A foundation for provitamin a biofortification of maize: Genome-wide association and genomic prediction models of carotenoid levels

Genetics

Volumn 198, Issue 4, 2014, Pages 1699-1716

  Owens, Brenda F ^a   Gore, Michael A ^b,b   Magallanes Lundback, Maria ^d   Tiede, Tyler ^a   Diepenbrock, Christine H ^b   Kandianis, Catherine B ^b,d   Kim, Eunha ^d   Cepela, Jason ^e   Mateos Hernandez, Maria ^a   Robin Buell, C ^e   Buckler, Edward S ^b,f   DellaPenna, Dean ^d   Rocheford, Torbert ^a  

^a PURDUE UNIVERSITY   (United States)

^b Department of Molecular Biology and Genetics   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d Michigan State University   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CAROTENE; ASPARTIC PROTEINASE; BETA CAROTENE; BETA CRYPTOXANTHIN; CAROTENE; CAROTENOID; TERPENOID DERIVATIVE; XANTHOPHYLL; ZEAXANTHIN; ZETA CAROTENE;

ARTICLE; BIOCHEMISTRY; BIOSYNTHESIS; FOOD COLOR; FOOD COMPOSITION; FOOD CROP; FOOD PROCESSING; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC CODE; GENETIC LINKAGE; GENETIC MARKER; GENETIC MODEL; GENETIC SELECTION; GENETIC VARIABILITY; GENOMICS; GERMPLASM; INBRED STRAIN; INDEL MUTATION; MAIZE; NONHUMAN; PHENOTYPIC VARIATION; PLANT GENE; PLANT GENETICS; QUANTITATIVE TRAIT LOCUS; SEED KERNEL; SINGLE NUCLEOTIDE POLYMORPHISM; BIOLOGICAL MODEL; GENE LINKAGE DISEQUILIBRIUM; GENETICS; METABOLISM; PHENOTYPE; QUANTITATIVE TRAIT; REPRODUCIBILITY;

ZEA MAYS;

BIOSYNTHETIC PATHWAYS; CAROTENOIDS; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; LINKAGE DISEQUILIBRIUM; MODELS, BIOLOGICAL; PHENOTYPE; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; REPRODUCIBILITY OF RESULTS; ZEA MAYS;

EID: 84915748046     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.169979     Document Type: Article

References (94)

1. Abdel-Aal, E. M., H. Akhtar, K. Zaheer, and R. Ali, 2013 Dietary sources of lutein and zeaxanthin carotenoids and their role in eye health. Nutrients 5: 1169-1185.
2. Azmach, G., M. Gedil, A. Menkir, and C. Spillane, 2013 Markertrait association analysis of functional gene markers for provitamin A levels across diverse tropical yellow maize inbred lines. BMC Plant Biol. 13: 227.
3. Babu, R., N. P. Rojas, S. B. Gao, J. B. Yan, and K. Pixley, 2013 Validation of the effects of molecular marker polymorphisms in LcyE and CrtRB1 on provitamin A concentrations for 26 tropical maize populations. Theor. Appl. Genet. 126: 389-399.
4. Baranzini, S. E., N.W. Galwey, J.Wang, P. Khankhanian, R. Lindberg et al., 2009 Pathway and network-based analysis of genomewide association studies in multiple sclerosis. Hum. Mol. Genet. 18: 2078-2090.
5. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57: 289-300.
6. Berardo, N., G. Mazzinelli, P. Valoti, P. Lagana, and R. Redaelli, 2009 Characterization of maize germplasm for the chemical composition of the grain. J. Agric. Food Chem. 57: 2378-2384.
7. Box, G. E. P., and D. R. Cox, 1964 An analysis of transformations. J. R. Stat. Soc., B 26: 211-252.
8. Bradbury, P. J., Z. Zhang, D. E. Kroon, T. M. Casstevens, Y. Ramdoss et al., 2007 TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23: 2633-2635.
9. Britton, G., 1995a Structure and properties of carotenoids in relation to function. FASEB J. 9: 1551-1558.
10. Britton, G., 1995b Carotenoids: Isolation and Analysis. Birkhäuser, Basel.
11. Buckner, B., T. L. Kelson, and D. S. Robertson, 1990 Cloning of the y1 locus of maize, a gene involved in the biosynthesis of carotenoids. Plant Cell 2: 867-876.
12. Burri, B. J., J. S. T. Chang, and T. R. Neidlinger, 2011 b-Cryptoxanthinand a-carotene-rich foods have greater apparent bioavailability than b-carotene-rich foods in Western diets. Br. J. Nutr. 105: 212-219.
13. Burt, A. J., C. M. Grainger, M. P. Smid, B. J. Shelp, and E. A. Lee, 2011 Allele mining of exotic maize germplasm to enhance macular carotenoids. Crop Sci. 51: 991-1004.
14. Califano, A., A. J. Butte, S. Friend, T. Ideker, and E. Schadt, 2012 Leveraging models of cell regulation and GWAS data in integrative network-based association studies. Nat. Genet. 44: 841-847.
15. Cazzonelli, C. I., and B. J. Pogson, 2010 Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 15: 266-274.
16. Chan, E. K. F., H. C. Rowe, J. A. Corwin, B. Joseph, and D. J. Kliebenstein, 2011 Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biol. 9: e1001125.
17. Chander, S., Y. Q. Guo, X. H. Yang, J. Zhang, X. Q. Lu et al., 2008 Using molecular markers to identify two major loci controlling carotenoid contents in maize grain. Theor. Appl. Genet. 116: 223-233.
18. Chandler, K., A. E. Lipka, B. F. Owens, H. H. Li, E. S. Buckler et al., 2013 Genetic analysis of visually scored orange kernel color in maize. Crop Sci. 53: 189-200.
19. Chen, J. H., and Z. H. Chen, 2008 Extended Bayesian information criteria for model selection with large model spaces. Biometrika 95: 759-771.
20. Chia, J. M., C. Song, P. J. Bradbury, D. Costich, N. de Leon et al., 2012 Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 44: 803-807.
21. Combs, G. F., 2012 Vitamin A, pp. 93-138 in Vitamins: Fundamental Aspects in Nutrition and Health, Ed 4. Academic Press, New York, NY.
22. Cunningham, F. X., B. Pogson, Z. R. Sun, K. A.McDonald, D. DellaPenna et al., 1996 Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8: 1613-1626.
23. Cuttriss, A. J., C. I. Cazzonelli, E. T. Wurtzel, and B. J. Pogson, 2011 Carotenoids. Adv. Bot. Res. 58: 1-36.
24. Davis, C., H. Jing, J. A. Howe, T. Rocheford, and S. A. Tanumihardjo, 2008 b-Cryptoxanthin from supplements or carotenoid-enhanced maize maintains liver vitamin A in Mongolian gerbils (Meriones unguiculatus) better than or equal to b-carotene supplements. Br. J. Nutr. 100: 786-793.
25. DellaPenna, D., and B. J. Pogson, 2006 Vitamin synthesis in plants: tocopherols and carotenoids. Annu. Rev. Plant Biol. 57: 711-738.
26. Egesel, C. O., J. C. Wong, R. J. Lambert, and T. R. Rocheford, 2003 Gene dosage effects on carotenoid concentration in maize grain. Maydica 48: 183-190.
27. Emerson, R. A., 1921 The Genetic Relations of Plant Colors in Maize. Cornell University Press, Ithaca, NY.
28. Endelman, J. B., 2011 Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4: 250-255.
29. Flint-Garcia, S. A., A. C. Thuillet, J. M. Yu, G. Pressoir, S. M. Romero et al., 2005 Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J. 44: 1054-1064.
30. Friedman, D. S., B.O'Colmain, S. C. Tomany, C. McCarty, P. T. de Jong et al., 2004 Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 122: 564-572.
31. Friedman, J., T. Hastie, and R. Tibshirani, 2010 Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33: 1-22.
32. Fu, J., Y. Cheng, J. Linghu, X. Yang, L. Kang et al., 2013 RNA sequencing reveals the complex regulatory network in the maize kernel. Nat. Commun. 4: 2832.
33. Fu, Z. Y., Y. C. Chai, Y. Zhou, X. H. Yang, M. L. Warburton et al., 2013 Natural variation in the sequence of PSY1 and frequency of favorable polymorphisms among tropical and temperate maize germplasm. Theor. Appl. Genet. 126: 923-935.
34. Gilmour, A. R. G., B.; B. Cullis, R. Thompson, D. Butler, 2009 Asreml User Guide Release 3.0. VSN International Ltd, Hemel Hempstead, UK.
35. Goff, S. A., and H. J. Klee, 2006 Plant volatile compounds: Sensory cues for health and nutritional value? Science 311: 815-819.
36. Gonzalez-Jorge, S., S.H.Ha, M. Magallanes-Lundback, L. U. Gilliland, A. L. Zhou et al., 2013 Carotenoid cleavage dioxygenase4 is a negative regulator of b-carotene content in Arabidopsis seeds. Plant Cell 25: 4812-4826.
37. Gore, M. A., J. M. Chia, R. J. Elshire, Q. Sun, E. S. Ersoz et al., 2009 A first-generation haplotype map of maize. Science 326: 1115-1117.
38. Harjes, C. E., T. R. Rocheford, L. Bai, T. P. Brutnell, C. B. Kandianis et al., 2008 Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-333.
39. Hieber, A. D., R. C. Bugos, and H. Y. Yamamoto, 2000 Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim. Biophys. Acta 1482: 84-91.
40. Holland, J. B., W. E. Nyquist, and C. T. Cervantes-Martinez, 2003 Estimating and interpreting heritability for plant breeding: an update. Plant Breed. Rev. 22: 9-112.
41. Howe, J. A., and S. A. Tanumihardjo, 2006 Carotenoid-biofortified maize maintains adequate vitamin A status in Mongolian gerbils. J. Nutr. 136: 2562-2567.
42. Howitt, C. A., and B. J. Pogson, 2006 Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ. 29: 435-445.
43. Hung, H. Y., C. Browne, K. Guill, N. Coles, M. Eller et al., 2012 The relationship between parental genetic or phenotypic divergence and progeny variation in the maize nested association mapping population. Heredity 108: 490-499.
44. Jerome-Morais, A., A. M. Diamond, and M. E. Wright, 2011 Dietary supplements and human health: For better or for worse? Mol. Nutr. Food Res. 55: 122-135.
45. Kandianis, C. B., R. Stevens, W. P. Liu, N. Palacios, K. Montgomery et al., 2013 Genetic architecture controlling variation in grain carotenoid composition and concentrations in two maize populations. Theor. Appl. Genet. 126: 2879-2895.
46. Kermode, A. R., 2005 Role of abscisic acid in seed dormancy. J. Plant Growth Regul. 24: 319-344.
47. Khoo, H. E., K. N. Prasad, K. W. Kong, Y. Jiang, and A. Ismail, 2011 Carotenoids and their isomers: color pigments in fruits and vegetables. Molecules 16: 1710-1738.
48. Kim, J., J. J. Smith, L. Tian, and D. DellaPenna, 2009 The evolution and function of carotenoid hydroxylases in Arabidopsis. Plant Cell Physiol. 50: 463-479.
49. Krinsky, N. I., J. T. Landrum, and R. A. Bone, 2003 Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu. Rev. Nutr. 23: 171-201.
50. Kutner, M. H., 2005 Applied Linear Statistical Models. McGraw-Hill Irwin, Boston.
51. Lantieri, F., M. A. Jhun, J. Park, T. Park, and M. Devoto, 2009 Comparative analysis of different approaches for dealing with candidate regions in the context of a genome-wide association study. BMC Proc. 3(Suppl 7): S93.
52. Li, Z. H., P. D. Matthews, B. Burr, and E. T. Wurtzel, 1996 Cloning and characterization of a maize cDNA encoding phytoene desaturase, an enzyme of the carotenoid biosynthetic pathway. Plant Mol. Biol. 30: 269-279.
53. Lipka, A. E., M. A. Gore, M. Magallanes-Lundback, A. Mesberg, H. N. Lin et al., 2013 Genome-wide association study and pathwaylevel analysis of tocochromanol levels in maize grain. G3 (Bethesda) 3: 1287-1299.
54. Loiselle, B. A., V. L. Sork, J. Nason, and C. Graham, 1995 Spatial genetic-structure of a tropical understory shrub, Psychotria Officinalis (Rubiaceae). Am. J. Bot. 82: 1420-1425.
55. Long, A. D., and C. H. Langley, 1999 The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res. 9: 720-731.
56. Lorenz, A. J., S. M. Chao, F. G. Asoro, E. L. Heffner, T. Hayashi et al., 2011 Genomic selection in plant breeding: knowledge and prospects. Adv. Agron. 110: 77-123.
57. Lubin, J. H., J. S. Colt, D. Camann, S. Davis, J. R. Cerhan et al., 2004 Epidemiologic evaluation of measurement data in the presence of detection limits. Environ. Health Perspect. 112: 1691-1696.
58. Matthews, P. D., R. B. Luo, and E. T. Wurtzel, 2003 Maize phytoene desaturase and zeta-carotene desaturase catalyse a poly-Z desaturation pathway: implications for genetic engineering of carotenoid content among cereal crops. J. Exp. Bot. 54: 2215-2230.
59. McMullen, M. D., S. Kresovich, H. S. Villeda, P. Bradbury, H. H. Li et al., 2009 Genetic properties of the maize nested association mapping population. Science 325: 737-740.
60. Meenakshi, J. V., A. Banerji, V. Manyong, K. Tomlins, P. Hamukwala et al., 2010 Consumer acceptance of provitamin A orange maize in rural Zambia. HarvestPlus Working Paper 4. IFPRI, Washington, DC.
61. Meuwissen, T.H. E., B. J. Hayes, andM. E.Goddard, 2001 Prediction of total genetic value using genome-wide dense marker maps. Genetics 157: 1819-1829.
62. Moise, A. R., S. Al-Babili, and E. T. Wurtzel, 2014 Mechanistic aspects of carotenoid biosynthesis. Chem. Rev. 114: 164-193.
63. Moran, N. A., and T. Jarvik, 2010 Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328: 624-627.
64. Muzhingi, T., A. S. Langyintuo, L. C. Malaba, and M. Banziger, 2008 Consumer acceptability of yellow maize products in Zimbabwe. Food Policy 33: 352-361.
65. Nestel, P., H. E. Bouis, J. V. Meenakshi, and W. Pfeiffer, 2006 Biofortification of staple food crops. J. Nutr. 136: 1064- 1067.
66. Pfeiffer, W. H., and B. McClafferty, 2007 HarvestPlus: breeding crops for better nutrition. Crop Sci. 47: S88-S105.
67. Pixley, K., N. P. Rojas, R. Babu, R. Mutale, R. Surles et al., 2013 Biofortification of maize with provitamin A carotenoids, pp. 271-292 in Carotenoids and Human Health, edited by S. Tanumihardjo. Humana Press, New York.
68. Platt, A., B. J. Vilhjálmsson, and M. Nordborg, 2010 Conditions under which genome-wide association studies will be positively misleading. Genetics 186: 1045-1052.
69. Price, A. L., N. J. Patterson, R. M. Plenge, M. E. Weinblatt, N. A. Shadick et al., 2006 Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38: 904-909.
70. Quinlan, R. F., M. Shumskaya, L. M. T. Bradbury, J. Beltran, C. H. Ma et al., 2012 Synergistic interactions between carotene ring hydroxylases drive lutein formation in plant carotenoid biosynthesis. Plant Physiol. 160: 204-214.
71. Resende, M. F. R., P. Munoz, M. D. V. Resende, D. J. Garrick, R. L. Fernando et al., 2012 Accuracy of genomic selection methods in a standard data set of loblolly pine (Pinus taeda L.). Genetics 190: 1503-1510.
72. Riedelsheimer, C., A. Czedik-Eysenberg, C. Grieder, J. Lisec, F. Technow et al., 2012 Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat. Genet. 44: 217-220.
73. Romay, M. C., M. J. Millard, J. C. Glaubitz, J. A. Peiffer, K. L. Swarts et al., 2013 Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol. 14: R55.
74. Rutkoski, J., J. Benson, Y. Jia, G. Brown-Guedira, J. L. Jannink et al., 2012 Evaluation of genomic prediction methods for fusarium head Blight resistance in wheat. Plant Genome 5: 51-61.
75. SAS Institute, 2012 The SAS System for Windows. Version 9.3. SAS Institute, Cary, NC.
76. Schwarz, G., 1978 Estimating the dimension of a model. Ann. Stat. 6: 461-464.
77. Segura, V., B. J. Vilhjalmsson, A. Platt, A. Korte, U. Seren et al., 2012 An efficient multi-locus mixed-model approach for genome- wide association studies in structured populations. Nat. Genet. 44: 825-830.
78. Sen, S., and R. Chakraborty, 2011 The role of antioxidants in human health, pp. 1-37 in Oxidative Stress: Diagnostics, Prevention, and Therapy, edited by S. Andreescu, and M. Hepel. Oxford University Press, New York.
79. Stahl, W., and H. Sies, 2005 Bioactivity and protective effects of natural carotenoids. Biochim. Biophys. Acta 1740: 101-107.
80. Stevens, R., and A. Winter-Nelson, 2008 Consumer acceptance of provitamin A-biofortified maize in Maputo, Mozambique. Food Policy 33: 341-351.
81. Sun, G., C. Zhu, M. H. Kramer, S. S. Yang, W. Song et al., 2010 Variation explained in mixed-model association mapping. Heredity 105: 333-340.
82. Tanumihardjo, S. A., H. Bouis, C. Hotz, J. V. Meenakshi, and B. McClafferty, 2008 Biofortification of staple crops: an emerging strategy to combat hidden hunger. Symposium on "Food Technology for Better Nutrition." Comp. Rev. Food Sci. Safety 7: 329-334.
83. Tian, L., V. Musetti, J. Kim, M. Magallanes-Lundback, and D. DellaPenna, 2004 The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid epsilon- ring hydroxylation activity. Proc. Natl. Acad. Sci. USA 101: 402-407.
84. Tibshirani, R., 1996 Regression shrinkage and selection via the Lasso. J. R. Stat. Soc. Series B Stat. Methodol. 58: 267-288.
85. Turner, T., B. J. Burri, K. M. Jamil, and M. Jamil, 2013 The effects of daily consumption of b-cryptoxanthin-rich tangerines and b-carotene-rich sweet potatoes on vitamin A and carotenoid concentrations in plasma and breast milk of Bangladeshi women with low vitamin A status in a randomized controlled trial. Am. J. Clin. Nutr. 98: 1200-1208.
86. Vallabhaneni, R., L. M. T. Bradbury, and E. T. Wurtzel, 2010 The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch. Biochem. Biophys. 504: 104-111.
87. Wang, K., M. Y. Li, and H. Hakonarson, 2010 Analysing biological pathways in genome-wide association studies. Nat. Rev. Genet. 11: 843-854.
88. Wen, W., D. Li, X. Li, Y. Gao, W. Li et al., 2014 Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat. Commun. 5: 3438.
89. Wong, J. C., R. J. Lambert, E. T. Wurtzel, and T. R. Rocheford, 2004 QTL and candidate genes phytoene synthase and zcarotene desaturase associated with the accumulation of carotenoids in maize. Theor. Appl. Genet. 108: 349-359.
90. Wurtzel, E. T., A. Cuttriss, and R. Vallabhaneni, 2012 Maize provitamin A carotenoids, current resources, and future metabolic engineering challenges. Front. Plant Sci. 3: 1-12.
91. Yan, J. B., C. B. Kandianis, C. E. Harjes, L. Bai, E. H. Kim et al., 2010 Rare genetic variation at Zea mays crtRB1 increases betacarotene in maize grain. Nat. Genet. 42: 322-327.
92. Yu, J. M., G. Pressoir, W. H. Briggs, I. V. Bi, M. Yamasaki et al., 2006 A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38: 203-208.
93. Zhou, Y., Y. J. Han, Z. G. Li, Y. Fu, Z. Y. Fu et al., 2012 ZmcrtRB3 encodes a carotenoid hydroxylase that affects the accumulation of a-carotene in maize kernel. J. Integr. Plant Biol. 54: 260-269.
94. Zou, H., and T. Hastie, 2005 Regularization and variable selection via the elastic net. J. R. Stat. Soc. B. 67: 301-320.