Mapping QTLs for improving grain yield using the USDA rice mini-core collection

Planta

Volumn 234, Issue 2, 2011, Pages 347-361

  Li, Xiaobai ^a,b,c   Yan, Wengui ^c   Agrama, Hesham ^b   Jia, Limeng ^a,b,c   Shen, Xihong ^d   Jackson, Aaron ^c   Moldenhauer, Karen ^b   Yeater, Kathleen ^c   McClung, Anna ^c   Wu, Dianxing ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF ARKANSAS   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d CHINA NATIONAL RICE RESEARCH INSTITUTE   (China)

Author keywords

Association mapping; Germplasm; Grain yield; Linkage disequilibrium (LD); Rice

Indexed keywords

ANALYSIS OF VARIANCE; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CEREAL; CHROMOSOME MAP; CROP; CROSS BREEDING; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; GENOTYPE; GOVERNMENT; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PLANT CHROMOSOME; QUANTITATIVE TRAIT LOCUS; RICE; UNITED STATES;

ANALYSIS OF VARIANCE; BAYES THEOREM; CEREALS; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CROPS, AGRICULTURAL; CROSSES, GENETIC; GENETIC ASSOCIATION STUDIES; GENETIC LOCI; GENETIC MARKERS; GENETIC VARIATION; GENOTYPE; LINKAGE DISEQUILIBRIUM; MODELS, BIOLOGICAL; ORYZA SATIVA; PHENOTYPE; QUANTITATIVE TRAIT LOCI; UNITED STATES; UNITED STATES DEPARTMENT OF AGRICULTURE;

ORYZA SATIVA;

EID: 79960743377     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-011-1405-0     Document Type: Article

References (101)

1. Abadie T, Cordeiro CMT, Fonseca JR, Alves RBN, Burle ML, Brondani C, Rangel PHN, Castro EM, Silva HT, Freire MS, Zimmermann FJP, Magalhaes JRSO (2005) Constructing a rice core collection for Brazil. Pesquisa Agropecu Bras 40: 129-136.
2. Abdurakhmonov IY, Abdukarimov A (2008) Application of association mapping to understanding the genetic diversity of plant germplasm. Int J Plant Genomics. doi: 10. 1155/2008/574927.
3. 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.
4. Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19: 341-356.
5. Agrama HA, Yan WG, Lee F, Fjellstrom R, Chen MH, Jia M, McClung A (2009) Genetic assessment of a mini-core subset developed from the USDA Rice Genebank. Crop Sci 49: 1336-1346.
6. Agrama HA, Yan WG, Jia M, Fjellstrom R, McClung A (2010) Genetic structure associated with diversity and geographic distribution in the USDA rice world collection. Nat Sci 2: 247-291.
7. Ando T, Yamamoto T, Shimizu T, Ma XF, Shomura A, Takeuchi Y, Lin SY, Yano M (2008) Genetic dissection and pyramiding of quantitative traits for panicle architecture by using chromosomal segment substitution lines in rice. Theor Appl Genet 116: 881-890.
8. Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C, Toomajian C, Traw B, Zheng H, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1: 531-539.
9. Ashikari M, Wu J, Yano M, Sasaki T, Yoshimura A (1999) Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein. Proc Natl Acad Sci USA 96: 10284-10289.
10. Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309: 741-745.
11. Bernardo R (2008) Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci 48: 1649-1664.
12. Borba TCO, Brondani RPV, Rangel PHN, Brondani C (2005) Evaluation of the number and information content of fluorescent-labeled SSR for rice germplasm characterization. Crop Breed Appl Biotechnol 2: 157-165.
13. Borba TCO, Brondani RPV, Rangel PHN, Brondani C (2009) Microsatellite marker-mediated analysis of the EMBRAPA Rice Core Collection genetic diversity. Genetica 137: 293-304.
14. Borba TCO, Brondani RPV, Breseghello F, Coelho ASG, Mendonça JA, Rangel PHN, Brondani C (2010) Association mapping for yield and grain quality traits in rice (Oryza sativa L.). Genet Mol Biol 33: 515-524.
15. Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172: 1165-1177.
16. Brondani C, Rangel N, Brondani V, Ferreira E (2002) QTL mapping and introgression of yield-related traits from Oryza glumaepatula to cultivated rice (Oryzasativa) using microsatellite markers. Theor Appl Genet 104: 1192-1203.
17. Brondani C, Borba TCO, Rangel PHN, Brondani RPV (2006) Determination of traditional varieties of Brazilian rice using microsatellite markers. Genet Mol Biol 29: 676-684.
18. 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.
19. Chen Y, Lubberstedt T (2010) Molecular basis of trait correlations. Trends Plant Sci 15: 454-461.
20. Chu Y, Ramos L, Holbrook CC, Ozias-Akins P (2007) Frequency of a loss-of-function mutation in oleoyl-PC desaturase (ahFAD2A) in the mini-core of the U. S. peanut germplasm collection. Crop Sci 47: 2372-2378.
21. Cooper M, Podlich DW, Smith OS (2005) Gene-to-phenotype models and complex trait genetics. Aust J Agric Res 56: 895-918.
22. Devlin B, Roeder K (1999) Genomic control for association studies. Biometrics 55: 997-1004.
23. Devlin B, Bacanu SA, Roeder K (2004) Genomic control to the extreme. Nat Genet 36: 1129-1130.
24. Dhanraj A, Jagadish CA (1987) Studies on character association in the F2 generation of ten selected crosses in rice (Oryza sativa L.). J Res A FAU 15: 64-65.
25. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18: 926-936.
26. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
27. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7: 574-578.
28. Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112: 1164-1171.
29. Farnir F, Coppieters W, Arranz J-J, Berzi P, Cambisano N, Grisart B, Karim L, Marcq F, Moreau L, Mni M, Nezer C, Simon P, Vanmanshoven P, Wagenaar D, Georges M (2000) Extensive genome-wide linkage disequilibrium in cattle. Genome Res 10: 220-227.
30. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54: 357-374.
31. Flint-Garcia SA, Thuillet AC, Yu JM, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44: 1054-1064.
32. Franco J, Crossa J, Warburton ML, Taba S (2006) Sampling strategies for conserving maize diversity when forming core subsets using genetic markers. Crop Sci 46: 854-864.
33. Fu Q, Zhang P, Tan L, Zhu Z, Ma D, Fu Y, Zhan X, Cai H, Sun C (2010) Analysis of QTLs for yield-related traits in Yuanjiang common wild rice (Oryzarufipogon Griff.). J Genet Genomics 37: 147-157.
34. Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165: 759-769.
35. Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch SR (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169: 1631-1638.
36. Gravois KA, McNew RW (1993) Genetic relationships among and selection for rice yield and yield components. Crop Sci 33: 249-252.
37. 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.
38. Hemamalini GS, Shashidhar HE, Hittalmani S (2000) Molecular marker assisted tagging of morphological and physiological traits under two contrasting moisture regimes at peak vegetative stage in rice (Oryza sativa L.). Euphytica 112: 69-78.
39. Holbrook CC, Dong W (2005) Development and evaluation of a mini core collection for the U. S. peanut germplasm collection. Crop Sci 45: 1540-1544.
40. Holland J (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10: 156-161.
41. Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41: 494-497.
42. Hunter DJ, Kraft P, Jacobs KB, Cox DG, Yeager M, Hankinson SE, Wacholder S, Wang Z, Welch R, Hutchinson A, Wang J, Yu K, Chatterjee N, Orr N, Willett WC, Colditz GA, Ziegler RG, Berg CD, Buys SS, McCarty CA, Feigelson HS, Calle EE, Thun MJ, Hayes RB, Tucker M, Gerhard DS, Fraumeni JF Jr, Hoover RN, Thomas G, Chanock SJ (2007) A genome-wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer. Nat Genet 39: 870-874.
43. Huttley GA, Smit MW, Carrington HM, O'Brien SJ (1999) A scan for linkage disequilibrium across the human genome. Genetics 152: 1711-1722.
44. Inostroza L, Pozo AD, Matus I, Castillo D, Hayes P, Machado S, Corey A (2009) Association mapping of plant height, yield, and yield stability in recombinant chromosome substitution lines (RCSLs) using Hordeum vulgare subsp. spontaneum as a source of donor alleles in a Hordeum vulgare subsp. vulgare background. Mol Breed 23: 365-376.
45. Itoh H, Tatsumi T, Sakamoto T, Otomo K, Toyomasu T, Kitano H, Ashikari M, Ichihara S, Matsuoka M (2004) A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol Biol 54: 533-547.
46. Jiang GH, Xu CG, Li XH, He YQ (2004) Characterization of the genetic basis for yield and its component traits of rice revealed by doubled haploid population. Acta Genet Sinicavol 31: 63-72.
47. Jin L, Lu Y, Xiao P, Sun M, Corke H, Bao J (2010) Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 121: 475-487.
48. Kraakman ATW, Niks RE, van den Berg PMMM, Stam P, van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168: 435-446.
49. Li DJ, Sun CQ, Fu YC, Chen L, Zhu ZF, Li C, Cai HW, Wang XK (2002) Identification and mapping of genes for improving yield from Chinese common wild rice (O. rufipogon Griff.) using advanced backcross QTL analysis. Chin Sci Bull 18: 1533-1537.
50. Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422: 618-621.
51. Li C, Zhou A, Sang T (2006) Genetic analysis of rice domestication syndrome with the wild annual species, Oryzanivara. New Phytol 170: 185-194.
52. Li X, Yan W, Agrama H, Hu B, Jia L, Jia M, Jackson A, Moldenhauer K, McClung A, Wu D (2010) Genotypic and phenotypic characterization of genetic differentiation and diversity in the USDA rice mini-core collection. Genetica 138: 1221-1230.
53. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21: 2128-2129.
54. Maccaferri M, Sanguineti MC, Noli E, Tuberosa R (2005) Population structure and long-range linkage disequilibrium in a drum wheat elite collection. Mol Breed 15: 271-289.
55. 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.
56. 2 population evaluated in an upland environment. Theor Appl Genet 102: 41-52.
57. Nei M, Takezaki N (1983) Estimation of genetic distances and phylogenetic trees from DNA analysis. Proceedings of the 5th world congress. Genet Appl Livestock Prod 21: 405-412.
58. Novembre J, Stephens M (2008) Interpreting principal component analyses of spatial population genetic variation. Nat Genet 40: 646-649.
59. 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.
60. Pande S, Kishore GK, Upadhyaya HD, Rao JN (2006) Identification of sources of multiple disease resistance in mini-core collection of chickpea. Plant Dis 90: 1214-1218.
61. Patterson N, Price AL, Reich D (2007) Population structure and eigenanalysis. PLoS Genet 2: e90.
62. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400: 256-261.
63. 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.
64. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
65. 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 Oryzasativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114: 731-743.
66. Reich D, Price AL, Patterson N (2008) Principal component analysis of genetic data. Nat Genet 40: 491-492.
67. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley 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.
68. Rohlf F (2000) NTSYS-PC numerical taxonomy and multivariate analysis system ver 2. 11L. Applied Biostatistics, New York.
69. Samonte SOP, Wilson LT, McClung AM (1998) Path analyses of yield and yield-related traits of fifteen diverse rice genotypes. Crop Sci 38: 1130-1136.
70. Shao Y, Jin L, Zhang G, Lu Y, Shen Y, Bao J (2010) Association mapping of grain color, phenolic content, flavonoid content and antioxidant capacity in dehulled rice. Theor Appl Genet. doi: 10. 1007/s00122-010-1505-4.
71. Sharma RS, Choubey SD (1985) Correlation studies in upland rice. Indian J Agron 30: 87-88.
72. Sharma R, Rao VP, Upadhyaya HD, Reddy VG, Thakur RP (2010) Resistance to grain mold and downy mildew in a mini-core collection of sorghum germplasm. Plant Dis 94: 439-444.
73. Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassicanapus. Genetics 182: 851-861.
74. Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39: 623-630.
75. Spielmeyer W, Ellis MH, Peter M (2002) Semidwarf (sd-1), "green revolution" rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99: 9043-9048.
76. Stich B, Melchinger AE, Frisch M, Maurer HP, Heckenberger M, Reif JC (2005) Linkage disequilibrium in European elite maize germplasm investigated with SSRs. Theor Appl Genet 111: 723-730.
77. Stich B, Maurer HP, Melchinger AE, Frisch M, Heckenberger M, van der Voort JR, Peleman J, Sørensen AP, Reif JC (2006) Comparison of linkage disequilibrium in elite European maize inbred lines using AFLP and SSR markers. Mol Breed 17: 217-226.
78. Stich B, Möhring J, Piepho HP, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178: 1745-1754.
79. Suh JP, Ahn SN, Cho YC, Kang KH, Choi IS, Kim YG, Suh HS, Hong HC (2005) Mapping of QTLs for yield traits using an advanced backcross population from a cross between Oryzasativa and O. glaberrima. Korean J Breed 37: 214-220.
80. Sweeney MT, Thomson MJ, Pfeil BE, McCouch S (2006) Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18: 283-294.
81. Takahashi Y, Shomura A, Sasaki T, Yano M (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA 98: 7922-7927.
82. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
83. Terao T, Nagata K, Morino K, Hirose T (2010) A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor Appl Genet 120: 875-893.
84. Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinea CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107: 479-493.
85. 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.
86. Upadhyaya HD (2005) Variability for drought resistance related traits in the mini core collection of peanut. Crop Sci 45: 1432-1440.
87. Upadhyaya HD, Oritz R (2001) A mini-core collection for capturing diversity and promoting utilization of chickpea genetic resources in crop improvement. Theor Appl Genet 102: 1292-1298.
88. Upadhyaya HD, Reddy LJ, Gowda CLL, Reddy KN, Singh S (2006) Development of a mini core for enhanced and diversified utilization of pigeonpea germplasm resources. Crop Sci 46: 2127-2132.
89. Upadhyaya HD, Pundir RPS, Dwivedi SL, Gowda CLL, Reddy VG, Singh S (2009) Developing a mini core collection of sorghum for diversified utilization of germplasm. Crop Sci 49: 1769-1780.
90. Wang ML, Zhu C, Barkley NA, Chen Z, Erpelding JE, Murray SC, Tuinstra MR, Tesso T, Pederson GA, Yu J (2009) Genetic diversity and population structure analysis of accessions in the US historic sweet sorghum collection. Theor Appl Genet 120: 13-23.
91. Weir BS (1996) Genetic data analysis. II. Methods for discrete population genetic data. Sinauer Associates, Sunderland.
92. Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 447: 661-678.
93. Xin Z, Velten JP, Oliver MJ, Burke JJ (2003) Highthroughput DNA extraction method suitable for PCR. Biotechniques 34: 820-826.
94. Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 143: 1-7.
95. Yan WG, Rutger JN, Bockelman HE, Tai TH (2005a) Agronomic evaluation and seed stock establishment of the USDA rice core collection. In Norman RJ et al (eds) B. R. Wells rice research studies 2004. University of Arkansas, Agricultural Experiment Station Research Series 529, pp 63-68.
96. Yan WG, Rutger JN, Bockelman HE, Tai TH (2005b) Evaluation of kernel characteristics of the USDA rice core collection. In Norman RJ et al (eds) B. R. Wells rice research studies 2004. University of Arkansas, Agricultural Experiment Station Research Series 529, pp 69-74.
97. Yan WG, Rutger JN, Bryant RJ, Bockelman HE, Fjellstrom RG, Chen MH, Tai TH, McClung AM (2007) Development and evaluation of a core subset of the USDA rice (Oryza sativa L.) germplasm collection. Crop Sci 47: 869-878.
98. Yan WG, Li Y, Agrama HA, Luo D, Gao F, Lu X, Ren G (2009) Association mapping of stigma and spikelet characteristics in rice (Oryza sativa L.). Mol Breed 24: 277-292.
99. Yeager M, Orr N, Hayes RB, Jacobs KB, Kraft P, Wacholder S, Minichiello MJ, Fearnhead P, Yu K, Chatterjee N, Wang Z, Welch R, Staats BJ, Calle EE, Feigelson HS, Thun MJ, Rodriguez C, Albanes D, Virtamo J, Weinstein S, Schumacher FR, Giovannucci E, Willett WC, Cancel-Tassin G, Cussenot O, Valeri A, Andriole GL, Gelmann EP, Tucker M, Gerhard DS, Fraumeni JF Jr, Hoover R, Hunter DJ, Chanock SJ, Thomas G (2007) Genome-wide association study of prostate cancer identifies a second risk locus at 8q24. Nat Genet 39: 645-649.
100. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki 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.
101. Zhu C, Yu J (2009) Nonmetric multidimensional scaling corrects for population structure in association mapping with different sample types. Genetics 182: 875-888.