Transgenic Research

, Volume 16, Issue 5, pp 581–585 | Cite as

Metabolic engineering of carotenoid accumulation by creating a metabolic sink

Perspective

Abstract

Carotenoids are highly beneficial for human nutrition and health because they provide essential nutrients and important antioxidants in our diets. However, many food crops, especially the major staple crops contain only trace to low amounts of carotenoids. Although significant progress has been made in developing food crops rich in carotenoids by altering the expression of carotenoid biosynthetic genes, in many cases it has proved to be difficult to reach the desired levels of carotenoid enrichment. The recent identification and characterization of a novel gene mutation in cauliflower reveals that creating a metabolic sink to sequester carotenoids is an important mechanism to control carotenoid accumulation in plants. The successful demonstration of increased carotenoid accumulation in association with the formation of sink structures in transgenic crops offers a new and alternative approach to increase carotenoid content. Manipulation of the formation of metabolic sink along with the catalytic activity of the pathway may represent a promising strategy for maximally improving the nutritional quality of food crops.

Keywords

Carotenoids Metabolic sink Carotenoid sequestering structures Chromoplasts Cauliflower Or gene 

Notes

Acknowledgements

We thank X. Zhou for the photograph. We are grateful to many colleagues for their contribution to this work. This research was supported by USDA National Research Initiative Grants, ARS Headquarter Postdoctoral Research Associated Fund, the Triad Foundation, and Helen Graham Charitable Foundation.

References

  1. Al Babili S, Hartung W, Kleinig H, Beyer P (1999) CPTA modulates levels of carotenogenic proteins and their mRNAs and affects carotenoid and ABA content as well as chromoplast structure in Narcissus pseudonarcissus flowers. Plant Biol 1:607–612Google Scholar
  2. Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7:1027–1038PubMedCrossRefGoogle Scholar
  3. Beyer P, Al Babili S, Ye X, Lucca P, Schaub P, Welsch R, Potrykus I (2002) Golden Rice: Introducing the beta-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J Nutr 132:506S–510SPubMedGoogle Scholar
  4. Botella-Pavia P, Rodriguez-Concepcion M (2006) Carotenoid biotechnology in plants for nutritionally improved foods. Physiol Plant 126:369–381CrossRefGoogle Scholar
  5. Brown CR, Culley D, Yang CP, Durst R, Wrolstad R (2005) Variation of anthocyanin and carotenoid contents and associated antioxidant values in potato breeding lines. J Am Soc Hortic Sci 130:174–180Google Scholar
  6. Camara B, Hugueney P, Bouvier F, Kuntz M, Moneger R (1995) Biochemistry and molecular biology of chromoplast development. Int Rev Cytol 163:175–247PubMedCrossRefGoogle Scholar
  7. Cookson PJ, Kiano JW, Shipton CA, Fraser PD, Romer S, Schuch W, Bramley P, Pyke KA (2003) Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta 217:896–903PubMedCrossRefGoogle Scholar
  8. Deruere J, Romer S, d’Harlingue A, Backhaus RA, Kuntz M, Camara B (1994) Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6:119–133PubMedCrossRefGoogle Scholar
  9. 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:e350PubMedCrossRefGoogle Scholar
  10. Diretto G, Tavazza R, Welsch R, Pizzichini D, Mourgues F, Papacchioli V, Beyer P, Giuliano G (2006) Metabolic engineering of potato tuber carotenoids through tuber-specific silencing of lycopene epsilon cyclase. BMC Plant Biol 6:13PubMedCrossRefGoogle Scholar
  11. Ducreux LJ, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein. J Exp Bot 56:81–89PubMedGoogle Scholar
  12. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265PubMedCrossRefGoogle Scholar
  13. Fraser PD, Romer S, Shipton CA, Mills PB, Kiano JW, Misawa N, Drake RG, Schuch W, Bramley PM (2002) Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci USA 99:1092–1097PubMedCrossRefGoogle Scholar
  14. Gerjets T, Sandmann G (2006) Ketocarotenoid formation in transgenic potato. J Exp Bot 57:3639–3645PubMedCrossRefGoogle Scholar
  15. Giovannucci E (1999) Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J Natl Cancer Inst 91:317–331PubMedCrossRefGoogle Scholar
  16. Hadley CW, Miller EC, Schwartz SJ, Clinton SK (2002) Tomatoes, lycopene, and prostate cancer: progress and promise. Exp Biol Med 227:869–880Google Scholar
  17. Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29:435–445PubMedCrossRefGoogle Scholar
  18. Krinsky NI, Landrum JT, Bone RA (2003) Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr 23:171–201PubMedCrossRefGoogle Scholar
  19. 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 26:59–67PubMedCrossRefGoogle Scholar
  20. Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902PubMedCrossRefGoogle Scholar
  21. Lu S, Eck Van J, Zhou X, Lopez AB, O’Halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J, Kochian LV, Kupper H, Earle ED, Cao J, Li L (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of beta-carotene accumulation. Plant Cell 18:3594–3605PubMedCrossRefGoogle Scholar
  22. Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487PubMedCrossRefGoogle Scholar
  23. Rabbani S, Beyer P, Lintig J, Hugueney P, Kleinig H (1998) Induced beta-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116:1239–1248PubMedCrossRefGoogle Scholar
  24. Romer S, Fraser PD, Kiano JW, Shipton CA, Misawa N, Schuch W, Bramley PM (2000) Elevation of the provitamin A content of transgenic tomato plants. Nat Biotechnol 18:666–669PubMedCrossRefGoogle Scholar
  25. Sandmann G, Romer S, Fraser PD (2006) Understanding carotenoid metabolism as a necessity for genetic engineering of crop plants. Metab Eng 8:291–302PubMedCrossRefGoogle Scholar
  26. Schaub P, Al-Babili S, Drake R, Beyer P (2005) Why is golden rice golden (yellow) instead of red? Plant Physiol 138:441–450PubMedCrossRefGoogle Scholar
  27. 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 20:401–412XPubMedCrossRefGoogle Scholar
  28. Taylor M, Ramsay G (2005) Carotenoid biosynthesis in plant storage organs: recent advances and prospects for improving plant food quality. Physiol Plant 124:143–151CrossRefGoogle Scholar
  29. Vishnevetsky M, Ovadis M, Vainstein A (1999) Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4:232–235PubMedCrossRefGoogle Scholar
  30. Vishnevetsky M, Ovadis M, Itzhaki H, Levy M, Libal WY, Adam Z, Vainstein A (1996) Molecular cloning of a carotenoid-associated protein from Cucumis sativus corollas: homologous genes involved in carotenoid sequestration in chromoplasts. Plant J 10:1111–1118PubMedCrossRefGoogle Scholar
  31. Wurtzel ET (2004) Genomics, genetics, and biochemistry of maize carotneoid biosynthesis. In: Romeo J (ed) Recent Advances in Phytochemistry, vol 38. Elsevier Ltd., pp 85–110Google Scholar
  32. Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.USDA-ARS, Plant, Soil and Nutrition LaboratoryCornell UniversityIthacaUSA
  2. 2.Boyce Thompson Institute for Plant ResearchCornell UniversityIthacaUSA

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