Genome-wide association studies for agronomical traits in a world wide spring barley collection

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Pasam, Raj K ^a   Sharma, Rajiv ^a   Malosetti, Marcos ^b   van Eeuwijk, Fred A ^b   Haseneyer, Grit ^a,c   Kilian, Benjamin ^a   Graner, Andreas ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HORDEUM;

ARTICLE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETICS; HORDEUM; METHODOLOGY; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM;

GENOME-WIDE ASSOCIATION STUDY; HORDEUM; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 84856167115     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-16     Document Type: Article

References (104)

1. Flint-Garcia SA, Thornsberry JM, Buckler ES. Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 2003, 54:357-374.
2. Zhu C, Gore M, Buckler ES, Yu J. Status and Prospects of Association Mapping in Plants. The Plant Genome Journal 2008, 1(1):5.
3. Hastbacka J, Delachapelle A, Kaitila I, Sistonen P, Weaver A, Lander E. Linkage Disequilibrium Mapping in Isolated Founder Populations - Diastrophic Dysplasia in Finland. Nature Genetics 1992, 2(3):204-211.
4. Lander ES, Schork NJ. Genetic dissection of complex traits. Science 1994, 265(5181):2037-2048.
5. Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES. Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 2005, 44(6):1054-1064.
6. Mackay I, Powell W. Methods for linkage disequilibrium mapping in crops. Trends in Plant Science 2007, 12(2):57-63.
7. Gupta PK, Rustgi S, Kulwal PL. Linkage disequilibrium and association studies in higher plants: Present status and future prospects. Plant MolBiol 2005, 57(4):461-485.
8. Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 2001, 98(16):9161-9166.
9. Caldwell KS, Russell J, Langridge P, Powell W. Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 2006, 172(1):557-567.
10. Hirschhorn JN, Daly MJ. Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 2005, 6(2):95-108.
11. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 2010, 465(7298):627-631.
12. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES. Dwarf8 polymorphisms associate with variation in flowering time. Nature Genetics 2001, 28(3):286-289.
13. Palaisa KA, Morgante M, Williams M, Rafalski A. Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 2003, 15(8):1795-1806.
14. Stracke S, Haseneyer G, Veyrieras JB, Geiger HH, Sauer S, Graner A, Piepho HP. Association mapping reveals gene action and interactions in the determination of flowering time in barley. Theor Appl Genet 2009, 118(2):259-273.
15. Singh A, Reimer S, Pozniak CJ, Clarke FR, Clarke JM, Knox RE, Singh AK. Allelic variation at Psy1-A1 and association with yellow pigment in durum wheat grain. Theoretical and Applied Genetics 2009, 118(8):1539-1548.
16. Li YH, Zhang C, Gao ZS, Smulders MJM, Ma ZL, Liu ZX, Nan HY, Chang RZ, Qiu LJ. Development of SNP markers and haplotype analysis of the candidate gene for rhg1, which confers resistance to soybean cyst nematode in soybean. Mol Breeding 2009, 24(1):63-76.
17. Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX, Purugganan MD. Candidate Gene Association Mapping of Arabidopsis Flowering Time. Genetics 2009, 183(1):325-335.
18. Zhao KY, Aranzana MJ, Kim S, Lister C, Shindo C, Tang CL, Toomajian C, Zheng HG, Dean C, Marjoram P, et al. An Arabidopsis example of association mapping in structured samples. Plos Genetics 2007, 3(1).
19. Kilian B, Özkan H, Kohl J, von Haeseler A, Barale F, Deusch O, Brandolini A, Yucel C, Martin W, Salamini F. Haplotype structure at seven barley genes: relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication. Molecular Genetics and Genomics 2006, 276(3):230-241.
20. Morrell PL, Clegg MT. Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. Proceedings of the National Academy of Sciences 2007, 104(9):3289-3294.
21. Kilian B, Özkan H, Pozzi C, Salamini F. Domestication of the Triticeae in the Fertile Crescent. Genetics and Genomics of the Triticeae 2009, 7:81-119. Springer New York, Muehlbauer G, Feuillet C.
22. Hayes P, Szucs P. Disequilibrium and association in barley: thinking outside the glass. Proc Natl Acad Sci USA 2006, 103(49):18385-18386.
23. Schulte D, Close TJ, Graner A, Langridge P, Matsumoto T, Muehlbauer G, Sato K, Schulman AH, Waugh R, Wise RP, et al. The International Barley Sequencing Consortium--At the Threshold of Efficient Access to the Barley Genome. Plant Physiology 2009, 149(1):142-147.
24. Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR, Roose ML, Svensson JT, Stein N, Varshney RK, Marshall DF, et al. Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc Natl Acad Sci USA 2006, 103(49):18656-18661.
25. Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, et al. A high-density consensus map of barley linking DArT markers to SSR RFLP and STS loci and agricultural traits. BMC Genomics 2006, 7:206.
26. Close TJBP, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szu{double acute}cs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R. Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 2009, 10:582.
27. Haseneyer G, Stracke S, Piepho HP, Sauer S, Geiger HH, Graner A. DNA polymorphisms and haplotype patterns of transcription factors involved in barley endosperm development are associated with key agronomic traits. BMC Plant Biology 2010, 10.
28. Cockram J, White J, Leigh FJ, Lea VJ, Chiapparino E, Laurie DA, Mackay IJ, Powell W, O'Sullivan DM. Association mapping of partitioning loci in barley. BMC Genet 2008, 9:16.
29. Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WTB, Macaulay M, MacKenzie K, Simpson C, Fuller J, Bonar N, et al. INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat Genet 2011, 43(2):169-172.
30. Waugh R, Jannink JL, Muehlbauer GJ, Ramsay L. The emergence of whole genome association scans in barley. Curr Opin Plant Biol 2009, 12(2):218-222.
31. Michalek T, Graner V. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). TAG Theoretical and Applied Genetics 2003, 106(3):411-422.
32. Breseghello F, Sorrells ME. Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 2006, 172(2):1165-1177.
33. Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES. Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 2009, 21(8):2194-2202.
34. Malosetti M, van der Linden CG, Vosman B, van Eeuwijk FA. A Mixed-Model Approach to Association Mapping Using Pedigree Information With an Illustration of Resistance to Phytophthora infestans in Potato. Genetics 2007, 175(2):879-889.
35. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P. Association mapping in structured populations. American Journal of Human Genetics 2000, 67(1):170-181.
36. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 2006, 38(2):203-208.
37. Stich B, Melchinger AE. Comparison of mixed-model approaches for association mapping in rapeseed, potato, sugar beet, maize, and Arabidopsis. BMC Genomics 2009, 10.
38. Haseneyer G, Stracke S, Paul C, Einfeldt C, Broda A, Piepho HP, Graner A, Geiger HH. Population structure and phenotypic variation of a spring barley world collection set up for association studies. Plant Breeding 2010, 129(3):271-279.
39. Knüpffer H, van Hintum T. Chapter 13 Summarised diversity--the Barley Core Collection. Developments in Plant Genetics and Breeding 2003, 7:259-267. Elsevier, von Bothmer R, van Hintum T, Knüpffer H, Kazuhiro S.
40. Naumann C, Bassler R. VDLUFA-Methodenbuch III: Die Chemische Untersuchung von Futtermitteln, 5. 2004, Ergänzungslieferung, Darmstadt, VDLUFA.
41. Payne RW, Murray DA, Harding SA, Baird DB, Soutar DM. GenStat for Windows (9th Edition) Introduction. VSN International, Hemel Hempstead. 2006,
42. Fan JB, Gunderson KL, Bibikova M, Yeakley JM, Chen J, Wickham Garcia E, Lebruska LL, Laurent M, Shen R, Barker D. Illumina Universal Bead Arrays. Methods in Enzymology 2006, 410:57-73. Academic Press, Alan K, Brian O.
43. Fan JB, Oliphant A, Shen R, Kermani BG, Garcia F, Gunderson KL, Hansen M, Steemers F, Butler SL, Deloukas P, et al. Highly parallel SNP genotyping. Cold Spring Harbor Symp Quant Biol 2003, 68:69-78.
44. Liu K, Muse SV. PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 2005, 21(9):2128-2129.
45. Nei M. Genetic Distance between Populations. Am Nat 1972, 106(949):283.
46. Falush D, Stephens M, Pritchard JK. Inference of Population Structure Using Multilocus Genotype Data: Linked Loci and Correlated Allele Frequencies. Genetics 2003, 164(4):1567-1587.
47. Pritchard J, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
48. Perrier X, Jacquemound-Collet JP. DARwin Software. 2006, , http://darwin.cirad.fr/darwin
49. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21(2):263-265.
50. Weir BS. Genetic Data Analysis II: Methods for Discrete Population Genetic Data. 1996, Sinauer Associates, Sunderland, Massachusetts.
51. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 2007, 23(19):2633-2635.
52. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E. Efficient control of population structure in model organism association mapping. Genetics 2008, 178(3):1709-1723.
53. Stich B, Mohring J, Piepho HP, Heckenberger M, Buckler ES, Melchinger AE. Comparison of mixed-model approaches for association mapping. Genetics 2008, 178(3):1745-1754.
54. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate - a Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc B Met 1995, 57(1):289-300.
55. Chan EK, Rowe HC, Kliebenstein DJ. Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics 2010, 185(3):991-1007.
56. Smith A, Cullis B, Gilmour A. The Analysis of Crop Variety Evaluation Data in Australia. Australian & New Zealand Journal of Statistics 2001, 43(2):129-145.
57. Malysheva-Otto LV, Ganal MW, Roder MS. Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genet 2006, 7:6.
58. Zhang LY, Marchand S, Tinker NA, Belzile F. Population structure and linkage disequilibrium in barley assessed by DArT markers. Theor Appl Genet 2009, 119(1):43-52.
59. Maccaferri M, Sanguineti MC, Noli E, Tuberosa R. Population structure and long-range linkage disequilibrium in a durum wheat elite collection. Mol Breeding 2005, 15(3):271-290.
60. Pourkheirandish M, Komatsuda T. The importance of barley genetics and domestication in a global perspective. Ann Bot 2007, 100(5):999-1008.
61. Wang G, Schmalenbach I, von Korff M, Leon J, Kilian B, Rode J, Pillen K. Association of barley photoperiod and vernalization genes with QTLs for flowering time and agronomic traits in a BC2DH population and a set of wild barley introgression lines. Theor Appl Genet 2010, 120(8):1559-1574.
62. Laurie DA, Pratchett N, Snape JW, Bezant JH. RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter x spring barley (Hordeum vulgare L.) cross. Genome 1995, 38(3):575-585.
63. Faure S, Higgins J, Turner A, Laurie DA. The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 2007, 176(1):599-609.
64. Comadran J, Russell JR, Booth A, Pswarayi A, Ceccarelli S, Grando S, Stanca AM, Pecchioni N, Akar T, Al-Yassin A, et al. Mixed model association scans of multi-environmental trial data reveal major loci controlling yield and yield related traits in Hordeum vulgare in Mediterranean environments. Theoretical and Applied Genetics 2011, 122(7):1363-1373.
65. Griffiths S, Dunford RP, Coupland G, Laurie DA. The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 2003, 131(4):1855-1867.
66. Qi X, Niks RE, Stam P, Lindhout P. Identification of QTLs for partial resistance to leaf rust (Puccinia hordei) in barley. Theoretical and Applied Genetics 1998, 96(8):1205-1215.
67. Marquez-Cedillo LA, Hayes PM, Kleinhofs A, Legge WG, Rossnagel BG, Sato K, Ullrich SE, Wesenberg DM, Proj NABGM. QTL analysis of agronomic traits in barley based on the doubled haploid progeny of two elite North American varieties representing different germplasm groups. Theoretical and Applied Genetics 2001, 103(4):625-637.
68. Gottwald S, Stein N, Borner A, Sasaki T, Graner A. The gibberellic-acid insensitive dwarfing gene sdw3 of barley is located on chromosome 2HS in a region that shows high colinearity with rice chromosome 7L. Mol Genet Genomics 2004, 271(4):426-436.
69. Hayes PM, Liu BH, Knapp SJ, Chen F, Jones B, Blake T, Franckowiak J, Rasmusson D, Sorrells M, Ullrich SE, et al. Quantitative Trait Locus Effects and Environmental Interaction in a Sample of North-American Barley Germplasm. Theoretical and Applied Genetics 1993, 87(3):392-401.
70. Jia QJ, Zhang XQ, Westcott S, Broughton S, Cakir M, Yang JM, Lance R, Li CD. Expression level of a gibberellin 20-oxidase gene is associated with multiple agronomic and quality traits in barley. Theoretical and Applied Genetics 2011, 122(8):1451-1460.
71. Yin X, Stam P, Dourleijn CJ, Kropff MJ. AFLP mapping of quantitative trait loci for yield-determining physiological characters in spring barley. Theoretical and Applied Genetics 1999, 99(1-2):244-253.
72. Pillen K, Zacharias A, Leon J. Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 2003, 107(2):340-352.
73. von Korff M, Wang H, Leon J, Pillen K. AB-QTL analysis in spring barley: II. Detection of favourable exotic alleles for agronomic traits introgressed from wild barley (H-vulgare ssp spontaneum). Theoretical and Applied Genetics 2006, 112(7):1221-1231.
74. von Korff M, Grando S, Del Greco A, This D, Baum M, Ceccarelli S. Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley. Theoretical and Applied Genetics 2008, 117(5):653-669.
75. Szücs P, Blake VC, Bhat PR, Chao S, Close TJ, Cuesta-Marcos A, Muehlbauer GJ, Ramsay L, Waugh R, Hayes PM. An Integrated Resource for Barley Linkage Map and Malting Quality QTL Alignment. Plant Gen 2009, 2(2):134-140.
76. Abdel-Haleem H, Bowman J, Giroux M, Kanazin V, Talbert H, Surber L, Blake T. Quantitative trait loci of acid detergent fiber and grain chemical composition in hulled × hull-less barley population. Euphytica 2010, 172(3):405-418.
77. Mather DE, Tinker NA, LaBerge DE, Edney M, Jones BL, Rossnagel BG, Legge WG, Briggs KG, Irvine RB, Falk DE, et al. Regions of the genome that affect grain and malt quality in a North American two-row barley cross. Crop Sci 1997, 37(2):544-554.
78. Oziel A, Hayes PM, Chen FQ, Jones B. Application of quantitative trait locus mapping to the development of winter-habit malting barley. Plant Breeding 1996, 115(1):43-51.
79. Rafalski JA. Association genetics in crop improvement. Current Opinion in Plant Biology 2010, 13(2):174-180.
80. Hamblin MT, Close TJ, Bhat PR, Chao SM, Kling JG, Abraham KJ, Blake T, Brooks WS, Cooper B, Griffey CA, et al. Population Structure and Linkage Disequilibrium in US Barley Germplasm: Implications for Association Mapping. Crop Sci 2010, 50(2):556-566.
81. Melchinger AE, Graner A, Singh M, Messmer MM. Relationships among European Barley Germplasm .1. Genetic Diversity among Winter and Spring Cultivars Revealed by RFLPS. Crop Sci 1994, 34(5):1191-1199.
82. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler E. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 2001, 98(20):11479-11484.
83. Stracke S, Presterl T, Stein N, Perovic D, Ordon F, Graner A. Effects of introgression and recombination on haplotype structure and linkage disequilibrium surrounding a locus encoding Bymovirus resistance in barley. Genetics 2007, 175(2):805-817.
84. Kraakman AT, Niks RE, Van den Berg PM, Stam P, Van Eeuwijk FA. Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 2004, 168(1):435-446.
85. Comadran J, Thomas WT, van Eeuwijk FA, Ceccarelli S, Grando S, Stanca AM, Pecchioni N, Akar T, Al-Yassin A, Benbelkacem A, et al. Patterns of genetic diversity and linkage disequilibrium in a highly structured Hordeum vulgare association-mapping population for the Mediterranean basin. Theor Appl Genet 2009, 119(1):175-187.
86. Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, et al. Mixed linear model approach adapted for genome-wide association studies. Nature Genetics 2010, 42(4):355-360.
87. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 2006, 38(8):904-909.
88. Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, et al. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci USA 2007, 104(4):1424-1429.
89. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, et al. The genetic architecture of maize flowering time. Science 2009, 325(5941):714-718.
90. Zhang J, Li Z, Zhang CH. Analysis of dwarfing genes in Zhepi 1 and Aizao 3: Two dwarfing gene donors in barley breeding in China. Can J Plant Sci 2007, 87(1):93-96.
91. Kleinhofs A. Integrating barley RFLP and classical marker maps. Barley Genet News letter 1997, 27:105-112.
92. Rohde W, Becker D, Salamini F. Structural analysis of the waxy locus from Hordeum vulgare. Nucleic Acids Res 1988, 16(14B):7185-7186.
93. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. Finding the missing heritability of complex diseases. Nature 2009, 461(7265):747-753.
94. Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ. Association mapping of spot blotch resistance in wild barley. Mol Breed 2010, 26(2):243-256.
95. Maher B. Personal genomes: The case of the missing heritability. Nature 2008, 456(7218):18-21.
96. Visscher PM. Sizing up human height variation. Nat Genet 2008, 40(5):489-490.
97. Frazer KA, Murray SS, Schork NJ, Topol EJ. Human genetic variation and its contribution to complex traits. Nat Rev Genet 2009, 10(4):241-251.
98. Gibson G. Hints of hidden heritability in GWAS. Nat Genet 2010, 42(7):558-560.
99. Hall D, Tegstrom C, Ingvarsson PK. Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genomics 2010, 9(2):157-165.
100. Blott S, Kim JJ, Moisio S, Schmidt-Kuntzel A, Cornet A, Berzi P, Cambisano N, Ford C, Grisart B, Johnson D, et al. Molecular Dissection of a Quantitative Trait Locus: A Phenylalanine-to-Tyrosine Substitution in the Transmembrane Domain of the Bovine Growth Hormone Receptor Is Associated With a Major Effect on Milk Yield and Composition. Genetics 2003, 163(1):253-266.
101. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 2010, 6:e1000940.
102. Mott R, Flint J. Simultaneous Detection and Fine Mapping of Quantitative Trait Loci in Mice Using Heterogeneous Stocks. Genetics 2002, 160(4):1609-1618.
103. Mayer KFX, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, et al. Unlocking the Barley Genome by Chromosomal and Comparative Genomics. Plant Cell 2011, 23(4):1249-1263.
104. Cockram J, White J, Zuluaga DL, Smith D, Comadran J, Macaulay M, Luo ZW, Kearsey MJ, Werner P, Harrap D, et al. Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci USA 2010, 107(50):21611-21616.