Association genetics of complex traits in plants

New Phytologist

Volumn 189, Issue 4, 2011, Pages 909-922

  Ingvarsson, Pär K ^a   Street, Nathaniel R ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

Association mapping; Complex traits; Genetic architecture; Genotyping; Phenotyping

Indexed keywords

CLONAL ORGANISM; FUTURE PROSPECT; GENE EXPRESSION; GENETIC STRUCTURE; GENOME; GENOTYPE; HERITABILITY; LIFE HISTORY TRAIT; MUTATION; PHENOTYPE; POPULATION SIZE;

GENETIC ASSOCIATION; GENETICS; GENOMICS; GENOTYPE; PLANT; QUANTITATIVE TRAIT; REPRODUCIBILITY; REVIEW;

GENETIC ASSOCIATION STUDIES; GENOMICS; GENOTYPE; PLANTS; QUANTITATIVE TRAIT, HERITABLE; REPRODUCIBILITY OF RESULTS;

EID: 79551537130     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03593.x     Document Type: Review

References (108)

1. Akey JM, Zhang K, Xiong M, Doris P, Jin L. 2001. The effect that genotyping errors have on the robustness of common linkage-disequilibrium measures. The American Journal of Human Genetics 68: 1447-1456.
2. Alcázar R, García AV, Parker JE, Reymond M. 2009. Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proceedings of the National Academy of Sciences, USA 106: 334-339.
3. Alimonti A, Carracedo A, Clohessy JG, Trotman LC, Nardella C, Egia A, Salmena L, Sampieri K, Haveman WJ, Brogi E et al. 2010. Subtle variations in PTEN dose determine cancer susceptibility. Nature Genetics 42: 454-458.
4. Andersen JR, Schrag T, Melchinger AE, Zein I, Lübberstedt T. 2005. Validation of Dwarf8 polymorphisms associated with flowering time in elite European inbred lines of maize (Zea mays L.). TAG Theoretical and Applied Genetics 111: 206-217.
5. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
6. Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C et al. 2005. Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genetics 1: e60.
7. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT et al. 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627-631.
8. Baranzini SE, Galwey NW, Wang J, Khankhanian P, Lindberg R, Pelletier D, Wu W, Uitdehaag BMJ, Kappos L, Consortium G et al. 2009. Pathway and network-based analysis of genome-wide association studies in multiple sclerosis. Human Molecular Genetics 18: 2078-2090.
9. Beavis WD. 1994. The power and deceit of QTL experiments: lessons from comparitive QTL studies. In: Proceedings of the forty-ninth annual Corn & Sorghum industry research conference. Washington, DC, USA: American Seed Trade Association, 250-266.
10. Bolton KL, Tyrer J, Song H, Ramus SJ, Notaridou M, Jones C, Sher T, Gentry-Maharaj A, Wozniak E, Tsai Y et al. 2010. Common variants at 19p13 are associated with susceptibility to ovarian cancer. Nature Genetics 42: 880-884.
11. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F. 2010. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genetics 6: e1000940.
12. Camus-Kulandaivelu L, Veyrieras J, Madur D, Combes V, Fourmann M, Barraud S, Dubreuil P, Gouesnard B, Manicacci D, Charcosset A. 2006. Maize adaptation to temperate climate: relationship between population structure and polymorphism in the Dwarf8 gene. Genetics 172: 2449-2463.
13. Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25-36.
14. Chanock SJ, Manolio T, Boehnke M, Boerwinkle E, Hunter DJ, Thomas G, Hirschhorn JN, Abecasis G, Altshuler D, Bailey-Wilson JE et al. 2007. Replicating genotype-phenotype associations. Nature 447: 655-660.
15. Clark AG, Hubisz MJ, Bustamante CD, Williamson SH, Nielsen R. 2005. Ascertainment bias in studies of human genome-wide polymorphism. Genome Research 15: 1496-1502.
16. Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, Warthmann N, Hu TT, Fu G, Hinds DA et al. 2007. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317: 338-342.
17. Doerge RW. 2002. Mapping and analysis of quantitative trait loci in experimental populations. Nature Reviews Genetics 3: 43-52.
18. Drost DR, Benedict CI, Berg A, Novaes E, Novaes CR, Yu Q, Dervinis C, Maia JM, Yap J, Miles B et al. 2010. Diversification in the genetic architecture of gene expression and transcriptional networks in organ differentiation of Populus. Proceedings of the National Academy of Sciences, USA 107: 8492-8497.
19. Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, St. Clair JB, Neale DB. 2009. Association genetics of coastal Douglas Fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182: 1289-1302.
20. Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX, Purugganan MD. 2009. Candidate gene association mapping of Arabidopsis flowering time. Genetics 183: 325-335.
21. Ehrenreich IM, Stafford PA, Purugganan MD. 2007. The genetic architecture of shoot branching in Arabidopsis thaliana: a comparative assessment of candidate gene associations vs. quantitative trait locus mapping. Genetics 176: 1223-1236.
22. Emerson JJ, Hsieh L-CC, Sung H-MM, Wang T-YY, Huang C-JJ, Lu HH-SH, Lu M-YJY, Wu S-HH, Li W-HH. 2010. Natural selection on cis and trans regulation in yeasts. Genome Research 20: 826-836.
23. Erdmann J, Groszhennig A, Braund PS, Konig IR, Hengstenberg C, Hall AS, Linsel-Nitschke P, Kathiresan S, Wright B, Tregouet D et al. 2009. New susceptibility locus for coronary artery disease on chromosome 3q22.3. Nature Genetics 41: 280-282.
24. Fisher RA. 1918. On the correlation between relatives on the supposition of Mendelian inheritance. Philosophical Transactions of the Royal Society of Edinburgh 52: 399-433.
25. Flint J, Mackay TF. 2009. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Research 19: 723-733.
26. Frayling TM. 2007. Genome-wide association studies provide new insights into type 2 diabetes aetiology. Nature Reviews Genetics 8: 657-662.
27. Ganal MW, Altmann T, Röder MS. 2009. SNP identification in crop plants. Current Opinion in Plant Biology 12: 211-217.
28. Gazzani S, Gendall AR, Lister C, Dean C. 2003. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiology 132: 1107-1114.
29. Gilad Y, Pritchard JK, Thornton K. 2009. Characterizing natural variation using next-generation sequencing technologies. Trends in Genetics 25: 463-471.
30. Gilad Y, Rifkin S, Pritchard J. 2008. Revealing the architecture of gene regulation: the promise of eQTL studies. Trends in Genetics 24: 408-415.
31. Goldstein DB. 2009. Common genetic variation and human height. New England Journal of Medicine 360: 1696-1698.
32. Gonzalez-Martinez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB. 2007. Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175: 399-409.
33. Gutierrez-Gonzalez J, Wu X, Gillman J, Lee J, Zhong R, Yu O, Shannon G, Ellersieck M, Nguyen H, Sleper D. 2010. Intricate environment-modulated genetic networks control isoflavone accumulation in soybean seeds. BMC Plant Biology 10: 105.
34. Hall D, Tegström C, Ingvarsson PK. 2010. Using association mapping to dissect the genetic basis of complex traits in plants. Briefings in Functional Genomics 9: 157-165.
35. Hardy J, Singleton A. 2009. Genome wide association studies and human disease. New England Journal of Medicine 360: 1759-1768.
36. He X, Qian W, Wang Z, Li Y, Zhang J. 2010. Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks. Nature Genetics 42: 272-276.
37. Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
38. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P et al. 2009. The genome of the cucumber, Cucumis sativus L. Nature Genetics 41: 1275-1281.
39. Imelfort M, Duran C, Batley J, Edwards D. 2009. Discovering genetic polymorphisms in next-generation sequencing data. Plant Biotechnology Journal 7: 312-317.
40. Imelfort M, Edwards D. 2009. De novo sequencing of plant genomes using second-generation technologies. Briefings in Bioinformatics 10: 609-618.
41. Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S. 2008. Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European Aspen (Populus tremula, Salicaceae). Genetics 178: 2217-2226.
42. International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. Nature 436: 793-800.
43. Jansen RC, Nap JP. 2001. Genetical genomics: the added value from segregation. Trends in Genetics 17: 388-391.
44. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
45. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E. 2008. Efficient control of population structure in model organism association mapping. Genetics 178: 1709-1723.
46. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, Waszak SM, Habegger L, Rozowsky J, Shi M, Urban AE et al. 2010. Variation in transcription factor binding among humans. Science 328: 232-235.
47. Keurentjes JJB, Fu J, Terpstra IR, Garcia JM, van den Ackerveken G, Snoek LB, Peeters AJM, Vreugdenhil D, Koornneef M, Jansen RC. 2007. Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proceedings of the National Academy of Sciences, USA 104: 1708-1713.
48. Kirst M, Basten CJ, Myburg AA, Zeng ZB, Sederoff RR. 2005. Genetic architecture of transcript-level variation in differentiating xylem of a Eucalyptus hybrid. Genetics 169: 2295-2303.
49. Kirst M, Myburg AA, De Leon JPG, Kirst ME, Scott J, Sederoff R. 2004. Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of Eucalyptus. Plant Physiology 135: 2368-2378.
50. Kliebenstein DJ. 2010. Systems biology uncovers the foundation of natural genetic diversity. Plant Physiology 152: 480-486.
51. Koornneef M, Alonso-Blanco C, Vreugdenhil D. 2004. Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review of Plant Biology 55: 141-172.
52. Kroymann J, Mitchell-Olds T. 2005. Epistasis and balanced polymorphism influencing complex trait variation. Nature 435: 95-98.
53. Lander ES, Botstein D. 1989. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121: 185-199.
54. Lee I, Ambaru B, Thakkar P, Marcotte EM, Rhee SY. 2010a. Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nature Biotechnology 28: 149-156.
55. Lee I, Lehner B, Vavouri T, Shin J, Fraser AG, Marcotte EM. 2010b. Predicting genetic modifier loci using functional gene networks. Genome Research 20: 1143-1153.
56. Long AD, Langley CH. 1999. The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Research 9: 720-731.
57. Lucioni PJ, Ayroles J, Chambers MM, Jordan K, Leips J, Mackay T, De Luca M. 2010. Systems genetics analysis of body weight and energy metabolism traits in Drosophila melanogaster. BMC Genomics 11: 297.
58. Lynch M, Walsh B. 1998. Genetics and analysis of quantitative traits. Sunderland, MA, USA: Sinauer Associates.
59. Ma D, Salyakina D, Jaworski JM, Konidari I, Whitehead PL, Andersen AN, Hoffman JD, Slifer SH, Hedges DJ, Cukier HN et al. 2009. A genome-wide association study of autism reveals a common novel risk locus at 5p14.1. Annals of Human Genetics 73: 263-273.
60. Mackay TFC, Stone EA, Ayroles JF. 2009. The genetics of quantitative traits: challenges and prospects. Nature Reviews Genetics 10: 565-577.
61. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A et al. 2009. Finding the missing heritability of complex diseases. Nature 461: 747-753.
62. Mauricio R. 2001. Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology. Nature Reviews Genetics 2: 370-381.
63. McCarroll SA, Altshuler DM. 2007. Copy-number variation and association studies of human disease. Nature Genetics 39: S37-S42.
64. McClellan J, King M-C. 2010. Genetic heterogeneity in human disease. Cell 141: 210-217.
65. McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ. 2010. Regulatory divergence in drosophila revealed by mRNA-Seq. Genome Research 20: 816-825.
66. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C et al. 2009. Genetic properties of the maize nested association mapping population. Science 325: 737-740.
67. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
68. Montgomery SB, Sammeth M, Gutierrez-Arcelus M, Lach RP, Ingle C, Nisbett J, Guigo R, Dermitzakis ET. 2010. Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464: 773-777.
69. Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES. 2009. Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21: 2194-2202.
70. Naukkarinen J, Surakka I, Pietiläinen KH, Rissanen A, Salomaa V, Ripatti S, Yki-Järvinen H, van Duijn CM, Wichmann Kaprio J, Taskinen M-R et al. 2010. Use of genome-wide expression data to mine the "gray zone" of GWA studies leads to novel candidate obesity genes. PLoS Genetics 6: e1000976.
71. Neale DB, Savolainen O. 2004. Association genetics of complex traits in conifers. Trends in Plant Science 9: 325-330.
72. Nicolae DL, Gamazon E, Zhang W, Duan S, Dolan ME, Cox NJ. 2010. Trait-associated SNPs are more likely to be eQTLs: Annotation to enhance discovery from GWAS. PLoS Genetics 6: e1000888.
73. Nordborg M, Tavaré S. 2002. Linkage disequilibrium: what history has to tell us. Trends in Genetics 18: 83-90.
74. Nordborg M, Weigel D. 2008. Next-generation genetics in plants. Nature 456: 720-723.
75. Noyes H, Agaba M, Anderson S, Archibald A, Brass A, Gibson J, Hall L, Hulme H, Oh S, Kemp S. 2010. Genotype and expression analysis of two inbred mouse strains and two derived congenic strains suggest that most gene expression is trans regulated and sensitive to genetic background. BMC Genomics 11: 361.
76. Orr HA, Coyne JA. 1992. The genetics of adaptation: a reassessment. The American Naturalist 140: 725.
77. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D. 2008. Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Research 18: 2024-2033.
78. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G et al. 2009. The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556.
79. Pearson TA, Manolio TA. 2008. How to interpret a genome-wide association study. JAMA 299: 1335-1344.
80. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F et al. 1999. 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400: 256-261.
81. Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE, Nkadori E, Veyrieras J-BB, Stephens M, Gilad Y, Pritchard JK. 2010. Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464: 768-772.
82. Rae AM, Street NRRobinsonKM, Harris N, Taylor G. 2009. Five QTL hotspots for yield in short rotation coppice bioenergy poplar: the Poplar Biomass Loci. BMC Plant Biology 9: 23.
83. Scarcelli N, Cheverud JM, Schaal BA, Kover PX. 2007. Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proceedings of the National Academy of Sciences, USA 104: 16986-16991.
84. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL et al. 2010. Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
85. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
86. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C. 2005. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiology 138: 1163-1173.
87. Simon SA, Zhai J, Nandety RS, McCormick KP, Zeng J, Mejia D, Meyers BC. 2009. Short-read sequencing technologies for transcriptional analyses. Annual Review of Plant Biology 60: 305-333.
88. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D, Paisan-Ruiz C, Lichtner P, Scholz SW, Hernandez DG et al. 2009. Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nature Genetics 41: 1308-1312.
89. Skot L, Humphreys J, Humphreys MO, Thorogood D, Gallagher J, Sanderson R, Armstead IP, Thomas ID. 2007. Association of candidate genes with flowering time and water-soluble carbohydrate content in Lolium perenne (L.). Genetics 177: 535-547.
90. Sobel E, Papp JC, Lange K. 2002. Detection and integration of genotyping errors in statistical genetics. The American Journal of Human Genetics 70: 496-508.
91. 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.
92. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES. 2001. Dwarf8 polymorphisms associate with variation in flowering time. Nature Genetics 28: 286-289.
93. Tian Z, Qian Q, Liu Q, Yan M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D et al. 2009. Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proceedings of the National Academy of Sciences, USA 106: 21760-21765.
94. Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV. 2010. Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genetics 42: 260-263.
95. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
96. Varshney RK, Nayak SN, May GD, Jackson SA. 2009. Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends in Biotechnology 27: 522-530.
97. Visscher PM. 2008. Sizing up human height variation. Nature Genetics 40: 489-490.
98. Walsh T, King M-C. 2007. Ten genes for inherited breast cancer. Cancer Cell 11: 103-105.
99. Weigel D, Mott R. 2009. The 1001 genomes project for Arabidopsis thaliana. Genome Biology 10: 107.
100. West MA, Kim K, Kliebenstein DJ, van Leeuwen H, Michelmore RW, Doerge RW, St Clair DA. 2007. Global eQTL mapping reveals the complex genetic architecture of transcript-level variation in Arabidopsis. Genetics 175: 1441-1450.
101. Wilson LM, Whitt SR, Ibanez AM, Rocheford TR, Goodman MM, Buckler ES. 2004. Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16: 2719-2733.
102. Xu S. 2003. Theoretical basis of the Beavis effect. Genetics 165: 2259-2268.
103. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, Madden PA, Heath AC, Martin NG, Montgomery GW et al. 2010. Common SNPs explain a large proportion of the heritability for human height. Nature Genetics 42: 565-569.
104. Yang X, Deignan JL, Qi H, Zhu J, Qian S, Zhong J, Torosyan G, Majid S, Falkard B, Kleinhanz RR et al. 2009. Validation of candidate causal genes for obesity that affect shared metabolic pathways and networks. Nature Genetics 41: 415-423.
105. Yu J, Holland JB, McMullen MD, Buckler ES. 2008. Genetic design and statistical power of nested association mapping in maize. Genetics 178: 539-551.
106. Yu J, Pressoir G, Briggs WH, Vroh BiI, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB et al. 2006. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38: 203-208.
107. Zhang X, Huang S, Zou F, Wang W. 2010. Team: efficient two-locus epistasis tests in human genome-wide association study. Bioinformatics 26: i217-i227.
108. Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P et al. 2007. An Arabidopsis example of association mapping in structured samples. PLoS Genetics 3: e4.