From phenotypes to causal sequences: Using genome wide association studies to dissect the sequence basis for variation of plant development

Current Opinion in Plant Biology

Volumn 23, Issue , 2015, Pages 98-108

  Ogura, Takehiko ^a   Busch, Wolfgang ^a  

^a GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

GENETIC ASSOCIATION; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT; PLANT DEVELOPMENT;

BASE SEQUENCE; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DEVELOPMENT; PLANTS;

EID: 84912022905     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.11.008     Document Type: Review

References (114)

1. Slate J., Gratten J., Beraldi D., Stapley J., Hale M., Pemberton J.M. Gene mapping in the wild with SNPs: guidelines and future directions (vol 136, pg 97, 2009). Genetica 2010, 138:467.
2. Manolio T.A., Collins F.S., Cox N.J., Goldstein D.B., Hindorff L.A., Hunter D.J., McCarthy M.I., Ramos E.M., Cardon L.R., Chakravarti A., Cho J.H., Guttmacher A.E., Kong A., Kruglyak L., Mardis E., Rotimi C.N., Slatkin M., Valle D., Whittemore A.S., Boehnke M., Clark A.G., Eichler E.E., Gibson G., Haines J.L., Mackay T.F.C., McCarroll S.A., Visscher P.M. Finding the missing heritability of complex diseases. Nature 2009, 461:747-753.
3. Robinson M.R., Wray N.R., Visscher P.M. Explaining additional genetic variation in complex traits. Trends Genet 2014, 30:124-132.
4. Zhang H., Wang Z.P., Wang S.Z., Li H. Progress of genome wide association study in domestic animals. J Anim Sci Biotechnol 2012, 3.
5. Ingvarsson P.K., Street N.R. Association genetics of complex traits in plants. New Phytol 2011, 189:909-922.
6. Rafalski J.A. Association genetics in crop improvement. Curr Opin Plant Biol 2010, 13:174-180.
7. Nordborg M., Weigel D. Next-generation genetics in plants. Nature 2008, 456:720-723.
8. Weigel D. Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol 2012, 158:2-22.
9. Bergelson J., Roux F. Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 2010, 11:867-879.
10. Atwell S., Huang Y.S., Vilhjalmsson B.J., Willems G., Horton M., Li Y., Meng D.Z., Platt A., Tarone A.M., Hu T.T., Jiang R., Muliyati N.W., Zhang X., Amer M.A., Baxter I., Brachi B., Chory J., Dean C., Debieu M., de Meaux J., Ecker J.R., Faure N., Kniskern J.M., Jones J.D.G., Michael T., Nemri A., Roux F., Salt D.E., Tang C.L., Todesco M., Traw M.B., Weigel D., Marjoram P., Borevitz J.O., Bergelson J., Nordborg M. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 2010, 465:627-631.
11. Aranzana M.J., Kim S., Zhao K.Y., Bakker E., Horton M., Jakob K., Lister C., Molitor J., Shindo C., Tang C.L., Toomajian C., Traw B., Zheng H.G., Bergelson J., Dean C., Marjoram P., Nordborg M. Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 2005, 1:531-539.
12. 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.
13. Li Y., Huang Y., Bergelson J., Nordborg M., Borevitz J.O. Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2010, 107:21199-21204.
14. Brachi B., Villoutreix R., Faure N., Hautekeete N., Piquot Y., Pauwels M., Roby D., Cuguen J., Bergelson J., Roux F. Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana. Mol Ecol 2013, 22:4222-4240.
15. Brachi B., Faure N., Bergelson J., Cuguen J., Roux F. Genome-wide association mapping of flowering time in Arabidopsis thaliana in nature: genetics for underlying components and reaction norms across two successive years. Acta Bot Gallica 2013, 160:205-218.
16. Li Y., Cheng R.Y., Spokas K.A., Palmer A.A., Borevitz J.O. Genetic variation for life history sensitivity to seasonal warming in Arabidopsis thaliana. Genetics 2014, 196:569-577.
17. Hung H.Y., Shannon L.M., Tian F., Bradbury P.J., Chen C., Flint-Garcia S.A., McMullen M.D., Ware D., Buckler E.S., Doebley J.F., Holland J.B. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci U S A 2012, 109:E1913-E1921.
18. Yang Q., Li Z., Li W.Q., Ku L.X., Wang C., Ye J.R., Li K., Yang N., Li Y.P., Zhong T., Li J.S., Chen Y.H., Yan J.B., Yang X.H., Xu M.L. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci U S A 2013, 110:16969-16974.
19. Putterill J., Robson F., Lee K., Simon R., Coupland G. The constants gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc-finger transcription factors. Cell 1995, 80:847-857.
20. Hao Z.F., Li X.H., Xie C.X., Weng J.F., Li M.S., Zhang D.G., Liang X.L., Liu L.L., Liu S.S., Zhang S.H. Identification of functional genetic variations underlying drought tolerance in maize using SNP markers. J Integr Plant Biol 2011, 53:641-652.
21. Van Inghelandt D., Melchinger A.E., Martinant J.P., Stich B. Genome-wide association mapping of flowering time and northern corn leaf blight (Setosphaeria turcica) resistance in a vast commercial maize germplasm set. BMC Plant Biol 2012, 12.
22. Bouchet S., Servin B., Bertin P., Madur D., Combes V., Dumas F., Brunel D., Laborde J., Charcosset A., Nicolas S. Adaptation of maize to temperate climates: mid-density genome-wide association genetics and diversity patterns reveal key genomic regions, with a major contribution of the Vgt2 (ZCN8) locus. PLoS ONE 2013, 8.
23. Romay M.C., Millard M.J., Glaubitz J.C., Peiffer J.A., Swarts K.L., Casstevens T.M., Elshire R.J., Acharya C.B., Mitchell S.E., Flint-Garcia S.A., McMullen M.D., Holland J.B., Buckler E.S., Gardner C.A. Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol 2013, 14.
24. Xue Y.D., Warburton M.L., Sawkins M., Zhang X.H., Setter T., Xu Y.B., Grudloyma P., Gethi J., Ribaut J.M., Li W.C., Zhang X.B., Zheng Y.L., Yan J.B. Genome-wide association analysis for nine agronomic traits in maize under well-watered and water-stressed conditions. Theor Appl Genet 2013, 126:2587-2596.
25. Zhao K., Tung C.W., Eizenga G.C., Wright M.H., Ali M.L., Price A.H., Norton G.J., Islam M.R., Reynolds A., Mezey J., McClung A.M., Bustamante C.D., McCouch S.R. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2011, 2.
26. Huang X.H., Zhao Y., Wei X.H., Li C.Y., Wang A., Zhao Q., Li W.J., Guo Y.L., Deng L.W., Zhu C.R., Fan D.L., Lu Y.Q., Weng Q.J., Liu K.Y., Zhou T.Y., Jing Y.F., Si L.Z., Dong G.J., Huang T., Lu T.T., Feng Q., Qian Q., Li J.Y., Han B. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 2012, 44:32-39.
27. Zanke C., Ling J., Plieske J., Kollers S., Ebmeyer E., Korzun V., Argillier O., Stiewe G., Hinze M., Beier S., Ganal M.W., Roder M.S. Genetic architecture of main effect QTL for heading date in European winter wheat. Front Plant Sci 2014, 5.
28. Le Gouis J., Bordes J., Ravel C., Heumez E., Faure S., Praud S., Galic N., Remoue C., Balfourier F., Allard V., Rousset M. Genome-wide association analysis to identify chromosomal regions determining components of earliness in wheat. Theor Appl Genet 2012, 124:597-611.
29. Lorenz A.J., Hamblin M.T., Jannink J.L. Performance of single nucleotide polymorphisms versus haplotypes for genome-wide association analysis in barley. PLoS ONE 2010, 5.
30. Cockram J., White J., Zuluaga D.L., Smith D., Comadran J., Macaulay M., Luo Z.W., Kearsey M.J., Werner P., Harrap D., Tapsell C., Liu H., Hedley P.E., Stein N., Schulte D., Steuernagel B., Marshall D.F., Thomas W.T.B., Ramsay L., Mackay I., Balding D.J., Waugh R., O'Sullivan D.M., Consortium A. Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci U S A 2010, 107:21611-21616.
31. Pasam R.K., Sharma R., Malosetti M., van Eeuwijk F.A., Haseneyer G., Kilian B., Graner A. Genome-wide association studies for agronomical traits in a world wide spring barley collection. BMC Plant Biol 2012, 12.
32. Wang H.Y., Smith K.P., Combs E., Blake T., Horsley R.D., Muehlbauer G.J. Effect of population size and unbalanced data sets on QTL detection using genome-wide association mapping in barley breeding germplasm. Theor Appl Genet 2012, 124:111-124.
33. Wang M.H., Jiang N., Jia T.Y., Leach L., Cockram J., Waugh R., Ramsay L., Thomas B., Luo Z.W. Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor Appl Genet 2012, 124:233-246.
34. Berger G.L., Liu S.Y., Hall M.D., Brooks W.S., Chao S.M., Muehlbauer G.J., Baik B.K., Steffenson B., Griffey C.A. Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor Appl Genet 2013, 126:693-710.
35. Munoz-Amatriain M., Cuesta-Marcos A., Endelman J.B., Comadran J., Bonman J.M., Bockelman H.E., Chao S.M., Russell J., Waugh R., Hayes P.M., Muehlbauer G.J. The USDA barley core collection: genetic diversity. Population structure, and potential for genome-wide association studies. PLoS ONE 2014, 9.
36. Saidou A.A., Clotault J., Couderc M., Mariac C., Devos K.M., Thuillet A.C., Amoukou I.A., Vigouroux Y. Association mapping, patterns of linkage disequilibrium and selection in the vicinity of the PHYTOCHROME C gene in pearl millet. Theor Appl Genet 2014, 127:19-32.
37. Jia G.Q., Huang X.H., Zhi H., Zhao Y., Zhao Q., Li W.J., Chai Y., Yang L.F., Liu K.Y., Lu H.Y., Zhu C.R., Lu Y.Q., Zhou C.C., Fan D.L., Weng Q.J., Guo Y.L., Huang T., Zhang L., Lu T.T., Feng Q., Hao H.F., Liu H.K., Lu P., Zhang N., Li Y.H., Guo E.H., Wang S.J., Wang S.Y., Liu J.R., Zhang W.F., Chen G.Q., Zhang B.J., Li W., Wang Y.F., Li H.Q., Zhao B.H., Li J.Y., Diao X.M., Han B. A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 2013, 45:957-961.
38. Galeano C.H., Cortes A.J., Fernandez A.C., Soler A., Franco-Herrera N., Makunde G., Vanderleyden J., Blair M.W. Gene-based single nucleotide polymorphism markers for genetic and association mapping in common bean. BMC Genet 2012, 13.
39. Stanton-Geddes J., Paape T., Epstein B., Briskine R., Yoder J., Mudge J., Bharti A.K., Farmer A.D., Zhou P., Denny R., May G.D., Erlandson S., Yakub M., Sugawara M., Sadowsky M.J., Young N.D., Tiffin P. Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLoS ONE 2013, 8.
40. Linkies A., Graeber K., Knight C., Leubner-Metzger G. The evolution of seeds. New Phytol 2010, 186:817-831.
41. Li F., Chen B., Xu K., Wu J., Song W., Bancroft I., Harper A.L., Trick M., Liu S., Gao G., Wang N., Yan G., Qiao J., Li J., Li H., Xiao X., Zhang T., Wu X. Genome-wide association study dissects the genetic architecture of seed weight and seed quality in rapeseed (Brassica napus L.). DNA Res 2014, 10.1093/dnares/dsu002.
42. Angelovici R., Lipka A.E., Deason N., Gonzalez-Jorge S., Lin H.N., Cepela J., Buell R., Gore M.A., DellaPenna D. Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 2013, 25:4827-4843.
43. Gonzalez-Jorge S., Ha S.H., Magallanes-Lundback M., Gilliland L.U., Zhou A.L., Lipka A.E., Nguyen Y.N., Angelovici R., Lin H.N., Cepela J., Little H., Buell C.R., Gore M.A., DellaPenna D. CAROTENOID CLEAVAGE DIOXYGENASE4 is a negative regulator of beta-carotene content in Arabidopsis seeds. Plant Cell 2013, 25:4812-4826.
44. Yano R., Takebayashi Y., Nambara E., Kamiya Y., Seo M. Combining association mapping and transcriptomics identify HD2B histone deacetylase as a genetic factor associated with seed dormancy in Arabidopsis thaliana. Plant J 2013, 74:815-828.
45. Fournier-Level A., Korte A., Cooper M.D., Nordborg M., Schmitt J., Wilczek A.M. A map of local adaptation in Arabidopsis thaliana. Science 2011, 334:86-89.
46. Huang J., Zhang J.H., Li W.Z., Hu W., Duan L.C., Feng Y., Qiu F.Z., Yue B. Genome-wide association analysis of ten chilling tolerance indices at the germination and seedling stages in maize. J Integr Plant Biol 2013, 55:735-744.
47. Chen H.D., Xie W.B., He H., Yu H.H., Chen W., Li J., Yu R.B., Yao Y., Zhang W.H., He Y.Q., Tang X.Y., Zhou F.S., Deng X.W., Zhang Q.F. A high-density SNP genotyping array for rice biology and molecular breeding. Mol Plant 2014, 7:541-553.
48. Yang W., Guo Z., Huang C., Duan L., Chen G., Jiang N., Fang W., Feng H., Xie W., Lian X., Wang G., Luo Q., Zhang Q., Liu Q., Xiong L. Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 2014, 5.
49. Cuesta-Marcos A., Szucs P., Close T.J., Filichkin T., Muehlbauer G.J., Smith K.P., Hayes P.M. Genome-wide SNPs and re-sequencing of growth habit and inflorescence genes in barley: implications for association mapping in germplasm arrays varying in size and structure. BMC Genomics 2010, 11.
50. Newell M.A., Asoro F.G., Scott M.P., White P.J., Beavis W.D., Jannink J.L. Genome-wide association study for oat (Avena sativa L.) beta-glucan concentration using germplasm of worldwide origin. Theor Appl Genet 2012, 125:1687-1696.
51. Hwang E.Y., Song Q.J., Jia G.F., Specht J.E., Hyten D.L., Costa J., Cregan P.B. A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 2014, 15.
52. Lucas M.R., Huynh B.-L., Vinholes PdS, Cisse N., Drabo I., Ehlers J.D., Roberts P.A., Close T.J. Association studies and legume synteny reveal haplotypes determining seed size in Vigna unguiculata. Front Plant Sci 2013, 4:1-9.
53. Muchero W., Roberts P.A., Diop N.N., Drabo I., Cisse N., Close T.J., Muranaka S., Boukar O., Ehlers J.D. Genetic architecture of delayed senescence, biomass, and grain yield under drought stress in cowpea. PLoS ONE 2013, 8.
54. Ranc N., Munos S., Xu J.X., Le Paslier M.C., Chauveau A., Bounon R., Rolland S., Bouchet J.P., Brunel D., Causse M. Genome-wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3-Genes Genom Genet 2012, 2:853-864.
55. Shirasawa K., Fukuoka H., Matsunaga H., Kobayashi Y., Kobayashi I., Hirakawa H., Isobe S., Tabata S. Genome-wide association studies using single nucleotide polymorphism markers developed by re-sequencing of the genomes of cultivated tomato. DNA Res 2013, 20:593-603.
56. Sauvage C., Segura V., Bauchet G., Stevens R., Do P.T., Nikoloski Z., Fernie A.R., Causse M. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol 2014, 165:1120-1132.
57. Parchman T.L., Gompert Z., Mudge J., Schilkey F.D., Benkman C.W., Buerkle C.A. Genome-wide association genetics of an adaptive trait in lodgepole pine. Mol Ecol 2012, 21:2991-3005.
58. Budde K.B., Heuertz M., Hernandez-Serrano A., Pausas J.G., Vendramin G.G., Verdu M., Gonzalez-Martinez S.C. In situ genetic association for serotiny, a fire-related trait, in Mediterranean maritime pine (Pinus pinaster). New Phytol 2014, 201:230-241.
59. Muchero W., Ehlers J.D., Close T.J., Roberts P.A. Mapping QTL for drought stress-induced premature senescence and maturity in cowpea [Vigna unguiculata (L.) Walp.]. Theor Appl Genet 2009, 118:849-863.
60. Saliba-Colombani V., Causse M., Langlois D., Philouze J., Buret M. Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 2001, 102:259-272.
61. Tian F., Bradbury P.J., Brown P.J., Hung H., Sun Q., Flint-Garcia S., Rocheford T.R., McMullen M.D., Holland J.B., Buckler E.S. Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 2011, 43:159-162.
62. Chitwood D.H., Ranjan A., Martinez C.C., Headland L.R., Thiem T., Kumar R., Covington M.F., Hatcher T., Naylor D.T., Zimmerman S., Downs N., Raymundo N., Buckler E.S., Maloof J.N., Aradhya M., Prins B., Li L., Myles S., Sinha N.R. A modern ampelography: a genetic basis for leaf shape and venation patterning in grape. Plant Physiol 2014, 164:259-272.
63. Slovak R., Göschl C., Su X., Shimotani K., Shiina T., Busch W. A scalable open-source pipeline for large-scale root phenotyping of Arabidopsis. Plant Cell 2014, 10.1105/tpc.114.124032.
64. Gifford M.L., Banta J.A., Katari M.S., Hulsmans J., Chen L., Ristova D., Tranchina D., Purugganan M.D., Coruzzi G.M., Birnbaum K.D. Plasticity regulators modulate specific root traits in discrete nitrogen environments. PLoS Genet 2013, 9.
65. Rosas U., Cibrian-Jaramillo A., Ristova D., Banta J.A., Gifford M.L., Fan A.H., Zhou R.W., Kim G.J., Krouk G., Birnbaum K.D., Purugganan M.D., Coruzzi G.M. Integration of responses within and across Arabidopsis natural accessions uncovers loci controlling root systems architecture. Proc Natl Acad Sci U S A 2013, 110:15133-15138.
66. Meijon M., Satbhai S.B., Tsuchimatsu T., Busch W. Genome-wide association study using cellular traits identifies a new regulator of root development in Arabidopsis. Nat Genet 2014, 46:77-81.
67. Korte A., Farlow A. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 2013, 9.
68. Kang H.M., Zaitlen N.A., Wade C.M., Kirby A., Heckerman D., Daly M.J., Eskin E. Efficient control of population structure in model organism association mapping. Genetics 2008, 178:1709-1723.
69. Seren U., Vilhjalmsson B.J., Horton M.W., Meng D.Z., Forai P., Huang Y.S., Long Q., Segura V., Nordborg M. GWAPP: a web application for genome-wide association mapping in Arabidopsis. Plant Cell 2012, 24:4793-4805.
70. Bradbury P.J., Zhang Z., Kroon D.E., Casstevens T.M., Ramdoss Y., Buckler E.S. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 2007, 23:2633-2635.
71. Benjamini Y., Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001, 29:1165-1188.
72. Nordborg M., Borevitz J.O., Bergelson J., Berry C.C., Chory J., Hagenblad J., Kreitman M., Maloof J.N., Noyes T., Oefner P.J., Stahl E.A., Weigel D. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 2002, 30:190-193.
73. Sorkheh K., Malysheva-Otto L.V., Wirthensohn M.G., Tarkesh-Esfahani S., Martinez-Gomez P. Linkage disequilibrium, genetic association mapping and gene localization in crop plants. Genet Mol Biol 2008, 31:805-814.
74. Bush W.S., Moore J.H. Chapter 11: genome-wide association studies. PLoS Comput Biol 2012, 8.
75. Weigel D., Nordborg M. Natural variation in Arabidopsis. How do we find the causal genes?. Plant Physiol 2005, 138:567-568.
76. Gazzarrini S., McCourt P. Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann Bot Lond 2003, 91:605-612.
77. Todesco M., Balasubramanian S., Hu T.T., Traw M.B., Horton M., Epple P., Kuhns C., Sureshkumar S., Schwartz C., Lanz C., Laitinen R.A.E., Huang Y., Chory J., Lipka V., Borevitz J.O., Dangl J.L., Bergelson J., Nordborg M., Weigel D. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 2010, 465:632-636.
78. DeRose-Wilson L., Gaut B.S. Mapping salinity tolerance during Arabidopsis thaliana germination and seedling growth. PLoS ONE 2011, 6.
79. Nemri A., Atwell S., Tarone A.M., Huang Y.S., Zhao K., Studholme D.J., Nordborg M., Jones J.D.G. Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc Natl Acad Sci U S A 2010, 107:10302-10307.
80. Pagny G., Paulstephenraj P.S., Poque S., Sicard O., Cosson P., Eyquard J.P., Caballero M., Chague A., Gourdon G., Negrel L., Candresse T., Mariette S., Decroocq V. Family-based linkage and association mapping reveals novel genes affecting Plum pox virus infection in Arabidopsis thaliana. New Phytol 2012, 196:873-886.
81. Huard-Chauveau C., Perchepied L., Debieu M., Rivas S., Kroj T., Kars I., Bergelson J., Roux F., Roby D. An atypical kinase under balancing selection confers broad-spectrum disease resistance in Arabidopsis. PLoS Genet 2013, 9.
82. Chan E.K.F., Rowe H.C., Kliebenstein D.J. Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics 2010, 185:991-1007.
83. Chan E.K.F., Rowe H.C., Hansen B.G., Kliebenstein D.J. The complex genetic architecture of the metabolome. PLoS Genet 2010, 6.
84. Baxter I., Brazelton J.N., Yu D.N., Huang Y.S., Lahner B., Yakubova E., Li Y., Bergelson J., Borevitz J.O., Nordborg M., Vitek O., Salt D.E. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet 2010, 6.
85. Chan E.K.F., Rowe H.C., Corwin J.A., Joseph B., Kliebenstein D.J. Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biol 2011, 9.
86. Chao D.Y., Silva A., Baxter I., Huang Y.S., Nordborg M., Danku J., Lahner B., Yakubova E., Salt D.E. Genome-wide association studies identify Heavy Metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Genet 2012, 8.
87. Verslues P.E., Lasky J.R., Juenger T.E., Liu T.W., Kumar M.N. Genome-wide association mapping combined with reverse genetics identifies new effectors of low water potential-induced proline accumulation in Arabidopsis. Plant Physiol 2014, 164:144-159.
88. Filiault D.L., Maloof J.N. A genome-wide association study identifies variants underlying the Arabidopsis thaliana shade avoidance response. PLoS Genet 2012, 8.
89. Long Q., Rabanal F.A., Meng D.Z., Huber C.D., Farlow A., Platzer A., Zhang Q.R., Vilhjalmsson B.J., Korte A., Nizhynska V., Voronin V., Korte P., Sedman L., Mandakova T., Lysak M.A., Seren U., Hellmann I., Nordborg M. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat Genet 2013, 45:884-890.
90. Weng J.F., Xie C.X., Hao Z.F., Wang J.J., Liu C.L., Li M.S., Zhang D.G., Bai L., Zhang S.H., Li X.H. Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS ONE 2011, 6.
91. Strigens A., Freitag N.M., Gilbert X., Grieder C., Riedelsheimer C., Schrag T.A., Messmer R., Melchinger A.E. Association mapping for chilling tolerance in elite flint and dent maize inbred lines evaluated in growth chamber and field experiments. Plant Cell Environ 2013, 36:1871-1887.
92. Kump K.L., Bradbury P.J., Wisser R.J., Buckler E.S., Belcher A.R., Oropeza-Rosas M.A., Zwonitzer J.C., Kresovich S., McMullen M.D., Ware D., Balint-Kurti P.J., Holland J.B. Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 2011, 43:163-168.
93. Weng J.F., Liu X.J., Wang Z.H., Wang J.J., Zhang L., Hao Z.F., Xie C.X., Li M.S., Zhang D.G., Bai L., Liu C.L., Zhang S.H., Li X.H. Molecular mapping of the major resistance quantitative trait locus qHS2.09 with simple sequence repeat and single nucleotide polymorphism markers in maize. Phytopathology 2012, 102:692-699.
94. Zila C.T., Samayoa L.F., Santiago R., Butron A., Holland J.B. A genome-wide association study reveals genes associated with Fusarium ear rot resistance in a maize core diversity panel. G3-Genes Genom Genet 2013, 3:2095-2104.
95. Olukolu B.A., Negeri A., Dhawan R., Venkata B.P., Sharma P., Garg A., Gachomo E., Marla S., Chu K., Hasan A., Ji J.B., Chintamanani S., Green J., Shyu C.R., Wisser R., Holland J., Johal G., Balint-Kurti P. A connected set of genes associated with programmed cell death implicated in controlling the hypersensitive response in maize. Genetics 2013, 193:609-620.
96. Liu C.L., Weng J.F., Zhang D.G., Zhang X.C., Yang X.Y., Shi L.Y., Meng Q.C., Yuan J.H., Guo X.P., Hao Z.F., Xie C.X., Li M.S., Ci X.K., Bai L., Li X.H., Zhang S.H. Genome-wide association study of resistance to rough dwarf disease in maize. Eur J Plant Pathol 2014, 139:205-216.
97. Riedelsheimer C., Lisec J., Czedik-Eysenberg A., Sulpice R., Flis A., Grieder C., Altmann T., Stitt M., Willmitzer L., Melchinger A.E. Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Natl Acad Sci U S A 2012, 109:8872-8877.
98. Li Q., Yang X.H., Xu S.T., Cai Y., Zhang D.L., Han Y.J., Li L., Zhang Z.X., Gao S.B., Li J.S., Yan J.B. Genome-wide association studies identified three independent polymorphisms associated with alpha-tocopherol content in maize kernels. PLoS ONE 2012, 7.
99. Lipka A.E., Gore M.A., Magallanes-Lundback M., Mesberg A., Lin H.N., Tiede T., Chen C., Buell C.R., Buckler E.S., Rocheford T., DellaPenna D. Genome-wide association study and pathway-level analysis of tocochromanol levels in maize grain. G3-Genes Genom Genet 2013, 3:1287-1299.
100. Waugh R., Marshall D., Thomas B., Comadran J., Russell J., Close T., Stein N., Hayes P., Muehlbauer G., Cockram J., O'Sullivan D., MacKay I., Flavell A., AGOUEB, BarleyCAP, Ramsay L. Whole-genome association mapping in elite inbred crop varieties. Genome 2010, 53:967-972.
101. Ramsay L., Comadran J., Druka A., Marshall D.F., Thomas W.T.B., Macaulay M., MacKenzie K., Simpson C., Fuller J., Bonar N., Hayes P.M., Lundqvist U., Franckowiak J.D., Close T.J., Muehlbauer G.J., Waugh R. INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat Genet 2011, 43:169-172.
102. Long N.V., Dolstra O., Malosetti M., Kilian B., Graner A., Visser R.G.F., van der Linden C.G. Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 2013, 126:2335-2351.
103. Massman J., Cooper B., Horsley R., Neate S., Dill-Macky R., Chao S., Dong Y., Schwarz P., Muehlbauer G.J., Smith K.P. Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol Breeding 2011, 27:439-454.
104. Visioni A., Tondelli A., Francia E., Pswarayi A., Malosetti M., Russell J., Thomas W., Waugh R., Pecchioni N., Romagosa I., Comadran J. Genome-wide association mapping of frost tolerance in barley (Hordeum vulgare L.). BMC Genomics 2013, 14.
105. Shu X.L., Backes G., Rasmussen S.K. Genome-wide association study of resistant starch (RS) phenotypes in a barley variety collection. J Agr Food Chem 2012, 60:10302-10311.
106. Shu X., Rasmussen S.K. Quantification of amylose, amylopectin and β-glucan in the search for genes controlling the three major quality traits in barley using genome-wide association studies. Front Plant Sci 2014, 5.
107. Famoso A.N., Zhao K., Clark R.T., Tung C.W., Wright M.H., Bustamante C., Kochian L.V., McCouch S.R. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet 2011, 7.
108. Huang X.H., Kurata N., Wei X.H., Wang Z.X., Wang A., Zhao Q., Zhao Y., Liu K.Y., Lu H.Y., Li W.J., Guo Y.L., Lu Y.Q., Zhou C.C., Fan D.L., Weng Q.J., Zhu C.R., Huang T., Zhang L., Wang Y.C., Feng L., Furuumi H., Kubo T., Miyabayashi T., Yuan X.P., Xu Q., Dong G.J., Zhan Q.L., Li C.Y., Fujiyama A., Toyoda A., Lu T.T., Feng Q., Qian Q., Li J.Y., Han B. A map of rice genome variation reveals the origin of cultivated rice. Nature 2012, 490:497-501.
109. Porth I., Klapste J., Skyba O., Hannemann J., McKown A.D., Guy R.D., DiFazio S.P., Muchero W., Ranjan P., Tuskan G.A., Friedmann M.C., Ehlting J., Cronk Q.C.B., El-Kassaby Y.A., Douglas C.J., Mansfield S.D. Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytol 2013, 200:710-726.
110. La Mantia J., Klapste J., El-Kassaby Y.A., Azam S., Guy R.D., Douglas C.J., Mansfield S.D., Hamelin R. Association analysis identifies Melampsora xcolumbiana poplar leaf rust resistance SNPs. PLoS ONE 2013, 8.
111. Morris G.P., Rhodes D.H., Brenton Z., Ramu P., Thayil V.M., Deshpande S., Hash C.T., Acharya C., Mitchell S.E., Buckler E.S., Yu J.M., Kresovich S. Dissecting genome-wide association signals for loss-of-function phenotypes in sorghum flavonoid pigmentation traits. G3-Genes Genom Genet 2013, 3:2085-2094.
112. Wurschum T., Maurer H.P., Kraft T., Janssen G., Nilsson C., Reif J.C. Genome-wide association mapping of agronomic traits in sugar beet. Theor Appl Genet 2011, 123:1121-1131.
113. Zhang D., Song H.N., Cheng H., Hao D.R., Wang H., Kan G.Z., Jin H.X., Yu D.Y. The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genet 2014, 10.
114. Uitdewilligen JGAML, Wolters A.M.A., D'hoop B.B., Borm T.J.A., Visser R.G.F., van Eck H.J. A next-generation sequencing method for genotyping-by-sequencing of highly heterozygous autotetraploid potato. PLoS ONE 2013, 8.