Skip to main content

Advertisement

Log in

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

  • Invited Review
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.

Similar content being viewed by others

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Anderson J. M.; Waldron J. C.; Thorne S. W. Chlorophyll-protein complexes of spinach and barley thylakoids. FEBS Lett. 92: 227–233; 1978.

    Article  CAS  Google Scholar 

  • Apel W.; Bock R. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol. 151: 59–66; 2009.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Beyer P. Golden Rice and ‘Golden’ crops for human nutrition. New Biotechnol. 27: 478–481; 2010.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Capell T.; Christou P. Progress in plant metabolic engineering. Curr. Opin. Biotechnol. 15: 148–154; 2004.

    Article  PubMed  CAS  Google Scholar 

  • Cazzonelli C. I.; Pogson B. J. Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 15: 266–274; 2010.

    Article  PubMed  CAS  Google Scholar 

  • Cervantes-Flores J. C. Development of a genetic linkage map and QTL analysis in sweet potato. Mol. Breed. 21: 511–532; 2006.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Chappell J. Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Ann Rev Plant Physiol Plant Mol Biol 46: 521–547; 1995.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Comai L.; Henikoff S. TILLING: practical single-nucleotide mutation discovery. Plant J. 45: 684–694; 2006.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Darnton-Hill I.; Nalubola R. Fortification strategies to meet micronutrient needs: successes and failures. Proc. Nutr. Soc. 61: 231–241; 2002.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Dickson M. H.; Lee C. Y.; Blamble A. E. Orange-curd high carotene cauliflower inbreds. HortScience 23: 778–779; 1988.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Grimme L. H.; Brown J. S. Functions of chlorophylls and carotenoids in thylakoid membranes. Adv Photosyn Res 2: 141–144; 1984.

    Google Scholar 

  • Gross J. Carotenoids: pigments in Fruits. Academic, London; 1987.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Harrison E. H. Mechanisms of digestion and absorption of dietary vitamin A. Ann Rev Nutr 25: 87–103; 2005.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kurilich A. C.; Juvik J. A. Quantification of carotenoid and tocopherol antioxidants in Zea mays. J. Agric. Food Chem. 47: 1948–1955; 1999.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lu S.; Li L. Carotenoid metabolism: biosynthesis, regulation, and beyond. J. Integr. Plant Biol. 50: 778–785; 2008.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Maes T.; De Keukelerie P.; Gerats T. Plant tagnology. Trends Plant Sci. 4: 90–96; 1999.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Molnar P.; Szabolcs J. β-Citraurin epoxide, a new carotenoid from valencia orange peel. Phytochemistry 19: 633–637; 1980.

    Article  CAS  Google Scholar 

  • Murkovic M.; Mulleder U.; Neunteufl H. Carotenoid content in different varieties of pumpkins. J Food Compos Anal 15: 633–638; 2002.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Navazio J. P. Utilization of high carotene cucumber germplasm for genetic improvement of nutritional quality. PhD thesis. University of Wisconsin- Madison; 1994.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Olson J. A. Needs and sources of carotenoids and vitamin A. Nutr. Rev. 52: S67–73; 1994.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Parinov S.; Sundaresan V. Functional genomics in Arabidopsis: large-scale insertional mutagenesis complements the genome sequencing project. Curr. Opin. Biotechnol. 11: 157–161; 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Rodríguez-Concepción M. Supply of precursors for carotenoid biosynthesis in plants. Arch. Biochem. Biophys. 504: 118–122; 2010.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Seo M.; Koshiba T. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 7: 41–48; 2002.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Slade A. J.; Knauf V. C. TILLING moves beyond functional genomics into crop improvement. Transgenic Res. 14: 109–115; 2005.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • UNICEF. Vitamin A deficiency. UNICEF; 2006. http://www.childinfo.org/areas/vitamina/

  • Underwood B. A. Scientific research: essential, but is it enough to combat world food insecurities? J. Nutr. 133: 1434S–1437S; 2003.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Vallabhaneni R.; Wurtzel E. T. Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize. Plant Physiol. 150: 562–572; 2009.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Wang Y.; Wang F.; Zhai H.; Liu Q. Production of a useful mutant by chronic irradiation in sweetpotato. Sci. Hortic. 111: 173–178; 2007.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Zamir D. Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2: 983–989; 2001.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Research in our laboratory is supported by the Ministry of Science and Innovation (MICINN) Grant BFU2007-61413; European Research Council Advanced Grant BIOFORCE; Center Consolider, MICINN, Spain; COST Action FA0804, Associated Unit CAVA; and the SmartCell, FP7 Integrated Project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Changfu Zhu.

Additional information

Editor: N. J. Taylor

Chao Bai and Richard M. Twyman contributed equally to this paper

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bai, C., Twyman, R.M., Farré, G. et al. A golden era—pro-vitamin A enhancement in diverse crops. In Vitro Cell.Dev.Biol.-Plant 47, 205–221 (2011). https://doi.org/10.1007/s11627-011-9363-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11627-011-9363-6

Keywords

Navigation