Abstract
Phytochemicals such as phenolics and flavonoids in rice grain are antioxidants that are associated with reduced risk of developing chronic diseases including cardiovascular disease, type-2 diabetes and some cancers. Understanding the genetic basis of these traits is necessary for the improvement of nutritional quality by breeding. Association mapping based on linkage disequilibrium has emerged as a powerful strategy for identifying genes or quantitative trait loci (QTL) underlying complex traits in plants. In this study, genome-wide association mapping using models controlling both population structure (Q) and relative kinship (K) were performed to identify the marker loci/QTLs underlying the naturally occurring variations of grain color and nutritional quality traits in 416 rice germplasm accessions including red and black rice. A total of 41 marker loci were identified for all the traits, and it was confirmed that Ra (i.e., Prp-b for purple pericarp) and Rc (brown pericarp and seed coat) genes were main-effect loci for rice grain color and nutritional quality traits. RM228, RM339, fgr (fragrance gene) and RM316 were important markers associated with most of the traits. Association mapping for the traits of the 361 white or non-pigmented rice accessions (i.e., excluding the red and black rice) revealed a total of 11 markers for four color parameters, and one marker (RM346) for phenolic content. Among them, Wx gene locus was identified for the color parameters of lightness (L*), redness (a*) and hue angle (H o). Our study suggested that the markers identified in this study can feasibly be used to improve nutritional quality or health benefit properties of rice by marker-assisted selection if the co-segregations of the marker–trait associations are validated in segregating populations.
Similar content being viewed by others
References
Abdel-Aal ESM, Young JC, Rabalski I (2006) Anthocyanin composition in black, blue, pink, purple, and red cereal grains. J Agric Food Chem 54:4696–4704
Agrama HA, Eizenga GC (2008) Molecular diversity and genome-wide linkage disequilibrium patterns in a worldwide collection of Oryza sativa and its wild relatives. Euphytica 160:339–355
Agrama HA, Yan W (2009) Association mapping of straighthead disorder induced by arsenic in Oryza sativa. Plant Breed 128:551–558
Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356
Bao JS, Corke H, Sun M (2006a) Microsatellites single nucleotide polymorphisms and a sequence tagged site in starch-synthesizing genes in relation to starch physicochemical properties in nonwaxy rice (Oryza sativa L.). Theor Appl Genet 113:1185–1196
Bao JS, Corke H, Sun M (2006b) Nucleotide diversity in starch synthase IIa and validation of single nucleotide polymorphisms in relation to starch gelatinization temperature and other physicochemical properties in rice (Oryza sativa L.). Theor Appl Genet 113:1171–1183
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Bouis HE, Chassy BM, Ochanda JO (2003) Genetically modified food crops and their contribution to human nutrition and food quality. Trend Food Sci Tech 14:191–209
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Brooks SA, Yan W, Jackson AK, Deren CW (2008) A natural mutation in rc reverts white-rice-pericarp to red and results in a new, dominant, wild-type allele: Rc-g. Theor Appl Genet 117:575–580
Doyle JJ (1991) DNA protocols for plants-CTAB total DNA isolation. In: Hewitt GM (ed) Molecular techniques in taxonomy. Springer, Berlin pp 283–293
Ersoz ES, Yu J, Buckler ES (2009) Applications of linkage disequilibrium and association mapping in maize. In: Kriz A, Larkins B (eds) Molecular genetic approaches to maize improvement. Springer, Berlin, p173–195
Finocchiaro F, Ferrari B, Gianinetti A, Dall’asta C, Galaverna G, Scazzina F, Pellegrini N (2007) Characterization of antioxidant compounds of red and white rice and changes in total antioxidant capacity during processing. Mol Nutr Food Res 51:1006–1019
Fitzgerald MA, McCouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trend Plant Sci 14:133–139
Furukawa T, Maekawa M, Oki T, Suda I, Iida S, Shimada H, Takamure I, Kadowaki KI (2007) The Rc and Rd genes are involved in proanthocyanidin synthesis in rice pericarp. Plant J 49:91–102
Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch SR (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638
Goffman FD, Bergman CJ (2004) Rice kernel phenolic content and its relationship with antiradical efficiency. J Sci Food Agric 10:1002–1007
Hall D, Tegstrom C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genom 9:157–165
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hu C, Zawistowski J, Ling W, Kitts DD (2003) Black rice (Oryza sativa L. indica) pigmented fraction suppresses both reactive oxygen species and nitric oxide in chemical and biological model systems. J Agric Food Chem 51:5271–5277
Iwata H, Ebana K, Uga Y, Hayashi T, Jannink J-L (2010) Genome-wide association study of grain shape variation among Oryza sativa L. germplasms based on elliptic Fourier analysis. Mol Breed 25:203–215
Jin L, Xiao P, Lu Y, Shao YF, Shen Y, Bao JS (2009) Quantitative trait loci for brown rice color, total phenolics and, flavonoid contents and antioxidant capacity in rice grain. Cereal Chem 86:609–615
Jin L, Lu Y, Xiao P, Sun M, Corke H, Bao JS (2010a) Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 121:475–487
Jin L, Lu Y, Shao YF, Zhang G, Xiao P, Shen SQ, Corke H, Bao JS (2010b) Molecular marker assisted selection for improvement of the eating, cooking and sensory quality of rice (Oryza sativa L.). J Cereal Sci 51:159–164
Ling WH, Cheng QX, Ma J, Wang T (2001) Red and black rice decrease atherosclerotic plaque formation and increase antioxidant status in rabbits. J Nutr 131:1421–1426
Liu RH (2007) Whole grain phytochemicals and health. J Cereal Sci 46:207–219
Lorieux M, Petrov M, Huang N, Guiderdoni E, Ghesquiere A (1996) Aroma in rice: genetic analysis of a quantitative trait. Theor Appl Genet 93:1145–1151
Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, Purugganan MD (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177:2223–2232
Oki T, Masuda M, Kobayashi M, Nishiba Y, Furuta S, Suda I, Sato T (2002) Polymeric procyanidins as radical-scavenging components in red-hulled rice. J Agric Food Chem 50:7524–7529
Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan D (2006) Selection under domestication: evidence for a sweep in the rice Waxy genomic region. Genetics 173:975–983
Ordonez SA Jr, Silva J, Oard JH (2010) Association mapping of grain quality and flowering time in elite japonica rice germplasm. J Cereal Sci 51:337–343
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rakshit S, Rakshit A, Matsumura H, Takahashi Y, Hasegawa Y, Ito A, Ishii T, Miyashita NT, Terauchi R (2007) Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114:731–743
Reddy VS, Dash S, Reddy AR (1995) Anthocyanin pathway in rice (Oryza sativa L.): identification of a mutant showing dominant inhibition of anthocyanins in leaf and accumulation of proanthocyanidins in pericarp. Theor Appl Genet 91:301–312
Rezaeizad A, Wittkop B, Snowdon R, Hasan M, Mohammadi V, Zali A, Friedt W (2010) Identification of QTLs for phenolic compounds in oilseed rape (Brassica napus L.) by association mapping using SSR markers. Euphytica. doi:10.1007/s10681-010-0231-y
Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185
Seal CJ (2006) Whole grains and CVD risk. Proc Nutr Soc 65:24–34
Shen Y, Jin L, Xiao P, Lu Y, Bao JS (2009) Total phenolics, flavonoids, antioxidant capacity in rice grain and their relations to grain color, size and weight. J Cereal Sci 49:106–111
Stich B, Melchinger AE (2010) An introduction to association mapping in plants. CAB Rev 5:039
Stich B, Mohring J, Piepho H, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445
Sweeney MT, Thomson MJ, Pfeil BE, McCouch SR (2006) Caught red-handed: Rc encodes a basic helix–loop–helix protein conditioning red pericarp in rice. Plant Cell 18:283–294
Takaiwa F, Yang L, Yasuda H (2008) Health-promoting transgenic rice: application of rice seeds as a direct delivery system for bioactive peptides in human health. In: Hirano HY, Sano Y, Hirai A, Sasaki T (eds) Rice biology in the genomics era. Springer, Berlin pp 357–373
Tan YF, Sun M, Xing YZ, Hua JP, Xun XL, Zhang QF, Corke H (2001) Mapping quantitative trait loci for milling quality, protein content and color characteristics of rice using a recombinant inbred line population derived from an elite rice hybrid. Theor Appl Genet 103:1037–1045
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, ES Buckler IV (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Tian S, Nakamura K, Kayara H (2004) Analysis of phenolic compounds in white rice, brown rice and germinated brown rice. J Agric Food Chem 52:4808–4813
Toyokuni S, Itani T, Morimitsu Y, Okada K, Ozeki M, Kondo S, Uchida K, Osawa T, Hiai H, Tashiro T (2002) Protective effect of coloured rice over white rice on Fenton reaction-based renal lipid peroxidation in rats. Free Radic Res35:583–592
Vitaglione P, Napolitano A, Fogliano V (2008) Cereal dietary fibre: a natural functional ingredient to deliver phenolic compounds into the gut. Trend Food Sci Tech 19:451–463
Wang CX, Shu QY (2007) Fine mapping and candidate gene analysis of purple pericarp gene Pb in rice (Oryza sativa L.). Chin Sci Bull 52:3097–3104
Welch RM, Graham R (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364
Wen W, Mei H, Feng F, Yu S, Huang Z, Wu J, Chen L, Xu X, Luo L (2009) Population structure and association mapping on chromosome 7 using a diverse panel of Chinese germplasm of rice (Oryza sativa L.). Theor Appl Genet 119:459–470
Xia M, Ling WH, Ma J, Kitts DD, Zawistowski J (2003) Supplementation of diets with the black rice pigment fraction attenuates atherosclerotic plaque formation in apolipoprotein E deficient mice. J Nutr 133:744–751
Yang XH, Yan JB, Shah T, Warburton ML, Li Q, Li L, Gao YF, Chai YC, Fu ZY, Zhou Y, Xu ST, Bai GH, Meng YJ, Zheng YP, Li JS (2010) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121:417–431
Yawadio R, Tanimori S, Morita N (2007) Identification of phenolic compounds isolated from pigmented rices and their aldose reductase inhibitory activities. Food Chem 101:1644–1653
Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrokus I (2000) Engineering the pro-vitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305
Yoshimura A, Ideta O, Iwata N (1997) Linkage map of phenotype and RFLP markers in rice. Plant Mol Biol 35:49–60
Yu J, Pressoir G, Briggs WH, Bi IV, Yamsaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhang CY, Shen Y, Chen J, Xiao P, Bao JS (2008) Nondestructive prediction of total phenolics and flavonoid contents, and antioxidant capacity of rice grain using near-infrared spectroscopy. J Agric Food Chem 56:8268–8272
Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20
Zhu F, Cai YZ, Bao JS, Corke H (2010) Effect of γ-irradiation on phenolic compounds in rice grain. Food Chem 120:74–77
Zimmermann MB, Hurrell RF (2002) Improving iron, zinc and vitamin A nutrition through plant biotechnology. Curr Opin Biotech 13:142–145
Acknowledgments
Financial support for this work was provided in part by the Zhejiang Provincial Natural Science Foundation of China (R3080016), the Science and Technology Department of Zhejiang Province (2010C32082), the Program for the New Century Excellent Talents in University (NCET-08-0484) and the ANTA project from the Chinese Ministry of Agriculture (200803034).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Yu.
Y. Shao and L. Jin have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shao, Y., Jin, L., Zhang, G. et al. Association mapping of grain color, phenolic content, flavonoid content and antioxidant capacity in dehulled rice. Theor Appl Genet 122, 1005–1016 (2011). https://doi.org/10.1007/s00122-010-1505-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-010-1505-4