Association studies including genotype by environment interactions: Prospects and limits

BMC Genetics

Volumn 15, Issue , 2014, Pages

  Saïdou, Abdoul Aziz ^a,b,c,d,e   Thuillet, Anne Céline ^a   Couderc, Marie ^a   Mariac, Cédric ^a,b   Vigouroux, Yves ^a  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^c UNIVERSITÉ ABDOU MOUMOUNI   (Niger)

^d MONTPELLIER SUPAGRO   (France)

^e CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Association study; G E; Model selection; PHYC; Power simulation; REML; Vgt1

Indexed keywords

ARTICLE; EFFECT SIZE; FIELD EXPERIMENT; GENE FREQUENCY; GENE INTERACTION; GENE LOCUS; GENE MAPPING; GENETIC ASSOCIATION; GENETIC TRAIT; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE PHENOTYPE CORRELATION; HERITABILITY; MAIZE; NONHUMAN; PEARL MILLET; PLANT ENVIRONMENT INTERACTION; PLANT GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL;

PENNISETUM GLAUCUM; ZEA MAYS;

GENE-ENVIRONMENT INTERACTION; GENETIC ASSOCIATION STUDIES; GENETIC PLEIOTROPY; GENOTYPE; LINEAR MODELS; MODELS, GENETIC; PANICUM; POLYMORPHISM, SINGLE NUCLEOTIDE; ZEA MAYS;

EID: 84891518323     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-15-3     Document Type: Article

References (55)

1. 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, 21:2194-2202. 10.1105/tpc.109.068437, 2751942, 19654263.
2. Nordborg M, Weigel D. Next-generation genetics in plants. Nature 2008, 456:720-723. 10.1038/nature07629, 19079047.
3. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P. Association mapping in structured populations. Am J Hum Genet 2000, 67:170-181. 10.1086/302959, 1287075, 10827107.
4. Pritchard JK, Stephens M, Donnelly M. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959. 1461096, 10835412.
5. Gao H, Williamson S, Bustamante CD. An MCMC approach for the joint inference of population structure and inbreeding rate from multi-locus genotype data. Genetics 2007, 176:1635-1651. 10.1534/genetics.107.072371, 1931536, 17483417.
6. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genoype data: linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587. 1462648, 12930761.
7. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 2007, 7(4):574-578. 10.1111/j.1471-8286.2007.01758.x, 1974779, 18784791.
8. Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 2009, 9:1322-1332. 10.1111/j.1755-0998.2009.02591.x, 3518025, 21564903.
9. Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet 2006, 2(12):e190. doi:10.1371/journal.pgen.0020190, 10.1371/journal.pgen.0020190, 1713260, 17194218.
10. Zhu C, Yu J. Nonmetric multidimensional scaling corrects for population structure in whole genome association studies. Genetics 2009, 182:875-888. 10.1534/genetics.108.098863, 2710166, 19414565.
11. Loiselle BA, Sork VL, Nason J, Graham C. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 1995, 82:1420-1425.
12. Hardy OJ, Vekemans X. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2002, 2:618-620.
13. Stich B, Mohring J, Piepho HP, Heckenberger M, Buckler ES, et al. Comparison of mixed-model approaches for association mapping. Genetics 2008, 178:1745-1754. 10.1534/genetics.107.079707, 2278052, 18245847.
14. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, et al. Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 2001, 28:286-289. 10.1038/90135, 11431702.
15. Zhang Y-M, Mao Y, Xie C, Smith H, Luo L, Xu S. Mapping quantitative trait loci using naturally occurring genetic variance among commercial inbred lines among maize (Zea mays L.). Genetics 2005, 169:2267-2275. 10.1534/genetics.104.033217, 1449576, 15716509.
16. Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, et al. A unified mixed-model method for association studies that accounts for multiple levels of relatedness. Nat Genet 2006, 38:203-208. 10.1038/ng1702, 16380716.
17. Saïdou AA, Mariac C, Luong V, Pham JL, Bezancon G, Vigouroux Y. Association studies identify natural variation at PHYC linked to flowering time and morphological variation in pearl millet. Genetics 2009, 182:899-910. 10.1534/genetics.109.102756, 2710168, 19433627.
18. Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES. Mixed linear model approach adapted for genome-wide association studies. Nat Genet 2010, 42:355-360. 10.1038/ng.546, 2931336, 20208535.
19. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 2010, 465:627-631. 10.1038/nature08800, 3023908, 20336072.
20. 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(5):e1000940. doi:10.1371/journal.pgen.1000940, 10.1371/journal.pgen.1000940, 2865524, 20463887.
21. Zhu C, Gore M, Buckler ES, Yu J. Status and prospects of association mapping in plants. Plant Genome 2008, 1:5-20.
22. Hall D, Tegström C, Ingvarsson PK. Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genomics 2010, 9(2):157-165. 10.1093/bfgp/elp048, 20053815.
23. Rafalski JA. Association genetics in crop improvement. Curr Opin Plant Biol 2010, 13:1-7. 10.1016/j.pbi.2009.12.001, 20047852.
24. Stracke S, Haseneyer G, Veyrieras JB, Geiger HH, Sauer S, Graner A, Piepho HP. Association studies reveals gene action and interactions in the determination of flowering time in barley. Theor Appl Genet 2009, 118:259-273. 10.1007/s00122-008-0896-y, 18830577.
25. Zhang N, Gur A, Gibon Y, Sulpice R, Flint-Garcia S, McMullen MD, Stitt M, Buckler ES. Genetic analysis of central carbon metabolism unveils an amino acid substitution that alters maize NAD-dependent isocitrate dehydrogenase activity. PLoS One 2010, 5(4):e9991. doi:10.1371/journal.pone.0009991, 10.1371/journal.pone.0009991, 2848677, 20376324.
26. Li L, Paulo MJ, van Eeuwijk F. Statistical epistasis between candidate gene alleles for complex tuber traits in an association mapping population of tetraploid potato. Theor Appl Genet 2010, 121:1303-1310. 10.1007/s00122-010-1389-3, 2955219, 20603706.
27. Wang D, Eskridge KM, Crossa J. Identifying QTLs and epistasis in structured plant populations using adaptive mixed LASSO. J Agr Biol Environ Stat 2010, 16:170-184.
28. Lü HY, Liu XF, Wei SP, Zhang YM. Epistatic association analysis in homozygous crop cultivars. PLoS One 2011, 6(3):e17773. 10.1371/journal.pone.0017773, 3058038, 21423630.
29. Falconer DS, Mackay TFC. Introduction to Quantitative Genetics 1996, Harlow, UK: Addison-Wesley Longman, 4.
30. Jannink JL. Identifying quantitative trait locus by genetic background interactions in association studies. Genetics 2007, 176:553-561. 10.1534/genetics.106.062992, 1893042, 17179077.
31. Phillips PC. Epistasis - the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 2008, 9:855-867. 10.1038/nrg2452, 2689140, 18852697.
32. Sambandan D, Carbone MA, Anholt RRH, Mackay TFC. Phenotypic plasticity and genotype by environment interaction for olfactory behavior in Drosophila melanogaster. Genetics 2008, 179(2):1079-1088. 10.1534/genetics.108.086769, 2429861, 18505870.
33. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, et al. Genetic properties of the maize nested association mapping population. Science 2009, 325:737-740. 10.1126/science.1174320, 19661427.
34. Buckler ES, James BH, Bradbury PJ, Acharya CB, Brown PJ, et al. The genetic architecture of maize flowering time. Science 2009, 325:714-718. 10.1126/science.1174276, 19661422.
35. Uwatoko N, Onishi A, Ikeda Y, Kontani M, Sasaki A, Matsubara K, Itoh Y, Sano Y. Epistasis among the three major flowering time genes in rice: coordinate changes of photoperiod sensitivity, basic vegetative growth and optimum photoperiod. Euphytica 2008, 163:167-175.
36. El-Lithy M, Bentsink L, Hanhart CJ, Ruys GJ, Rovito D, et al. New Arabidopsis recombinant inbred line populations genotyped using SNPwave and their use for mapping flowering-time quantitative trait loci. Genetics 2006, 172:1867-1876. 1456291, 16361234.
37. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci U S A 2004, 101:15670-15675. 10.1073/pnas.0406232101, 524852, 15505218.
38. Kover PX, Valdar W, Trakalo J, Scarcelli N, Ehrenreich IM, et al. A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet 2009, 5(7):e1000551. 10.1371/journal.pgen.1000551, 2700969, 19593375.
39. Manolio TA, Collins FS, Cox NJ, et al. Finding the missing heritability of complex diseases. Nature 2009, 461:747-753. 10.1038/nature08494, 2831613, 19812666.
40. Kaprio J. Twins and the mystery of missing heritability: the contribution of gene-environment interactions. J Intern Med 2012, http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2796.2012.02587.x/pdf.
41. Jannink JL. QTL by genetic background interaction: predicting inbred progeny value. Euphytica 2008, 161:61-69.
42. Korte A, Vilhjálmsson BJ, Segura V, Platt A, Long Q, Nordborg M. A mixed-model approach for genome-wide association studies of correlated traits in structured populations. Nat Genet 2012, 44(9):1066-1071. 10.1038/ng.2376, 3432668, 22902788.
43. VSN International Ltd ASReml package for R (ASReml-R), version 2.0/32 2011, UK: VSN International Ltd, Hemel Hempstead, HP1 1ES, http://www.vsni.co.uk" http://www.vsni.co.uk, VSN International Ltd.
44. Mariac C, Luong V, Kapran I, Mamadou A, Sagnard F, et al. Diversity of wild and cultivated pearl millet accessions (Pennisetum glaucum [L.] R. Br.) in Niger assessed by microsatellite markers. Theor Appl Genet 2006, 114:49-58. 10.1007/s00122-006-0409-9, 17047913.
45. Allinne C, Mariac C, Vigouroux Y, Bezançon G, Couturon E, et al. Role of seed flow on the pattern and dynamics of pearl millet (Pennisetum glaucum [L.] R. Br.) genetic diversity assessed by AFLP markers: a study in south-western Niger. Genetica 2008, 133:167-178. 10.1007/s10709-007-9197-7, 17828466.
46. Flint-Garcia SA, Thuillet AC, Yu JM, Pressoir G, Romero SM, et al. Maize association population: a high resolution platform for QTL dissection. Plant J 2005, 44:1054-1064. 10.1111/j.1365-313X.2005.02591.x, 16359397.
47. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, et al. Efficient control of population structure in model organism association mapping. Genetics 2008, 178:1709-1723. 10.1534/genetics.107.080101, 2278096, 18385116.
48. Gilmour AR, Gogel BJ, Cullis BR, Thompson R. ASReml User Guide Release 2.0 2006, UK: VSN International Ltd, Hemel Hempstead, HP1 1ES.
49. Hurvich CM, Tsai CL. Regression and time series model selection in small samples. Biometrika 1989, 76:297-307.
50. Schwarz G. Estimating the dimension of a model. Annals Statistics 1978, 6:461-464.
51. Gurka MJ. Extending the Box-Cox transformation to the linear mixed model. J R Statist Soc A 2006, 169(2):273-288.
52. Mackay TFC, Anholt RRH. Ain't misbehavin'? Genotype-environment interactions and the genetics of behavior. Trends Genet 2007, 23:311-314. 10.1016/j.tig.2007.03.013, 17418441.
53. MacKay TFC, Stone E, Ayroles J. The genetics of quantitative traits: Challenges and prospects. Nat Rev Genet 2009, 10:565-577. 10.1038/nrg2612, 19584810.
54. Hoggart CJ, Whittaker JC, De Iorio M, Balding DJ. Simultaneous analysis of all SNPs in genome-wide and re-sequencing association studies. PLoS Genet 2008, 4(7):e1000130. 10.1371/journal.pgen.1000130, 2464715, 18654633.
55. Segura V, Vilhjálmsson BJ, Platt A, et al. An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 2012, 44(7):825-830. 10.1038/ng.2314, 3386481, 22706313.