Abstract
Carotenoids are a class of fat-soluble antioxidant vitamin compounds present in maize (Zea mays L.) that may provide health benefits to animals or humans. Four carotenoid compounds are predominant in maize grain: β-carotene, β-cryptoxanthin, zeaxanthin, and lutein. Although β-carotene has the highest pro-vitamin A activity, it is present in a relatively low concentration in maize kernels. We set out to identify quantitative trait loci (QTL) affecting carotenoid accumulation in maize kernels. Two sets of segregating families were evaluated—a set of F2:3 lines derived from a cross of W64a x A632, and their testcross progeny with AE335. Molecular markers were evaluated on the F2:3 lines and a genetic linkage map created. High-performance liquid chromatography was performed to measure β-carotene, β-cryptoxanthin, zeaxanthin, and lutein on both sets of materials. Composite interval mapping identified chromosome regions with QTL for one or more individual carotenoids in the per se and testcross progenies. Notably QTL in the per se population map to regions with candidate genes, yellow 1 and viviparous 9, which may be responsible for quantitative variation in carotenoids. The yellow 1 gene maps to chromosome six and is associated with phytoene synthase, the enzyme catalyzing the first dedicated step in the carotenoid biosynthetic pathway. The viviparous 9 gene maps to chromosome seven and is associated with ζ-carotene desaturase, an enzyme catalyzing an early step in the carotenoid biosynthetic pathway. If the QTL identified in this study are confirmed, particularly those associated with candidates genes, they could be used in an efficient marker-assisted selection program to facilitate increasing levels of carotenoids in maize grain.
Similar content being viewed by others
References
Blessin CW, Brecher JD, Dimler RJ (1963a) Carotenoids of corn and sorghum V. Distribution of xanthophylls and carotenes in hand-dissected and dry-milled fractions of Yellow Dent Corn. Cereal Chem 40:582–586
Blessin CW, Brecher JD, Dimler RJ, Grogan CO, Campbell CM (1963b) Carotenoids of corn and sorghum III. Variation in xanthophylls and carotenes in hybrid, inbred, and exotic corn lines. Cereal Chem 40:436–442
Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB 9:1551–1558
Brunson AM, Quackenbush FW (1962) Breeding corn with high provitamin A in the grain. Crop Sci 2:344–347
Buckner B, Kelson TL, Robertson DS (1990) Cloning of the y1 locus of maize, a gene involved in the biosynthesis of carotenoids. Plant Cell 2:867–876
Buckner B, Miguel PS, Janik-Buckner D, Bennetzen JL (1996) The y1 gene of maize codes for phytoene synthase. Genetics 143:479–488
Cunningham FX, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) 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
Darnoko D, Cheryan M, Moros E, Jerrel J, Perkins EG (2000) Simultaneous HPLC analysis of palm carotenoids and tocopherols using a C-30 column and photodiode array detector. J Liq Chromatogr Relat Technol 23:1873–1885
Dudley JW (1993) Molecular markers in plant improvement—manipulation of genes affecting quantitative traits. Crop Sci 33:660–668
Faris JD, Li WL, Liu DJ, Chen PD, Gill BS (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor Appl Genet 98:219–225
Federer WT, Wolfinger RD (1998) SAS code for recovering intereffect information in experiments with incomplete block and lattice rectangle designs. Agron J 90:545–551
Food and Nutrition Board and Institute of Medicine (2000) Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids: a report of the Panel on Dietary Antioxidants and Related Compounds, Subcommittees on Upper Reference Levels of Nutrients and of Interpretation and Use of Dietary Reference Intakes, and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. Food and Nutrition Board and Institute of Medicine, Washington, D.C.
Hable WE, Oishi KK, Schumaker KS (1998) Viviparous-5 encodes phytoene desaturase, an enzyme essential for abscisic acid (aba) accumulation and seed development in maize. Mol Gen Genet 257:167–176
Hadden WL, Watkins RH, Levy LW, Regalado E, Rivadeneira DM, van Breemen RB, Schwartz SJ (1999) Carotenoid composition of marigold (Tagetes erecta) flower extract used as nutritional supplement. J Agric Food Chem 47:4189–4194
Hart DJ, Scott KJ (1995) Development of an HPLC method for the analysis of carotenoids in foods, and the measurement of carotenoid content of vegetables and fruits commonly consumed in the UK. Food Chem 54:101–111
Kurilich AC, Juvik JA (1999) Simultaneous quantification of carotenoids and tocopherols in corn kernel extracts by HPLC. J Liq Chromatogr Relat Technol 22:2925–2934
Li ZH, Matthews PD, Burr B, Wurtzel ET (1996) Cloning and characterization of a maize cDNA encoding phytoene desaturase, an enzyme of the carotenoid biosynthetic pathway. Plant Mol Biol 30:269–279
Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996a) Best linear unbiased prediction, SAS system for mixed models. SAS Institute, Cary N.C., pp 229–252
Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996b) Random effects models, SAS system for mixed models. SAS Institute, Cary N.C., pp 135–169
Luo R, Wurtzel ET (1999) A maize cDNA encoding zeta carotene resaturase, Plant Physiol 120:1206
Maize database (2002) MaizeDB. In: Missouri Maize Project http://www.agron.missouri.edu
Matthews PD, Luo R, Wurtzel ET (2003) Maize phytoene desaturase and zetacarotene desaturase catalyze a poly-Z desaturation pathway: implications for genetic engineering of carotenoid content among cereal crops. J Exp Bot 54:1–16
McMullen MD, Byrne PF, Snook ME, Wiseman BR, Lee EA, Widstrom NW, Coe EH (1998) Quantitative trait loci and metabolic pathways. Proc Natl Acad Sci USA 95:1996–2000
Mikkilineni V (1997) Restriction fragment length polymorphism analysis of the Illinois long-term selection chemical strains. Crop Sciences, University of Illinois, Urbana, p 113
National Institute of Standards and Technology (1994) The fat-soluble vitamin and carotenoid analysis tutorial. National Institute of Standards and Technology, Washington, D.C.
Ooijen JWV, Voorrips RE (2001) joinmap version 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Perez-Vendrell AM, Hernandez JM, Llaurado L, Schierle J, Brufau J (2001) Influence of source and ratio of xanthophyll pigments on broiler chicken pigmentation and performance. Poult Sci 80:320–326
Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291
Prioul JL, Pelleschi S, Sene M, Thevenot C, Causse M, de Vienne D, Leonardi A (1999) From QTLs for enzyme activity to candidate genes in maize. J Exp Bot 50:1281–1288
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doeblay J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Ruiz JA, Perez-Vendrell AM, Esteve-Garcia E (1999) Effect of beta-carotene and vitamin E on oxidative stability in leg meat of broilers fed different supplemental fats. J Agric Food Chem 47:448–454
Sander LC, Sharpless KE, Pursch M (2000) C-30 stationary phases for the analysis of food by liquid chromatography. J Chromatogr A 880:189–202
Sandmann G (1991) Biosynthesis of cyclic carotenoids: biochemistry and molecular genetics of the reaction sequence. Physiol Plant 83:186–193
SAS Institute (1996) SAS Software, Cary, N.C.
Senior ML, Chin ECL, Lee M, Smith JSC, Stuber CW (1996) Simple sequence repeat markers developed from maize sequences found in the GENBANK database: map construction. Crop Sci 36:1676–1683
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Thorup TA, Tanyolac B, Livingstone KD, Popovsky S, Paran I, Jahn M (2000) Candidate gene analysis of organ pigmentation loci in the Solanaceae. Proc Natl Acad Sci USA 97:11192–11197
Utz HF, Melchinger AE (1996) plabqtl: a program for composite interval mapping of QTL. J Quant Trait Loci 2:http://www.uni-hohenheim.de/~ipspwww/soft.html
Van den Berg H, Faulks R, Granado HF, Hirschberg J, Olmedilla B, Sandmann G, Southon S, Stahl W (2000) The potential for the improvement of carotenoid levels in foods and the likely systemic effects. J Sci Food Agric 80:880–912
Watson SA (1962) The yellow carotenoid pigments of corn. In: Heckendorn W, Sutherland JI (eds) 17th Hybrid Corn Industry Res Conf. American Seed Trade Association, Chicago, Ill., pp 92–100
Weber EJ (1987a) Carotenoids and tocols of corn grain determined by HPLC. J Am Oil Chem Soc 64:1129–1134
Weber EJ (1987b) Lipids of the kernel. In: Watson SA, Ramstad PE (eds) Corn: chemistry and technology. American Association of Cereal Chemists, St. Paul, Minn., pp 311–349
Wong JC, Lambert RJ, Tadmor Y, Rocheford TR (2003) QTL associated with accumulation of tocopherols in per se and testcross progenies of maize. Crop Sci (in press)
Acknowledgements
This research was supported by a grant from the Bi-National Agricultural Research and Development Fund (BARD), and also supported by a University of Illinois Research Board Grant and the Agricultural Experiment Station. JCW was supported by the BARD grant, and by Pioneer Hi-Bred, Troyer/Darwin, and William and Nancy Ambrose Fellowships. We would also like to thank the following people for their support and assistance: Craig Anderson, Jerry Chandler, Janet Jackson, Jeremy Johnson, Venugopal Mikkilineni, Chandra Paul, Don Roberts, Jennifer Schultz, and Shane Zimmerman. We thank Martin Bohn for critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. Langridge
Rights and permissions
About this article
Cite this article
Wong, J.C., Lambert, R.J., Wurtzel, E.T. et al. QTL and candidate genes phytoene synthase and ζ-carotene desaturase associated with the accumulation of carotenoids in maize. Theor Appl Genet 108, 349–359 (2004). https://doi.org/10.1007/s00122-003-1436-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-003-1436-4