Encyclopedia of Sustainability Science and Technology

2012 Edition
| Editors: Robert A. Meyers

Biotechnology and Nutritional Improvement of Crops

  • Gemma Farre
  • Sonia Gomez-Galera
  • Shaista Naqvi
  • Chao Bai
  • Georgina Sanahuja
  • Dawei Yuan
  • Uxue Zorrilla
  • Laura Tutusaus Codony
  • Eduard Rojas
  • Marc Fibla
  • Richard M. Twyman
  • Teresa Capell
  • Paul Christou
  • Changfu Zhu
Reference work entry
DOI: https://doi.org/10.1007/978-1-4419-0851-3_160

Definition of the Subject and Its Importance

Food insecurity is one of the most important social issues faced today, with nearly one billion people enduring chronic hunger and an additional two billion people suffering from nutrient deficiencies, mostly in the developing world. Strategies to address food insecurity must ultimately address underlying problems such as poverty and poor governance/infrastructure, but the improvement of agricultural productivity in the developing world is an important goal, and biotechnology is one of a raft of measures being considered to achieve it. Genetically engineered plants provide one route to sustainable higher yields, which will increase the quantity of food available. However, genetic engineering can also increase the nutritional quality of crops, and this is the definition elaborated in this article. In particular, the focus is on biotechnology-based methods to increase the availability of essential nutrients, which are often limiting in...

This is a preview of subscription content, log in to check access.


Primary Literature

  1. 1.
    FAO (2006) The state of food insecurity in the world 2006. FAO, RomeGoogle Scholar
  2. 2.
    Christou P, Twyman RM (2004) The potential of genetically enhanced plants to address food insecurity. Nutr Res Rev 17:23–42CrossRefGoogle Scholar
  3. 3.
    Ramessar K, Naqvi S, Dashevskaya S, Peremarti A, Yuan D, Gomez-Galera D, Velez SMR, Farre G, Sabalza M, Miralpeix B, Twyman RM, Zhu C, Bassie L, Capell T, Christou P (2009) The contribution of plant biotechnology to food security in the 21st century. In: Amsel L, Hirsch L (eds) Food science and security. Nova Science, New YorkGoogle Scholar
  4. 4.
    FAO/WHO (2002) Human vitamin and mineral requirements. Report of a joint FAO/WHO expert consultation. FAO/WHO Press, Rome/GenevaGoogle Scholar
  5. 5.
    FAO/WHO/UNU (2007) Protein and amino acid requirements in human nutrition. Report of a joint WHO/FAO/UNU Expert Consultation. FAO/WHO Press, Rome/GenevaGoogle Scholar
  6. 6.
    Burr GO, Burr MM, Miller E (1930) On the fatty acids essential in nutrition. III. J Biol Chem 86:1–9Google Scholar
  7. 7.
    Fürst P, Stehle P (2004) What are the essential elements needed for the determination of amino acid requirements in humans? J Nutr 134:1558S–1565SGoogle Scholar
  8. 8.
    Harrison EH (2005) Mechanisms of digestion and absorption of dietary vitamin A. Annu Rev Nutr 25:87–103CrossRefGoogle Scholar
  9. 9.
    UNICEF (2006) Vitamin A deficiency. http://www.childinfo.org/areas/vitamina/
  10. 10.
    Scott JM, Kirke P, Molloy A, Daly L, Weir D (1994) The role of folate in the prevention of neural tube defects. Proc Nutr Soc 53:631–636CrossRefGoogle Scholar
  11. 11.
    Basu TK, Dickerson JWT (1996) Vitamin C (ascorbic acid). In: Basu TK, Dickerson JWT (eds) Vitamins in health and disease. CAB International, Oxford, UK, pp 125–147Google Scholar
  12. 12.
    WHO (2003) Battling iron deficiency anemia: the challenge. WHO Press, GenevaGoogle Scholar
  13. 13.
    Schümann K (2001) Safety aspects of iron in food. Ann Nutr Metab 45:91–101CrossRefGoogle Scholar
  14. 14.
    Maret W, Sandstead HH (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20:3–18CrossRefGoogle Scholar
  15. 15.
    WHO (2004) Iodine status worldwide: WHO global database on iodine deficiency. WHO Press, GenevaGoogle Scholar
  16. 16.
    Lyons GH, Stangoulis JCR, Graham RD (2004) Exploiting micronutrient interaction to optimize biofortification programs: The case for inclusion of selenium and iodine in the HarvestPlus Program. Nutr Rev 62:247–252Google Scholar
  17. 17.
    Lyons GH, Lewis J, Lorimer MF, Holloway RE, Brace DM, Stangoulis JCR, Graham RD (2004) High-selenium wheat: agronomic biofortification strategies to improve human nutrition. Food Agric Environ 2:171–178Google Scholar
  18. 18.
    Combs GF (2001) Selenium in global food system. Br J Nutr 85:517–547CrossRefGoogle Scholar
  19. 19.
    Shrimpton R, Schultink W (2002) Can supplements help meet the micronutrient needs of the developing world? Proc Nutr Soc 61:223–229CrossRefGoogle Scholar
  20. 20.
    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 Fund. WHO Press, GenevaGoogle Scholar
  21. 21.
    Allen LH, Gillespie SR (2001) What works? A review of the efficacy and effectiveness of nutrition interventions. ACC/SCN/Asian Development Bank, Geneva/ManilaGoogle Scholar
  22. 22.
    Black RE (2003) Zinc deficiency, infectious disease and mortality in the developing world. J Nutr 133:1485S–1489SGoogle Scholar
  23. 23.
    Gomez-Galera S, Rojas E, Sudhakar D, Zhu C, Pelacho AM, Capell T, Christou P (2010) Critical evaluation of strategies for mineral fortification of staple food crops. Transgenic Res 19:165–180CrossRefGoogle Scholar
  24. 24.
    Underwood BA, Smitasiri S (1999) Micronutrient malnutrition: policies and programs for control and their implications. Annu Rev Nutr 19:303–324CrossRefGoogle Scholar
  25. 25.
    UNICEF (2008) Sustainable elimination of iodine deficiency. UNICEF, New YorkGoogle Scholar
  26. 26.
    Sadighi J, Mohammad K, Shikholeslam R, Amirkhani MA, Torabi P, Salehi F, Abdolahi Z (2009) Anaemia control: lessons from the flour fortification programme. Public Health 123:794–799CrossRefGoogle Scholar
  27. 27.
    Frossard E, Bucher M, Mächler F, Mozafar A, Hurrell R (2000) Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition. J Sci Food Agric 80:861–879CrossRefGoogle Scholar
  28. 28.
    Li Y, Diosady LL, Jankowski S (2008) Effect of iron compounds on the storage stability of multiple-fortified Ultra Rice®. Int J Food Sci Technol 43:423–429CrossRefGoogle Scholar
  29. 29.
    Zimmermann MB, Wegmueller R, Zeder C, Chaouki N, Biebinger R, Hurrell RF, Windhab E (2004) Triple fortification of salt with microcapsules of iodine, iron, and vitamin A. J Clin Nutr 80:1283–1290Google Scholar
  30. 30.
    IZINCG (2007) Zinc fortification (technical brief 4). http://www.izincg.org/index.php
  31. 31.
    Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, Wasantwisut E, Furr H, Wieringa FT (2009) Decreased prevalence of anemia and improved micronutrient status and effectiveness of deworming in rural Vietnamese school children. J Nutr 139:1013–1021CrossRefGoogle Scholar
  32. 32.
    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 12:548–555CrossRefGoogle Scholar
  33. 33.
    Jeong J, Guerinot ML (2008) Biofortified and bioavailable: The gold standard for plant-based diets. Proc Natl Acad Sci USA 105:1777–1778CrossRefGoogle Scholar
  34. 34.
    Naqvi S, Zhu C, Farre G, Sandmann G, Capell T, Christou P (2010) Synergistic metabolism in hybrid corn reveals bottlenecks in the carotenoid pathway and leads to the accumulation of extraordinary levels of the nutritionally important carotenoid zeaxanthin. Plant Biotechnol J. doi:10.1111/j.1467-7652.2010.00554.x.Google Scholar
  35. 35.
    Stein AJ, Meenakshi JV, Qaim M, Nestel P, Sachdev HPS, Bhutta ZA (2008) Potential impacts of iron biofortification in India. Soc Sci Med 66:1797–1808CrossRefGoogle Scholar
  36. 36.
    Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17CrossRefGoogle Scholar
  37. 37.
    Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364CrossRefGoogle Scholar
  38. 38.
    White PJ, Broadley MR (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci 10:586–593CrossRefGoogle Scholar
  39. 39.
    Wong JC, Lambert RJ, Wurtzel ET, Rocheford TR (2004) QTL and candidate genes phytoene synthase and zeta-carotene desaturase associated with the accumulation of carotenoids in maize. Theor Appl Genet 108:349–359CrossRefGoogle Scholar
  40. 40.
    Santos CA, Simon PW (2002) QTL analyses reveal clustered loci for accumulation of major provitamin A carotenes and lycopene in carrot roots. Mol Genet Genomics 268:122–129CrossRefGoogle Scholar
  41. 41.
    Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, Yan J, Buckler ES (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319:330–333CrossRefGoogle Scholar
  42. 42.
    Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, Fernandez MG, Zaharieva M, Babu R, Fu Y, Palacios N, Li J, Dellapenna D, Brutnell T, Buckler ES, Warburton ML, Rocheford T (2010) Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat Genet 42:322–327CrossRefGoogle Scholar
  43. 43.
    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 70:77–142CrossRefGoogle Scholar
  44. 44.
    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 182:49–84CrossRefGoogle Scholar
  45. 45.
    Prasanna BM, Vasal SK, Singh NN (2001) Quality protein maize. Curr Sci 81:1308–1319Google Scholar
  46. 46.
    Zarkadas C, Hamilton R, Yu Z, Choi V, Khanizadeh S, Rose N, Pattison P (2000) Assessment of the protein quality of 15 new northern adapted cultivars of quality protein maize using amino acid analysis. J Agric Food Chem 48:5351–5361CrossRefGoogle Scholar
  47. 47.
    Segal G, Song R, Messing J (2003) A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165:387–397Google Scholar
  48. 48.
    Huang S, Frizzi A, Florida C, Kriger D, Luethy M (2006) High lysine and high tryptophan transgenic maize resulting from the reduction of both 19- and 22-kD α-zeins. Plant Mol Biol 61:525–535CrossRefGoogle Scholar
  49. 49.
    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 130:189–196CrossRefGoogle Scholar
  50. 50.
    Stöger E, Parker M, Christou P, Casey R (2001) Pea legumin overexpressed in wheat endosperm assembles into an ordered paracrystalline matrix. Plant Physiol 125:1732–1742CrossRefGoogle Scholar
  51. 51.
    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
  52. 52.
    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 14:1–7CrossRefGoogle Scholar
  53. 53.
    Yang S, Moran D, Jia H, Bicar E, Lee M, Scott M (2002) Expression of a synthetic porcine α-lactoalbumin gene in the kernels of transgenic maize. Transgenic Res 11:11–20CrossRefGoogle Scholar
  54. 54.
    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 17:59–71CrossRefGoogle Scholar
  55. 55.
    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 50:627–663CrossRefGoogle Scholar
  56. 56.
    Muntz K, Christov V, Saalbach G, Saalbach I, Waddell D, Pickardt T, Schieder O, Wustenhagen T (1998) Genetic engineering for high methionine grain legumes. Nahrung 42:125–127CrossRefGoogle Scholar
  57. 57.
    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 97:3724–3729CrossRefGoogle Scholar
  58. 58.
    Chiaiese P, Ohkama-Ohtsu N, Molvig L, Godfree R, Dove H, Hocart C, Fujiwara T, Higgins TJ, Tabe LM (2004) Sulphur and nitrogen nutrition influence the response of chickpea seeds to an added, transgenic sink for organic sulphur. J Exp Bot 55:1889–1901CrossRefGoogle Scholar
  59. 59.
    Pastorello EA, Pompei C, Pravettoni V, Brenna O, Farioli L, Trambaioli C, Conti A (2001) Lipid transfer proteins and 2S albumins as allergens. Allergy 56:45–47CrossRefGoogle Scholar
  60. 60.
    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 108:335–342CrossRefGoogle Scholar
  61. 61.
    Tamás C, Kisgyorgy BN, Rakszegi M, Wilkinson MD, Yang MS, Láng L, Tamás L, Bedo Z (2009) Transgenic approach to improve wheat (Triticum aestivum L.) nutritional quality. Plant Cell Rep 28:1085–1094CrossRefGoogle Scholar
  62. 62.
    Zhang P, Jaynes JM, Potrykus I, Gruissem W, Puonti-Kaerlas J (2003) Transfer and expression of an artificial storage protein (asp1) gene in cassava (Manihot esculenta Crantz). Transgenic Res 12:243–250CrossRefGoogle Scholar
  63. 63.
    Galili G, Höfgen R (2002) Metabolic engineering of amino acids and storage proteins in plants. Metab Eng 4:3–11CrossRefGoogle Scholar
  64. 64.
    Frizzi A, Huang S, Gilbertson LA, Armstrong TA, Luethy MH, Malvar TM (2008) Modifying lysine biosynthesis and catabolism in corn with a single bifunctional expression/silencing transgene cassette. Plant Biotechnol J 6:13–21Google Scholar
  65. 65.
    Falco SC, Guida T, Locke M, Mauvais J, Sandres C, Ward RT, Webber P (1995) Transgenic canola and soybean seeds with increased lysine. Biotechnol (NY) 13:577–582CrossRefGoogle Scholar
  66. 66.
    Mazur B, Krebbers E, Tingey S (1999) Gene discovery and product development for grain quality traits. Science 285:372–375CrossRefGoogle Scholar
  67. 67.
    Karchi H, Shaul O, Galili G (1994) Lysine synthesis and catabolism are coordinately regulated during tobacco seed development. Proc Natl Acad Sci USA 91:2577–2581CrossRefGoogle Scholar
  68. 68.
    Karchi H, Miron D, Ben-Yaacob S, Galili G (1995) The lysine-dependent stimulation of lysine catabolism in tobacco seeds requires calcium and protein phosphorylation. Plant Cell 7:1963–1970Google Scholar
  69. 69.
    Zhu X, Galili G (2003) Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15:845–853CrossRefGoogle Scholar
  70. 70.
    Huang S, Kruger DE, Frizzi A, D’Ordine RL, Florida CA, Adams WR, Brown WE, Luethy MH (2005) High-lysine corn produced by the combination of enhanced lysine biosynthesis and reduced zein accumulation. Plant Biotechnol J 3:555–569CrossRefGoogle Scholar
  71. 71.
    Houmard NM, Mainville JL, Bonin CP, Huang S, Luethy MH, Malvar TM (2007) High-lysine corn generated by endosperm-specific suppression of lysine catabolism using RNAi. Plant Biotechnol J 5:605–614CrossRefGoogle Scholar
  72. 72.
    Hacham Y, Avraham T, Amir R (2002) The N-terminal region of Arabidopsis cystathionine gamma-synthase plays an important regulatory role in methionine metabolism. Plant Physiol 128:454–462CrossRefGoogle Scholar
  73. 73.
    Hacham Y, Schuster G, Amir R (2006) An in vivo internal deletion in the N-terminus region of Arabidopsis cystathionine gamma-synthase results in CGS expression that is insensitive to methionine. Plant J 45:955–967CrossRefGoogle Scholar
  74. 74.
    Hacham Y, Matityahu I, Schuster G, Amir R (2008) Overexpression of mutated forms of aspartate kinase and cystathionine gamma-synthase in tobacco leaves resulted in the high accumulation of methionine and threonine. Plant J 54:260–271CrossRefGoogle Scholar
  75. 75.
    Cho HJ, Brotherton JE, Song HS, Widholm JM (2000) Increasing tryptophan synthesis in a forage legume Astragalus sinicus by expressing the tobacco feedback-insensitive anthranilate synthase (ASA2) gene. Plant Physiol 123:1069–1076CrossRefGoogle Scholar
  76. 76.
    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 Exp Bot 57:3069–3078CrossRefGoogle Scholar
  77. 77.
    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 14:363–373CrossRefGoogle Scholar
  78. 78.
    Ishimoto M, Rahman SM, Hanafy MS, Khalafalla MM, El-Shemy HA, Nakamoto Y, Kita Y, Takanashi K, Matsuda F, Murano Y, Funadashi 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 25:313–326CrossRefGoogle Scholar
  79. 79.
    Inaba Y, Brotherton JE, Ulanov A, Widholm JM (2007) Expression of a feedback insensitive anthranilate synthase gene from tobacco increases free tryptophan in soybean plants. Plant Cell Rep 26:1763–1771CrossRefGoogle Scholar
  80. 80.
    Tabe L, Wirtz M, Molvig L, Droux M, Hell R (2009) Overexpression of serine acetlytransferase produced large increases in O-acetylserine and free cysteine in developing seeds of a grain legume. J Exp Bot 61:721–733CrossRefGoogle Scholar
  81. 81.
    Goyens P, Spilker M, Zock P, Katan M, Mensink R (2005) Compartmental modeling to quantify γ-linolenic acid conversion after longer term intake of multiple tracer boluses. J Lipid Res 46:1474–1483CrossRefGoogle Scholar
  82. 82.
    Napier JA (2007) The production of unusual fatty acids in transgenic plants. Annu Rev Plant Biol 58:295–319CrossRefGoogle Scholar
  83. 83.
    Robert SS (2005) Production of eicosapentaenoic and docosahexaenoic acid-containing oils in transgenic land plants for human and aquaculture nutrition. Mar Biotechnol 8:103–109CrossRefGoogle Scholar
  84. 84.
    Truksa M, Vrinten P, Qiu X (2009) Metabolic engineering of plants for polyunsaturated fatty acid production. Mol Breed 23:1–11CrossRefGoogle Scholar
  85. 85.
    Wu G, Truksa M, Datla N, Vrinten P, Bauer J, Zank T, Cirpus P, Heinz E, Qiu X (2005) Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants. Nat Biotechnol 23:1013–1017CrossRefGoogle Scholar
  86. 86.
    Kajikawa M, Matsui D, Ochiai M, Tanak Y, Kita Y, Ishimoto M, Kohzu Y, Shoji S, Yamato KT, Ohyama K, Fukuzawa H, Kohchi T (2008) Production of arachidonic and eicosapentaenoic acids in plants using bryophyte fatty acid Δ6-desaturase, Δ6-elongase and Δ5-desaturase genes. Biosci Biotechnol Biochem 72:435–444CrossRefGoogle Scholar
  87. 87.
    Kinney AJ, Cahoon EB, Damude HG, Hitz WD, Kolar CW, Liu Z-B (2004) Production of very long chain polyunsaturated fatty acids in oilseed plants. WO 2004/071467 A2Google Scholar
  88. 88.
    Qi B, Fraser T, Mugford S, Dobson G, Sayanova O, Butler J, Napier JA, Stobart AK, Lazarus CM (2004) Production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in plants. Nat Biotechnol 22:739–745CrossRefGoogle Scholar
  89. 89.
    Eisenreich W, Schwarz M, Cartavrade A, Arigoni D, Zenk MH, Bacher A (1998) The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem Biol 5:221–233CrossRefGoogle Scholar
  90. 90.
    Zhu C, Naqvi S, Capell T, Christou P (2009) Metabolic engineering of ketocarotenoid biosynthesis in higher plants. Arch Biochem Biophys 483:182–190CrossRefGoogle Scholar
  91. 91.
    Enfissi E, Fraser P, Lois L, Boronat A, Schuch W, Bramley P (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 3:17–27CrossRefGoogle Scholar
  92. 92.
    Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305CrossRefGoogle Scholar
  93. 93.
    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 23:482–487CrossRefGoogle Scholar
  94. 94.
    Aluru M, Xu Y, Guo R, Wang Z, Li S, White W, Wang K, Rodermel S (2008) Generation of transgenic maize with enhanced provitamin A content. J Exp Bot 59:3551–3562CrossRefGoogle Scholar
  95. 95.
    Zhu C, Naqvi S, Breitenbach J, Sandmann G, Christou P, Capell T (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in corn. Proc Natl Acad Sci USA 105:18232–18237CrossRefGoogle Scholar
  96. 96.
    Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J, Conesa D, Ros G, Sandmann G, Capell T, Christou P (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106:7762–7767CrossRefGoogle Scholar
  97. 97.
    Shewmaker CK, Sheehy JA, Daley M, Colburn S, Ke DY (1999) Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J 20:401–412CrossRefGoogle Scholar
  98. 98.
    Ravanello M, Dangyang K, Alvarez J, Huang B, Shewmaker C (2003) Coordinate expression of multiple bacterial carotenoid genes in canola leading to altered carotenoid production. Metab Eng 5:255–263CrossRefGoogle Scholar
  99. 99.
    Fujisawa M, Takita E, Harada H, Sakurai N, Suzuki H, Ohyama K, Shibata D, Misawa N (2009) Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation. J Exp Bot 60:1319–1332CrossRefGoogle Scholar
  100. 100.
    Diretto G, Welsch R, Tavazza MF, Pizzichini D, Beyer P, Giuliano G (2007) Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers. BMC Plant Biol 7:11CrossRefGoogle Scholar
  101. 101.
    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. PLoS ONE 2:e350CrossRefGoogle Scholar
  102. 102.
    Rosati C, Aquilani R, Dharmapuri S, Pallara P, Marusic C, Tavazza R, Bouvier F, Camara B, Giuliano G (2000) Metabolic engineering of beta-carotene and lycopene content in tomato fruit. Plant J 24:413–419CrossRefGoogle Scholar
  103. 103.
    D’Ambrosio C, Giorio G, Marino I, Merendino A, Petrozza A, Salfi L, Stigliani A, Cellini F (2004) Virtually complete conversion of lycopene into beta-carotene in fruits of tomato plants transformed with the tomato lycopene beta-cyclase (tlcy-b) cDNA. Plant Sci 166:207–214CrossRefGoogle Scholar
  104. 104.
    Dharmapuri S, Rosati C, Pallara P, Aquilani R, Bouvier F, Camara B, Giuliano G (2002) Metabolic engineering of xanthophylls content in tomato fruits. FEBS Lett 519:30–34CrossRefGoogle Scholar
  105. 105.
    Apel W, Bock R (2009) Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene to provitamin A conversion. Plant Physiol 151:59–66CrossRefGoogle Scholar
  106. 106.
    Wurbs D, Ruf S, Bock R (2007) Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J 49:276–288CrossRefGoogle Scholar
  107. 107.
    Davuluri GR, van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Bramley PM, Pennings HM, Bowler C (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23:890–895CrossRefGoogle Scholar
  108. 108.
    Li L, Paolillo DJ, Parthasarathy MV, Dimuzio EM, Garvin DF (2001) A novel gene mutation that confers abnormal patterns of beta-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26:59–67CrossRefGoogle Scholar
  109. 109.
    Lu S, Eck J, Zhou X, Lopez A, O’Halloran D, Cosman K, Conlin B, Paolillo D, Garvin D, Vrebalov J, Kochian L, Küpper H, Earle E, Cao J, Lia L (2006) The cauliflower Or gene encodes a DNAJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell 18:3594–3605CrossRefGoogle Scholar
  110. 110.
    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 59:213–223CrossRefGoogle Scholar
  111. 111.
    DellaPenna D, Pogson B (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–773CrossRefGoogle Scholar
  112. 112.
    Collakova E, DellaPenna D (2003) The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in the regulation of tocopherol synthesis during abiotic stress. Plant Physiol 133:930–940CrossRefGoogle Scholar
  113. 113.
    Tsegaye Y, Shintani D, DellaPenna D (2002) Overexpression of the enzyme p-hydroxyphenylpyruvate dioxygenase in Arabidopsis and its relation to tocopherol biosynthesis. Plant Physiol Biochem 40:913–920CrossRefGoogle Scholar
  114. 114.
    Falk J, Brosch M, Schäfer A, Braun S, Krupinska K (2005) Characterization of transplastomic tobacco plants with a plastid localized barley 4-hydroxyphenylpyruvate dioxygenase. J Plant Physiol 162:738–742CrossRefGoogle Scholar
  115. 115.
    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 19:16–22Google Scholar
  116. 116.
    Raclaru M, Gruber J, Kumar R, Sadre R, Luhs W, Zarhloul K, Friedt W, Frentzen M, Weier D (2006) Increase of the tocochromanol content in transgenic Brassica napus seeds by overexpression of key enzymes involved in prenylquinone biosynthesis. Mol Breed 18:93–107CrossRefGoogle Scholar
  117. 117.
    Rippert P, Scimemi C, Dubald M, Matringe M (2004) Engineering plant shikimate pathway for production of tocotrienol and improving herbicide resistance. Plant Physiol 134:92–100CrossRefGoogle Scholar
  118. 118.
    Karunanandaa B, Qi Q, Haoa M, Baszis S, Jensen P, Wong Y, Jiang J, Venkatramesh M, Gruys K, Moshiri F, Beittenmiller D, Weiss J, Valentin H (2005) Metabolically engineered oilseed crops with enhanced seed tocopherol. Metab Eng 7:384–400CrossRefGoogle Scholar
  119. 119.
    Van Eenennaam A, Lincoln K, Durrett T, Valentin H, Shewmaker C, Thorne G, Jiang J, Baszis S, Levering C, Aasen E, Hao M, Stein J, Norris S, Last R (2003) Engineering vitamin E content: from Arabidopsis mutant to soy oil. Plant Cell 15:3007–3019CrossRefGoogle Scholar
  120. 120.
    Tavva 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 26:61–70CrossRefGoogle Scholar
  121. 121.
    Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369CrossRefGoogle Scholar
  122. 122.
    Ishikawa T, Dowdle J, Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126:343–355CrossRefGoogle Scholar
  123. 123.
    Chen Z, Young T, Ling J, Chang S, Gallie D (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530CrossRefGoogle Scholar
  124. 124.
    Jain AK, Nessler CL (2000) Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol Breed 6:73–78CrossRefGoogle Scholar
  125. 125.
    Badejo A, Eltelib H, Fukunaga K, Fujikawa Y, Esaka M (2009) Increase in ascorbate content of transgenic tobacco plants overexpressing the acerola (Malpighia glabra) phosphomannomutase gene. Plant Cell Physiol 50:423–428CrossRefGoogle Scholar
  126. 126.
    Laing WA, Wright MA, Cooney J, Bulley SM (2007) The missing step of the l-galactose pathway of ascorbate biosynthesis in plants, an l-galactose guanyltransferase, increases leaf ascorbate content. Proc Natl Acad Sci USA 104:9534–9539CrossRefGoogle Scholar
  127. 127.
    Bulley SM, Rassam M, Hoser D, Otto W, Schünemann N, Wright M, MacRae E, Gleave A, Laing W (2009) Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-l-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot 60:765–778CrossRefGoogle Scholar
  128. 128.
    Díaz de la Garza RI, Quinlivan EP, Klaus SM, Basset GJ, Gregory JF III, Hanson AD (2004) Folate biofortification in tomatoes by engineering the pteridine branch of folate synthesis. Proc Natl Acad Sci USA 101:13720–13725CrossRefGoogle Scholar
  129. 129.
    Díaz de la Garza R, Quinlivan EP, Klaus SM, Basset GJ, Gregory JF, Hanson AD (2007) Folate biofortification in tomatoes by engineering the pteridine branch of folate synthesis. Proc Natl Acad Sci USA 104:4218–4222CrossRefGoogle Scholar
  130. 130.
    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 25:1277–1279CrossRefGoogle Scholar
  131. 131.
    Fouad W, Rathinasabapathi B (2006) Expression of bacterial l-aspartate-α-decarboxilase in tobacco increases β-alanine and pantothenate levels and improves thermotolerance. Plant Mol Biol 60:495–505CrossRefGoogle Scholar
  132. 132.
    Chakauya E, Coxon K, Wei M, MacDonald M, Barsby T, Abell C, Smith A (2008) Towards engineering increased pantothenate (vitamin B5) levels in palnts. Plant Mol Biol 68:493–503CrossRefGoogle Scholar
  133. 133.
    Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346CrossRefGoogle Scholar
  134. 134.
    Ghandilyan A, Vreugdenhil D, Aarts MGM (2006) Progress in the genetic understanding of plant iron and zinc nutrition. Physiol Plant 126:407–417CrossRefGoogle Scholar
  135. 135.
    Takahashi M, Nakanishi H, Kawasaki S, Nishizawa N, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469CrossRefGoogle Scholar
  136. 136.
    Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263–1280CrossRefGoogle Scholar
  137. 137.
    Ramesh SA, Choimes S, Schachtman DP (2004) Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Mol Biol 54:373–385CrossRefGoogle Scholar
  138. 138.
    Tiong J, Genc Y, McDonald GK, Langridge P, Huang CY (2009) Over-expressing a barley ZIP gene doubles grain zinc content in barley (Hordeum vulgare). In: Proceedings of the international plant nutrition colloquium XVI. UC Davis, CaliforniaGoogle Scholar
  139. 139.
    Van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JA, Hooykaas PJ (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 119:1047–1055CrossRefGoogle Scholar
  140. 140.
    Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389CrossRefGoogle Scholar
  141. 141.
    Pilon-Smits EAH, Hwang S, Lytle CM, Zhu Y, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction and tolerance. Plant Physiol 119:123–132CrossRefGoogle Scholar
  142. 142.
    Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51:401–432CrossRefGoogle Scholar
  143. 143.
    LeDuc DJ, AbdelSamie M, Móntes-Bayon M, Wu CP, Reisinger SJ, Terry N (2006) Overexpressing both ATP sulfurylase and selenocysteine methyltransferase enhances selenium phytoremediation traits in Indian mustard. Environ Pollut 144:70–76CrossRefGoogle Scholar
  144. 144.
    McKenzie MJ, Hunter DA, Pathirana R, Watson LM, Joyce NI, Matich AJ, Rowan DD, Brummell DA (2009) Accumulation of an organic anticancer selenium compound in a transgenic Solanaceous species shows wider applicability of the selenocysteine methyltransferase transgene from selenium hyperaccumulators. Transgenic Res 18:407–424CrossRefGoogle Scholar
  145. 145.
    Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427CrossRefGoogle Scholar
  146. 146.
    Park S, Kim CK, Pike LM, Smith RH, Hirschi KD (2004) Increased calcium in carrots by expression of an Arabidopsis H+/Ca2+ transporter. Mol Breed 14:275–282CrossRefGoogle Scholar
  147. 147.
    Park S, Kang 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 53:5598–5603CrossRefGoogle Scholar
  148. 148.
    Connolly EL (2008) Raising the bar for biofortification: enhanced levels of bioavailable calcium in carrots. Trends Biotechnol 26:401–403CrossRefGoogle Scholar
  149. 149.
    Park S, Elless MP, Park J, Jenkins A, Lim W, Chambers E IV, Hirschi KD (2009) Sensory analysis of calcium-biofortified lettuce. Plant Biotechnol J 7:106–117CrossRefGoogle Scholar
  150. 150.
    Kim CK, Han JS, Lee HS, Oh JY, Shigaki T, Park SH, Hirschi K (2006) Expression of an Arabidopsis CAX2 variant in potato tubers increases calcium levels with no accumulation of manganese. Plant Cell Rep 25:1226–1232CrossRefGoogle Scholar
  151. 151.
    Sellappan K, Datta K, Parkhi V, Datta SK (2009) Rice caryopsis structure in relation to distribution of micronutrients (iron, zinc, beta-carotene) of rice cultivars including transgenic indica rice. Plant Sci 177:557–562CrossRefGoogle Scholar
  152. 152.
    Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seeds by the soybean ferritin gene. Nat Biotechnol 17:282–286CrossRefGoogle Scholar
  153. 153.
    Drakakaki G, Christou P, Stöger E (2000) Constitutive expression of soybean ferritin cDNA in transgenic wheat and rice results in increased iron levels in vegetative tissues but not in seeds. Transgenic Res 9:445–452CrossRefGoogle Scholar
  154. 154.
    Qu LQ, Yoshihara T, Ooyama A, Goto F, Takaiwa F (2005) Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta 222:225–233CrossRefGoogle Scholar
  155. 155.
    Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, Oliveira M, Goto F, Datta SK (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164:371–378CrossRefGoogle Scholar
  156. 156.
    Hong-Xia Y, Mei L, Ze-Jian G, Qing-Yao S, Xiao-Hui X, Jin-Song B (2008) Evaluation and application of two high-iron transgenic rice lines expressing a pea ferritin gene. Rice Sci 15:51–56CrossRefGoogle Scholar
  157. 157.
    Wirth J, Poletti S, Aeschlimann B, Yakandawal 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 7:631–644CrossRefGoogle Scholar
  158. 158.
    Theil EC, Briat JF (2004) Plant ferritin and non-heme iron nutrition in humans, HarvestPlus technical monographs 1. International Food Policy Research Institute/International Center for Tropical Agriculture (CIAT), Washington, DC/CaliforniaGoogle Scholar
  159. 159.
    Karunaratne AM, Amerasinghe PH, Sadagopa Ramanujam VM, Sandstead HH, Perera PAJ (2008) Zinc, iron and phytic acid levels of some popular foods consumed by rural children in Sri Lanka. J Food Compos Anal 21:481–488CrossRefGoogle Scholar
  160. 160.
    Welch RM, Graham RD (2005) Agriculture: the real nexus for enhancing bioavailable micronutrients in food crops. J Trace Elem Med Biol 18:299–307CrossRefGoogle Scholar
  161. 161.
    Raboy V (2002) Progress in breeding low phytate crops. J Nutr 132:503S–505SGoogle Scholar
  162. 162.
    Liu QL, Xu XH, Ren XL, Fu HW, Wu DX, Shu QY (2007) Generation and characterization of low phytic acid germplasm in rice (Oryza sativa L.). Theor Appl Genet 114:803–814CrossRefGoogle Scholar
  163. 163.
    Campion B, Sparvoli F, Doria E, Tagliabue G, Galasso I, Fileppi M, Bollini R, Nielsen E (2009) Isolation and characterization of an lpa (low phytic acid) mutant in common bean (Phaseolus vulgaris L.). Theor Appl Genet 118:1211–1221CrossRefGoogle Scholar
  164. 164.
    Morris J, Nakata PA, McConn M, Brock A, Hirschi KD (2007) Increased calcium bioavailability in mice fed genetically engineered plants lacking calcium oxalate. Plant Mol Biol 64:613–618CrossRefGoogle Scholar
  165. 165.
    Brinch-Pedersen H, Hatzack F, Sørensen LD, Holm PB (2003) Concerted action of endogenous and heterologous phytase on phytic acid degradation in seed of transgenic wheat (Triticum aestivum L.). Transgenic Res 12:649–659CrossRefGoogle Scholar
  166. 166.
    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 54:4624–4632CrossRefGoogle Scholar
  167. 167.
    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 17:633–643CrossRefGoogle Scholar
  168. 168.
    Lucca P, Hurrell R, Potrykus I (2002) Fighting iron deficiency anemia with iron-rich rice. J Am Coll Nutr 21:184S–190SGoogle Scholar
  169. 169.
    Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stöger 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 59:869–880CrossRefGoogle Scholar
  170. 170.
    Halpin C, Barakate A, Askari BM, Abbott JC, Ryan MD (2001) Enabling technologies for manipulating multiple genes on complex pathways. Plant Mol Biol 47:295–310CrossRefGoogle Scholar
  171. 171.
    Farré G, Sanahuja G, Naqvi D, Bai C, Capell T, Zhu C, Christou P (2010) Travel advice on the road to carotenoids in plants. Plant Sci 179:28–48CrossRefGoogle Scholar
  172. 172.
    Bekaert S, Storozhenko S, Mehrshahi P, Bennett MJ, Lambert W, Gregory JF III, Schubert K, Hugenholtz J, Van Der Straeten D, Hanson AD (2008) Folate biofortification in food plants. Trends Plant Sci 13:28–35CrossRefGoogle Scholar

Books and Reviews

  1. Lemaux PG (2008) Genetically engineered plants and foods: a scientist’s analysis of the issues (Part I). Annu Rev Plant Biol 59:771–812CrossRefGoogle Scholar
  2. Lemaux PG (2009) Genetically engineered plants and foods: a scientist’s analysis of the issues (part II). Annu Rev Plant Biol 60:511–559CrossRefGoogle Scholar
  3. Mène-Saffrané L, DellaPenna D (2009) Biosynthesis, regulation and functions of tocochromanols in plants. Plant Physiol Biochem 48:301–309CrossRefGoogle Scholar
  4. Rosati C, Diretto G, Giuliano G (2009) Biosynthesis and engineering of carotenoids and apocarotenoids in plants: state of the art and future prospects. Biotechnol Genet Eng Rev 26:139–162CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Gemma Farre
    • 1
  • Sonia Gomez-Galera
    • 1
  • Shaista Naqvi
    • 1
  • Chao Bai
    • 1
  • Georgina Sanahuja
    • 1
  • Dawei Yuan
    • 1
  • Uxue Zorrilla
    • 1
  • Laura Tutusaus Codony
    • 1
  • Eduard Rojas
    • 1
  • Marc Fibla
    • 1
  • Richard M. Twyman
    • 2
  • Teresa Capell
    • 1
  • Paul Christou
    • 3
    • 4
  • Changfu Zhu
    • 1
  1. 1.Department of Vegetal Production and Forestry Science, ETSEAUniversity of LleidaLleidaSpain
  2. 2.Department of Biological SciencesUniversity of WarwickCoventryUK
  3. 3.Department de Produccio Vegetal i Ciencia ForestalUniversitat de Lleida/ICREALleidaSpain
  4. 4.Institució Catalana de Recerca i Estudis Avançats (ICREA)BarcelonaSpain