A golden era—pro-vitamin A enhancement in diverse crops

  • Chao Bai
  • Richard M. Twyman
  • Gemma Farré
  • Georgina Sanahuja
  • Paul Christou
  • Teresa Capell
  • Changfu Zhu
Invited Review

Abstract

Numerous crops have been bred or engineered to increase carotenoid levels in an effort to develop novel strategies that address vitamin A deficiency in the developing world. The pioneering work in rice (not covered in this review) has been followed up in many additional crops, some of which are staples like rice whereas others are luxury products whose impact on food security is likely to be marginal. This review surveys the progress that has been made in carotenoid breeding and metabolic engineering, focusing on β-carotene enhancement in crops other than rice. We ask if these efforts have the potential to address vitamin A deficiency in developing countries by comparing bioavailable pro-vitamin A levels in wild type and enhanced crops to determine whether nutritional requirements can be met without the consumption of unrealistic amounts of food. The potential impact of carotenoid enhancement should therefore be judged against benchmarks that include the importance of particular crops in terms of global food security, the amount of bioavailable β-carotene, and the amount of food that must be consumed to achieve the reference daily intake of vitamin A.

Keywords

Beta carotene Metabolic engineering Nutritional enhancement Biofortification Genetic engineering Food crops 

References

  1. Aluru M.; Xu Y.; Guo R.; Wang Z.; Li S.; White W.; Wang K.; Rodermel S. Generation of transgenic maize with enhanced provitamin A content. J. Exp. Bot. 59: 3551–3562; 2008.PubMedCrossRefGoogle Scholar
  2. Alvarez J. B.; Martin L. M.; Martin A. Genetic variation for carotenoid pigment content in the amphiploid Hordeum chilense × Triticum turgidum conv. durum. Plant Breed. 118: 187–189; 1999.CrossRefGoogle Scholar
  3. Ampomah-Dwamena C.; McGhie T.; Wibisono R.; Montefiori M.; Hellens R. P.; Allan A. C. The kiwifruit lycopene beta-cyclase plays a significant role in carotenoid accumulation in fruit. J. Exp. Bot. 60: 3765–3779; 2009.PubMedCrossRefGoogle Scholar
  4. Anderson J. M.; Waldron J. C.; Thorne S. W. Chlorophyll-protein complexes of spinach and barley thylakoids. FEBS Lett. 92: 227–233; 1978.CrossRefGoogle Scholar
  5. Apel W.; Bock R. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol. 151: 59–66; 2009.PubMedCrossRefGoogle Scholar
  6. Azevedo-Meleiro C. H.; Rodriguez-Amaya D. B. Qualitative and quantitative differences in carotenoid composition among Cucurbita moschata, Cucurbita maxima, and Cucurbita pepo. J. Agric. Food Chem. 55: 4027–4033; 2007.PubMedCrossRefGoogle Scholar
  7. Beyer P. Golden Rice and ‘Golden’ crops for human nutrition. New Biotechnol. 27: 478–481; 2010.CrossRefGoogle Scholar
  8. Bonierbale M. W.; Plaisted R. L.; Tanksley S. D. RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120: 1095–1103; 1988.PubMedGoogle Scholar
  9. Braumann T.; Weber G.; Grimme L. H. Carotenoid and chlorophyll composition of light harvesting and reaction centre proteins of the thylakoid membrane. Photobiochem Photobiophys 4: 1–8; 1982.Google Scholar
  10. Breitenbach J.; Sandmann G. ζ-Carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta 220: 785–793; 2005.PubMedCrossRefGoogle Scholar
  11. Buishand J. G.; Gableman W. H. Investigations of the inheritance of color and carotenoid content in phloem and xylem of carrot roots (Daucus carota L.). Euphytica 28: 611–632; 1979.CrossRefGoogle Scholar
  12. Capell T.; Christou P. Progress in plant metabolic engineering. Curr. Opin. Biotechnol. 15: 148–154; 2004.PubMedCrossRefGoogle Scholar
  13. Cazzonelli C. I.; Pogson B. J. Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 15: 266–274; 2010.PubMedCrossRefGoogle Scholar
  14. Cervantes-Flores J. C. Development of a genetic linkage map and QTL analysis in sweet potato. Mol. Breed. 21: 511–532; 2006.CrossRefGoogle Scholar
  15. Chander S.; Guo Y. Q.; Yang X. H.; Zhang J.; Lu X. Q.; Yan J. B.; Song T. M.; Rocheford T. R.; Li J. S. Using molecular markers to identify two major loci controlling carotenoid contents in maize grain. Theor. Appl. Genet. 116: 223–233; 2008.PubMedCrossRefGoogle Scholar
  16. Chappell J. Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Ann Rev Plant Physiol Plant Mol Biol 46: 521–547; 1995.CrossRefGoogle Scholar
  17. Chen Y.; Li F.; Wurtzel E. T. Isolation and characterization of the Z-ISO gene encoding a missing component of carotenoid biosynthesis in plants. Plant Physiol. 153: 66–79; 2010.PubMedCrossRefGoogle Scholar
  18. Clarke F. R.; Clarke J. M.; McCaig T. N.; Knox R. E.; DePauw R. M. Inheritance of yellow pigment concentration in seven durum wheat crosses. Canad J Plant Sci 86: 133–141; 2006.CrossRefGoogle Scholar
  19. Comai L.; Henikoff S. TILLING: practical single-nucleotide mutation discovery. Plant J. 45: 684–694; 2006.PubMedCrossRefGoogle Scholar
  20. Cong L.; Wang C.; Chen L.; Liu H.; Yang G.; He G. 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: 8652–8660; 2009.PubMedCrossRefGoogle Scholar
  21. Crisp P.; Walkey D. G. A.; Bellman E.; Roberts E. A mutation affecting curd colour in cauliflower (Brassica oleracea L. var. botrytis DC). Euphytica 24: 173–176; 1975.CrossRefGoogle Scholar
  22. Cuevas H. E.; Staub J. E.; Simon P. W.; Zalapa J. E.; McCreight J. D. Mapping of genetic loci that regulate quantity of beta-carotene in fruit of US Western Shipping melon (Cucumis melo L.). Theor. Appl. Genet. 117: 1345–1359; 2008.PubMedCrossRefGoogle Scholar
  23. Cuevas H. E.; Staub J. E.; Simon P. W.; Zalapa J. E. A consensus linkage map identifies genomic regions controlling fruit maturity and beta-carotene-associated flesh color in melon (Cucumis melon L.). Theor. Appl. Genet. 119: 741–756; 2009.PubMedCrossRefGoogle Scholar
  24. Cunningham Jr. F. X.; Pogson B.; Sun Z.; McDonald K. A.; DellaPenna D.; Gantt E. Functional analysis of the β and ε lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8: 1613–1626; 1996.PubMedCrossRefGoogle Scholar
  25. D'Ambrosio C.; Giorio G.; Marino I.; Merendino A.; Petrozza A.; Salfi L.; Stigliani A. L.; Cellini F. Virtually complete conversion of lycopene into β-carotene in fruits of tomato plants transformed with the tomato lycopene β-cyclase (tlcy-b) cDNA. Plant Sci. 166: 207–214; 2004.CrossRefGoogle Scholar
  26. Darnton-Hill I.; Nalubola R. Fortification strategies to meet micronutrient needs: successes and failures. Proc. Nutr. Soc. 61: 231–241; 2002.PubMedCrossRefGoogle Scholar
  27. Davuluri G. R.; Van Tuinen A.; Fraser P. D.; Manfredonia A.; Newman R.; Burgess D.; Brummell D. A.; King S. R.; Palys J.; Uhlig J.; Bramley P. M.; Pennings H. M. J.; Bowler C. Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat. Biotechnol. 23: 890–895; 2005.PubMedCrossRefGoogle Scholar
  28. de Pee S.; West C. E.; Permaesih D.; Martuti S.; Muhilal; Hautvast J. G. Orange fruit is more effective than are dark-green, leafy vegetables in increasing serum concentrations of retinol and beta-carotene in schoolchildren in Indonesia. Am. J. Clin. Nutr. 68: 1058–1067; 1998.PubMedGoogle Scholar
  29. Dharmapuri S.; Rosati C.; Pallara P.; Aquilani R.; Bouvier F.; Camara B.; Giuliano G. Metabolic engineering of xanthophyll content in tomato fruits. FEBS Lett. 519: 30–34; 2002.PubMedCrossRefGoogle Scholar
  30. Dickson M. H.; Lee C. Y.; Blamble A. E. Orange-curd high carotene cauliflower inbreds. HortScience 23: 778–779; 1988.Google Scholar
  31. Dietz J. M.; Sri K. S.; Erdman Jr. J. W. Reversed phase HPLC analysis of alpha- and beta-carotene from selected raw and cooked vegetables. Plant Foods Hum. Nutr. 38: 333–341; 1988.PubMedCrossRefGoogle Scholar
  32. Diretto G.; Al-Babili S.; Tavazza R.; Papacchioli V.; Beyer P.; Giuliano G. Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS ONE 2: e350; 2007a.PubMedCrossRefGoogle Scholar
  33. Diretto G.; Tavazza R.; Welsch R.; Pizzichini D.; Mourgues F.; Papacchioli V.; Beyer P.; Giuliano G. Metabolic engineering of potato tuber carotenoids through tuber-specific silencing of lycopene ε-cyclase. BMC Plant Biol. 6: 13; 2006.Google Scholar
  34. Diretto G.; Welsch R.; Tavazza R.; Mourgues F.; Pizzichini D.; Beyer P.; Giuliano G. Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers. BMC Plant Biol. 7: 11; 2007b.PubMedCrossRefGoogle Scholar
  35. Ducreux L. J. M.; Morris W. L.; Hedley P. E.; Shepherd T.; Davies H. V.; Millam S.; Taylor M. A. Metabolic engineering of high carotenoid potato tubers containing enhanced levels of β-carotene and lutein. J. Exp. Bot. 56: 81–89; 2005.PubMedGoogle Scholar
  36. Dwivedi S. L.; Crouch J. H.; Mackill D. J.; Xu Y.; Blair M. W.; Ragot M.; Upadhyaya H. D.; Ortiz R. The molecularization of public sector crop breeding: progress, problems, and prospects. Adv. Agron. 3: 163–319; 2007.CrossRefGoogle Scholar
  37. Enfissi E. M.; Fraser P. D.; Lois L. M.; Boronat A.; Schuch W.; Bramley P. M. 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: 17–27; 2005.PubMedCrossRefGoogle Scholar
  38. Englberger L.; Wills R. B.; Blades B.; Dufficy L.; Daniells J. W.; Coyne T. Carotenoid content and flesh color of selected banana cultivars growing in Australia. Food Nutr. Bull. 27: 281–291; 2006.PubMedGoogle Scholar
  39. Farre G.; Sanahuja G.; Naqvi S.; Bai C.; Capell T.; Zhu C.; Christou P. Travel advice on the road to carotenoids in plants. Plant Sci. 179: 28–48; 2010a.CrossRefGoogle Scholar
  40. Farre G.; Twyman R. M.; Zhu C.; Capell T.; Christou P. Nutritionally enhanced crops and food security: Scientific achievements versus political expediency. Curr. Opin. Biotechnol. 22: 1–7; 2010b.Google Scholar
  41. Feng H.; Li Y.; Liu Z.; Liu J. Mapping of or, a gene conferring orange color on the inner leaf of the Chinese cabbage (Brassica rapa L. ssp. pekinensis). Mol Breed; 2010. doi:10.1007/s11032-010-9542-x.Google Scholar
  42. Ferreira C. F.; Alves E.; Pestana K. N.; Junghans D. T.; Kobayashi A. K.; de Jesus Santos V.; Silva R. P.; Silva P. H.; Soares E.; Fukuda W. Molecular characterization of cassava (Manihot esculenta Crantz) with yellow-orange roots for beta-carotene improvement. Crop Breed Appl Biotechnol 8: 23–29; 2008.Google Scholar
  43. Fraser P. D.; Enfissi E. M. A.; Halket J. M.; Truesdale M. R.; Yu D.; Gerrish C.; Bramley P. M. Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19: 3194–3211; 2007.PubMedCrossRefGoogle Scholar
  44. Fraser P. D.; Romer S.; Shipton C. A.; Mills P. B.; Kiano J. W.; Misawa N.; Drake R. G.; Schuch W.; Bramley P. M. Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc. Natl Acad. Sci. U.S.A. 99: 1092–1097; 2002.PubMedCrossRefGoogle Scholar
  45. Fraser P. D.; Truesdale M. R.; Bird C. R.; Schuch W.; Bramley P. M. Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol. 105: 405–413; 1994.Google Scholar
  46. Fujisawa M.; Takita E.; Harada H.; Sakurai N.; Suzuki H.; Ohyama K.; Shibata D.; Misawa N. Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation. J. Exp. Bot. 60: 1319–1332; 2009.PubMedCrossRefGoogle Scholar
  47. Giliberto L.; Perrotta G.; Pallara P.; Weller J. L.; Fraser P. D.; Bramley P. M.; Fiore A.; Tavazza M.; Giuliano G. Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol. 137: 199–208; 2005.PubMedCrossRefGoogle Scholar
  48. Giorio G.; Stigliani A. L.; D'Ambrosio C. Agronomic performance and transcriptional analysis of carotenoid biosynthesis in fruits of transgenic HighCaro and control tomato lines under field conditions. Transgenic Res. 16: 15–28; 2007.PubMedCrossRefGoogle Scholar
  49. Goldman I. L.; Breitbach D. N. Inheritance of a recessive character controlling reduced carotenoid pigmentation in carrot (Daucus carota L.). J. Hered. 87: 380–382; 1996.Google Scholar
  50. Goodner K. L.; Rouseff R. L.; Hofsommer H. J. Orange, mandarin, and hybrid classification using multivariate statistics based on carotenoid profiles. J. Agric. Food Chem. 49: 1146–1150; 2001.PubMedCrossRefGoogle Scholar
  51. Grimme L. H.; Brown J. S. Functions of chlorophylls and carotenoids in thylakoid membranes. Adv Photosyn Res 2: 141–144; 1984.Google Scholar
  52. Gross J. Carotenoids: pigments in Fruits. Academic, London; 1987.Google Scholar
  53. Harjes C. E.; Rocheford T. R.; Bai L.; Brutnell T. P.; Kandianis C. B.; Sowinski S. G.; Stapleton A. E.; Vallabhaneni R.; Williams M.; Wurtzel E. T.; Yan J.; Buckler E. S. Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330–333; 2008.PubMedCrossRefGoogle Scholar
  54. Harrison E. H. Mechanisms of digestion and absorption of dietary vitamin A. Ann Rev Nutr 25: 87–103; 2005.CrossRefGoogle Scholar
  55. Hart D. J.; Scott K. J. Development and evaluation of an HPLC method for the analysis of carotenoids in foods, and the measurement of the carotenoid content of vegetables and fruits commonly consumed in the UK. Food Chem. 54: 101–111; 1995.CrossRefGoogle Scholar
  56. Haskell M. J.; Jamil K. M.; Hassan F.; Peerson J. M.; Hossain M. I.; Fuchs G. J.; Brown K. H. Daily consumption of Indian spinach (Basella alba) or sweet potatoes has a positive effect on total body vitamin A stores in Bangladeshi men. Am. J. Clin. Nutr. 80: 705–714; 2004.PubMedGoogle Scholar
  57. Howard L. A.; Wong A. D.; Perry A. K.; Klein B. P. β-carotene and ascorbic acid retention in fresh and processed vegetables. J. Food Sci. 64: 929–936; 1999.CrossRefGoogle Scholar
  58. Ikoma Y.; Komatsu A.; Kita M.; Ogawa K.; Omura M.; Yano M.; Moriguchi T. Expression of a phytoene synthase gene and characteristic carotenoid accumulation during citrus fruit development. Physiol. Plant. 111: 232–238; 2001.CrossRefGoogle Scholar
  59. Imam M. K.; Gabelman W. H. Inheritance of carotenoids in carrots, Daucus carota L. Proc Am Soc Hortic Sci 93: 419–428; 1968.Google Scholar
  60. IOM. Dietary reference intakes for vitamin a, vitamin k, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium and zinc. National Academy Press, Washington, DC; 2001.Google Scholar
  61. Isaacson T.; Ohad I.; Beyer P.; Hirschberg J. Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol. 136: 4246–4255; 2004.PubMedCrossRefGoogle Scholar
  62. Just B. J.; Santos C. A.; Yandell B. S.; Simon P. W. Major QTL for carrot color are positionally associated with carotenoid biosynthetic genes and interact epistatically in a domesticated x wild carrot cross. Theor. Appl. Genet. 119: 1155–1169; 2009.PubMedCrossRefGoogle Scholar
  63. Kato M.; Ikoma Y.; Matsumoto H.; Sugiura M.; Hyodo H.; Yano M. Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol. 134: 824–837; 2004.PubMedCrossRefGoogle Scholar
  64. Kean E. G.; Ejeta G.; Hamaker B. R.; Ferruzzi M. G. Characterization of carotenoid pigments in mature and developing kernels of selected yellow-endosperm sorghum varieties. J. Agric. Food Chem. 55: 2619–2626; 2007.PubMedCrossRefGoogle Scholar
  65. Khan N. C.; West C. E.; de Pee S.; Bosch D.; Phuong H. D.; Hulshof P. J.; Khoi H. H.; Verhoef H.; Hautvast J. G. The contribution of plant foods to the vitamin A supply of lactating women in Vietnam: a randomized controlled trial. Am. J. Clin. Nutr. 85: 1112–1120; 2007.PubMedGoogle Scholar
  66. Kim M.; Kim S. C.; Song K. J.; Kim H. B.; Kim I. J.; Song E. Y.; Chun S. J. Transformation of carotenoid biosynthetic genes using a micro-cross section method in kiwifruit (Actinidia deliciosa cv. Hayward). Plant Cell Rep. 29: 1339–1349; 2010.PubMedCrossRefGoogle Scholar
  67. Kurilich A. C.; Juvik J. A. Quantification of carotenoid and tocopherol antioxidants in Zea mays. J. Agric. Food Chem. 47: 1948–1955; 1999.PubMedCrossRefGoogle Scholar
  68. Lawrence R. J.; Pikaard C. S. Transgene-induced RNA interference: a strategy for overcoming gene redundancy in polyploids to generate loss-of-function mutations. Plant J. 36: 114–121; 2003.PubMedCrossRefGoogle Scholar
  69. Lee H. S.; Castle W. S. Seasonal changes of carotenoid pigments and color in Hamlin, Earlygold, and Budd Blood orange juices. J. Agric. Food Chem. 49: 877–882; 2001.PubMedCrossRefGoogle Scholar
  70. Li F.; Murillo C.; Wurtzel E. T. Maize Y9 encodes a product essential for 15-cis-zeta-carotene isomerization. Plant Physiol. 144: 1181–1189; 2007.PubMedCrossRefGoogle Scholar
  71. Li F.; Vallabhaneni R.; Yu J.; Rocheford T.; Wurtzel E. T. The maize phytoene synthase gene family: overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance. Plant Physiol. 146: 1334–1346; 2008.CrossRefGoogle Scholar
  72. Li L.; Garvin D. F. Molecular mapping of Or, a gene inducing β-carotene accumulation in cauliflower (Brassica oleracea L. var. botrytis). Genome 46: 588–594; 2003.PubMedCrossRefGoogle Scholar
  73. Li L.; Paolillo D. J.; Parthasarathy M. V.; Dimuzio E. M.; Garvin D. F. A novel gene mutation that confers abnormal patterns of beta-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J. 26: 59–67; 2001.PubMedCrossRefGoogle Scholar
  74. Li Q.; Farre G.; Naqvi S.; Breitenbach J.; Sanahuja G.; Bai C.; Sandmann G.; Capell T.; Christou P.; Zhu C. Cloning and functional characterization of the maize carotenoid isomerase and β-carotene hydroxylase genes and their regulation during endosperm maturation. Transgenic Res 19: 1053–1068; 2010a.PubMedCrossRefGoogle Scholar
  75. Li S.; Nugroho A.; Rocherford T.; White W. S. Vitamin A equivalence of the β-carotene in β-carotene-biofortified maize porridge consumed by women. Am. J. Clin. Nutr. 92: 1105–1112; 2010b.PubMedCrossRefGoogle Scholar
  76. Lopez A. B.; Van Eck J.; Conlin B. J.; Paolillo D. J.; O'Neill J.; Li L. Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J. Exp. Bot. 59: 213–223; 2008.PubMedCrossRefGoogle Scholar
  77. Lu S.; Li L. Carotenoid metabolism: biosynthesis, regulation, and beyond. J. Integr. Plant Biol. 50: 778–785; 2008.PubMedCrossRefGoogle Scholar
  78. Lu S.; Van Eck J.; Zhou X.; Lopez A. B.; O'Halloran D. M.; Cosman K. M.; Conlin B. J.; Paolillo D. J.; Garvin D. F.; Vrebalov J.; Kochian L. V.; Kupper H.; Earle E. D.; Cao J.; Li L. The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell 18: 3594–3605; 2006.PubMedCrossRefGoogle Scholar
  79. Maes T.; De Keukelerie P.; Gerats T. Plant tagnology. Trends Plant Sci. 4: 90–96; 1999.PubMedCrossRefGoogle Scholar
  80. Maass D.; Arango J.; Wust F.; Beyer P.; Welsch R. Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS ONE 4: e6373; 2009.PubMedCrossRefGoogle Scholar
  81. Mansoor S.; Amin I.; Hussain M.; Zafar Y.; Briddon R. W. Engineering novel traits in plants through RNA interference. Trends Plant Sci. 11: 559–565; 2006.PubMedCrossRefGoogle Scholar
  82. Misawa N.; Truesdale M. R.; Sandmann G.; Fraser P. D.; Bird C.; Schuch W.; Bramley P. M. Expression of a tomato cDNA coding for phytoene synthase in Escherichia coli, phytoene formation in vivo and in vitro, and functional analysis of the various truncated gene products. J. Biochem. 116: 980–985; 1994.PubMedGoogle Scholar
  83. Molnar P.; Szabolcs J. β-Citraurin epoxide, a new carotenoid from valencia orange peel. Phytochemistry 19: 633–637; 1980.CrossRefGoogle Scholar
  84. Murkovic M.; Mulleder U.; Neunteufl H. Carotenoid content in different varieties of pumpkins. J Food Compos Anal 15: 633–638; 2002.CrossRefGoogle Scholar
  85. Naqvi S.; Farre G.; Sanahuja G.; Capell T.; Zhu C.; Christou P. When more is better: multigene engineering in plants. Trends Plant Sci. 15: 48–56; 2010.Google Scholar
  86. Naqvi S.; Zhu C.; Farre G.; Ramessar K.; Bassie L.; Breitenbach J.; Perez C. D.; Ros G.; Sandmann G.; Capell T.; Christou P. Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc. Natl Acad. Sci. U.S.A. 106: 7762–7767; 2009.PubMedCrossRefGoogle Scholar
  87. Nassar N. M. A.; Fernandes P. C.; Melani R. D.; Pires Jr. O. R. Amarelinha do Amapa: a carotenoid-rich cassava cultivar. Genet. Mol. Res. 8: 1051–1055; 2009.PubMedCrossRefGoogle Scholar
  88. Navazio J. P. Utilization of high carotene cucumber germplasm for genetic improvement of nutritional quality. PhD thesis. University of Wisconsin- Madison; 1994.Google Scholar
  89. Nesi N.; Delourme R.; Bregeon M.; Falentin C.; Renard M. Genetic and molecular approaches to improve nutritional value of Brassica napus L. seed. C R Biol 331: 763–771; 2008.PubMedCrossRefGoogle Scholar
  90. Olson J. A. Needs and sources of carotenoids and vitamin A. Nutr. Rev. 52: S67–73; 1994.PubMedCrossRefGoogle Scholar
  91. Paolillo D. J.; Garvin Jr. D. F.; Parthasarathy M. V. The chromoplasts of Or mutants of cauliflower (Brassica oleracea L. var. botrytis). Protoplasma 224: 245–253; 2004.PubMedCrossRefGoogle Scholar
  92. Parinov S.; Sundaresan V. Functional genomics in Arabidopsis: large-scale insertional mutagenesis complements the genome sequencing project. Curr. Opin. Biotechnol. 11: 157–161; 2000.PubMedCrossRefGoogle Scholar
  93. Potrykus I. Lessons from the ‘Humanitarian Golden Rice’ project: regulation prevents development of public good genetically engineered crop products. New Biotechnol. 27: 466–472; 2010.CrossRefGoogle Scholar
  94. Pozniak C. J.; Knox R. E.; Clarke F. R.; Clarke J. M. Identification of QTL and association of a phytoene synthase gene with endosperm colour in durum wheat. Theor. Appl. Genet. 114: 525–537; 2007.PubMedCrossRefGoogle Scholar
  95. Ravanello M. P.; Ke D.; Alvarez J.; Huang B.; Shewmaker C. K. Coordinate expression of multiple bacterial carotenoid genes in canola leading to altered carotenoid production. Metab. Eng. 5: 255–263; 2003.PubMedCrossRefGoogle Scholar
  96. Rodriguez-Concepcion M. Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem. Rev. 5: 1–15; 2006.CrossRefGoogle Scholar
  97. Rodríguez-Concepción M. Supply of precursors for carotenoid biosynthesis in plants. Arch. Biochem. Biophys. 504: 118–122; 2010.PubMedGoogle Scholar
  98. Rodriguez-Concepcion M.; Boronat A. Elucidation of the methylerthritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130: 1079–1089; 2002.PubMedCrossRefGoogle Scholar
  99. Romer S.; Fraser P. D.; Kiano J. W.; Shipton C. A.; Misawa N.; Schuch W.; Bramley P. M. Elevation of the provitamin A content of transgenic tomato plants. Nat. Biotechnol. 18: 666–669; 2000.PubMedCrossRefGoogle Scholar
  100. Romer S.; Lubeck J.; Kauder F.; Steiger S.; Adomat C.; Sandmann G. Genetic engineering of a zeaxanthin-rich potato by antisense inactivation and co-suppression of carotenoid epoxidation. Metab. Eng. 4: 263–272; 2002.PubMedCrossRefGoogle Scholar
  101. Rosati C.; Aquilani R.; Dharmapuri S.; Pallara P.; Marusic C.; Tavazza R.; Bouvier F.; Camara B.; Giuliano G. Metabolic engineering of β-carotene and lycopene content in tomato fruit. Plant J. 24: 413–419; 2000.PubMedCrossRefGoogle Scholar
  102. Salas Fernandez M. G.; Hamblin M. T.; Li L.; Rooney W. L.; Tuinstra M. R.; Kresovich S. Quantitative trait loci analysis of endosperm color and carotenoid content in sorghum grain. Crop Sci. 48: 1732–1743; 2008.CrossRefGoogle Scholar
  103. Santos C. A.; Senalik D.; Simon P. W. Path analysis suggests phytoene accumulation is the key step limiting the carotenoid pathway in white carrot roots. Genet Mol Biol 28: 287–293; 2005.Google Scholar
  104. Santos C. A.; Simon P. W. QTL analyses reveal clustered loci for accumulation of major provitmain A carotenes and lycopene in carrot roots. Mol. Genet. Genomics 268: 122–129; 2002.PubMedCrossRefGoogle Scholar
  105. Seo M.; Koshiba T. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 7: 41–48; 2002.PubMedCrossRefGoogle Scholar
  106. Shewmaker C. K.; Sheehy J. A.; Daley M.; Colburn S.; Ke D. Y. Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J. 20: 401–412; 1999.PubMedCrossRefGoogle Scholar
  107. Simkin A. J.; Gaffe J.; Alcaraz J. P.; Carde J. P.; Bramley P. M.; Fraser P. D.; Kuntz M. Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Photochemestry 68: 1545–1556; 2007.CrossRefGoogle Scholar
  108. Singh M.; Lewis P. E.; Hardeman K.; Bai L.; Rose J. K. C.; Mazourek M.; Chomet P.; Brutnell T. P. Activator mutagenesis of the pink scutellum1/viviparous7 locus of maize. Plant Cell 15: 874–884; 2003.PubMedCrossRefGoogle Scholar
  109. Slade A. J.; Knauf V. C. TILLING moves beyond functional genomics into crop improvement. Transgenic Res. 14: 109–115; 2005.PubMedCrossRefGoogle Scholar
  110. Tang G.; Gu X.; Hu S.; Xu Q.; Qin J.; Dolnikowski G. G.; Fjeld C. R.; Gao X.; Russell R. M.; Yin S. Green and yellow vegetables can maintain body stores of vitamin A in Chinese children. Am. J. Clin. Nutr. 70: 1069–1076; 1999.PubMedGoogle Scholar
  111. Tang G.; Qin J.; Dolnikowski G. G.; Russell R. M.; Grusak M. A. Spinach or carrot can supply significant amounts of vitamin A as assessed by feeding with intrinsically deuterium-labeled vegetables. Am. J. Clin. Nutr. 82: 821–828; 2005.Google Scholar
  112. Tang G.; Qin J.; Dolinowski G. G.; Russell R. M.; Grusak M. A. Golden Rice is an effective source of vitamin A. Am. J. Clin. Nutr. 89: 1776–1783; 2009.PubMedCrossRefGoogle Scholar
  113. Tanumihardjo S. A. Factors influencing the conversion of carotenoids to retinol: bioavailability to bioconversion to bioefficacy. Int. J. Vitam. Nutr. Res. 72: 40–45; 2002.PubMedCrossRefGoogle Scholar
  114. Tian L.; Magallanes-Lundback M.; Musetti V.; DellaPenna D. Functional analysis of beta- and epsilon-ring carotenoid hydroxylases in Arabidopsis. Plant Cell 5: 1320–1332; 2003.CrossRefGoogle Scholar
  115. Thorup T. A.; Tanyolac B.; Livingstone K. D.; Popovsky S.; Paran I.; Jahn M. Candidate gene analysis of organ pigmentation loci in the Solanaceae. Proc. Natl Acad. Sci. U.S.A. 97: 11192–11197; 2000.PubMedCrossRefGoogle Scholar
  116. UNICEF. Vitamin A deficiency. UNICEF; 2006. http://www.childinfo.org/areas/vitamina/
  117. Underwood B. A. Scientific research: essential, but is it enough to combat world food insecurities? J. Nutr. 133: 1434S–1437S; 2003.PubMedGoogle Scholar
  118. Vallabhaneni R.; Gallagher C. E.; Licciardello N.; Cuttriss A. J.; Quinlan R. F.; Wurtzel E. T. Metabolite sorting of a germplasm collection reveals the Hydroxylase3 locus as a new target for maize provitamin A biofortification. Plant Physiol. 150: 1635–1645; 2009.CrossRefGoogle Scholar
  119. Vallabhaneni R.; Wurtzel E. T. Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize. Plant Physiol. 150: 562–572; 2009.PubMedCrossRefGoogle Scholar
  120. Van Eck J.; Conlin B.; Garvin D. F.; Mason H.; Navarre D. A.; Brown C. R. Enhancing beta-carotene content in potato by RNAi-mediated silencing of the beta-carotene hydroxylase gene. Am. J. Potato Res. 84: 331–342; 2007.CrossRefGoogle Scholar
  121. Vasquez-Caicedo A. L.; Sruamsiri P.; Carle R.; Neidhart S. Accumulation of all-trans-beta-carotene and its 9-cis and 13-cis stereoisomers during postharvest ripening of nine Thai mango ciltivars. J. Agric. Food Chem. 53: 4827–4835; 2005.PubMedCrossRefGoogle Scholar
  122. Wang Y.; Wang F.; Zhai H.; Liu Q. Production of a useful mutant by chronic irradiation in sweetpotato. Sci. Hortic. 111: 173–178; 2007.CrossRefGoogle Scholar
  123. Wei S.; Yu B.; Gruber M. Y.; Khachatourians G. G.; Hegedus D. D.; Hannoufa A. Enhanced seed carotenoid levels and branching in transgenic Brassica napus expressing the Arabidopsis miR156b Gene. J. Agric. Food Chem. 58: 9572–9578; 2010.PubMedCrossRefGoogle Scholar
  124. Welsch R.; Arango J.; Bar C.; Salazar B.; Al-Babili S.; Beltran J.; Chavarriaga P.; Ceballos H.; Tohme J.; Beyer P. Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. Plant Cell 22: 3348–3356; 2010.PubMedCrossRefGoogle Scholar
  125. Wong J. C.; Lambert R. J.; Wurtzel E. T.; Rocheford T. R. QTL and candidate genes phytoene synthase and zeta-carotene desaturase associated with the accumulation of carotenoids in maize. Theor. Appl. Genet. 108: 349–359; 2004.PubMedCrossRefGoogle Scholar
  126. Wurbs D.; Ruf S.; Bock R. Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J. 49: 276–288; 2007.PubMedCrossRefGoogle Scholar
  127. Wurtzel E. T.; Luo R.; Yatou O. A simple approach to identify the first rice mutants blocked in carotenoid biosynthesis. J. Exp. Bot. 52: 161–166; 2001.PubMedCrossRefGoogle Scholar
  128. Yan J.; Kandianis C. B.; Harjes C. E.; Bai L.; Kim E. H.; Yang X.; Skinner D. J.; Fu Z.; Mitchell S.; Li Q.; Fernandez M. G.; Zaharieva M.; Babu R.; Fu Y.; Palacios N.; Li J.; Dellapenna D.; Brutnell T.; Buckler E. S.; Warburton M. L.; Rocheford T. Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat. Genet. 42: 322–327; 2010.PubMedCrossRefGoogle Scholar
  129. Yu B.; Lydiate D. J.; Young L. W.; Schafer U. A.; Hannoufa A. Enhancing the carotenoid content of Brassica napus seeds by downregulating lycopene epsilon cyclase. Transgenic Res. 17: 573–585; 2007.PubMedCrossRefGoogle Scholar
  130. Zamir D. Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2: 983–989; 2001.PubMedCrossRefGoogle Scholar
  131. Zhang J.; Tao N.; Xu Q.; Zhou W.; Cao H.; Xu J.; Deng X. Functional characterization of Citrus PSY gene in Hongkong kumquat (Fortunella hindsii Swingle). Plant Cell Rep. 28: 1737–1746; 2009.PubMedCrossRefGoogle Scholar
  132. Zhu C.; Bai C.; Sanahuja G.; Yuan D.; Farre G.; Naqvi S.; Shi L.; Capell T.; Christou P. The regulation of carotenoid pigmentation in flowers. Arch. Biochem. Biophys. 504: 132–141; 2010.PubMedGoogle Scholar
  133. Zhu C.; Naqvi S.; Breitenbach J.; Sandmann G.; Christou P.; Capell T. Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc. Natl Acad. Sci. U.S.A. 105: 18232–18237; 2008.PubMedCrossRefGoogle Scholar
  134. Zhu C.; Naqvi S.; Gomez-Galera S.; Pelacho A. M.; Capell T.; Christou P. Transgenic strategies for the nutritional enhancement of plants. Trends Plant Sci. 12: 548–555; 2007.PubMedCrossRefGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2011

Authors and Affiliations

  • Chao Bai
    • 1
  • Richard M. Twyman
    • 2
  • Gemma Farré
    • 1
  • Georgina Sanahuja
    • 1
  • Paul Christou
    • 1
    • 3
  • Teresa Capell
    • 1
  • Changfu Zhu
    • 1
  1. 1.Department of Plant Production and Forestry Science, ETSEAUniversity of LleidaLleidaSpain
  2. 2.Department of Biological SciencesUniversity of WarwickWarwickUK
  3. 3.Institució Catalana de Reserca i Estudis AvançatsBarcelonaSpain

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