron bioavailability of vegetables through proper preparation—principles and applications. AVRDC—The World Vegetable Center, Taiwan. J International Cooperation 1:107–119Google Scholar
  123. Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305PubMedGoogle Scholar
  124. Yu J, Peng P, Zhang X, Zhao Q, Zhu D, Sun X, Liu J, Ao G (2004) Seed-specific expression of a lysine rich protein sb401 gene significantly increases both lysine and total protein content in maize seeds. Mol Breed 14:1–7Google Scholar
  125. Yuan D, Bassie L, Sabalza M, Miralpeix B, Dashevskaya S, Farre G, Rivera SM, Banakar R, Bai C, Sanahuja G, Arjo G, Avilla E, Zorrilla-López U, Ugidos-Damboriena N, López A, Almacellas D, Zhu C, Capell T, Hahne G, Twyman RM, Christou P (2011) Potential impact of plant biotechnology on the Millennium Development Goals. Plant Cell Rep 30:249–265PubMedGoogle Scholar
  126. Zheng L, Chengz AiC, Jiang X, Bei X, Zheng Y, Glahn RP, Welch RP, Miller DD, Lei XG, Shou H (2010) Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5:e10190PubMedGoogle Scholar
  127. Zhu C, Naqvi S, Gomez-Galera S, Pelacho AM, Capell T, Christou P (2007) Transgenic strategies for the nutritional enhancement of plants. Trends Plant Sci 12:548–555PubMedGoogle Scholar
  128. Zhu C, Naqvi S, Breitenbach J, Sandman G, Christou P, Capell T (2008) Combinatorial genetic transformation generated a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci USA 105:18232–18237PubMedGoogle Scholar
  129. Zhu C, Naqvi S, Capell T, Christou P (2009) Metabolic engineering of ketocarotenoid biosynthesis in higher plants. Arch Biochem Biophys 483:182–190PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Eduard Pérez-Massot
    • 1
  • Raviraj Banakar
    • 1
  • Sonia Gómez-Galera
    • 1
  • Uxue Zorrilla-López
    • 1
  • Georgina Sanahuja
    • 1
  • Gemma Arjó
    • 2
  • Bruna Miralpeix
    • 1
  • Evangelia Vamvaka
    • 1
  • Gemma Farré
    • 1
  • Sol Maiam Rivera
    • 3
  • Svetlana Dashevskaya
    • 1
  • Judit Berman
    • 1
  • Maite Sabalza
    • 1
  • Dawei Yuan
    • 1
  • Chao Bai
    • 1
  • Ludovic Bassie
    • 1
  • Richard M. Twyman
    • 4
  • Teresa Capell
    • 1
  • Paul Christou
    • 1
    • 5
  • Changfu Zhu
    • 1
  1. 1.Department of Plant Production and Forestry Science, ETSEAUniversity of Lleida-Agrotecnio CenterLleidaSpain
  2. 2.Department of MedicineUniversity of LleidaLleidaSpain
  3. 3.Chemistry Department, ETSEAUniversity of LleidaLleidaSpain
  4. 4.Department of Biological SciencesUniversity of WarwickCoventryUK
  5. 5.Institució Catalana de Recerca i Estudis AvançatsBarcelonaSpain

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