review. Plant Methods 9:29. https://doi.org/
10.1186/1746-4811-9-29
4. 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(5):e60. https://doi.org/
10.1371/journal.pgen.0010060
5. Atwell S, Huang YS, Vilhjalmsson BJ,
Willems G, Horton M, Li Y, Meng D,
Platt A, Tarone AM, Hu TT, Jiang R, Muliyati
NW, Zhang X, Amer MA, Baxter I, Brachi B,
Chory J, Dean C, Debieu M, de Meaux J,
Ecker JR, Faure N, Kniskern JM, Jones JD,
Michael T, Nemri A, Roux F, Salt DE,
Tang C, Todesco M, Traw MB, Weigel D,
Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association
study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465(7298):627–631.
https://doi.org/10.1038/nature08800
6. Kim S, Plagnol V, Hu TT, Toomajian C, Clark
RM, Ossowski S, Ecker JR, Weigel D, Nordborg M (2007) Recombination and linkage
disequilibrium in Arabidopsis thaliana. Nat
Genet 39(9):1151–1155. https://doi.org/10.
1038/ng2115
7. Horton MW, Hancock AM, Huang YS,
Toomajian C, Atwell S, Auton A, Muliyati
NW, Platt A, Sperone FG, Vilhjalmsson BJ,
Nordborg M, Borevitz JO, Bergelson J
(2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat Genet 44
(2):212–216. https://doi.org/10.1038/ng.
1042
8. Genomes Consortium
Electronic address
mngoaa, Genomes C (2016) 1,135 genomes
reveal the global pattern of polymorphism in
Arabidopsis thaliana. Cell 166(2):481–491.
https://doi.org/10.1016/j.cell.2016.05.063
9. 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(2):203–208. https://doi.org/
10.1038/ng1702
10. 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
(3):1709–1723. https://doi.org/10.1534/
genetics.107.080101
11. Kang HM, Sul JH, Service SK, Zaitlen NA,
Kong SY, Freimer NB, Sabatti C, Eskin E
(2010) Variance component model to account
for sample structure in genome-wide association studies. Nat Genet 42(4):348–354.
https://doi.org/10.1038/ng.548
12. Zhang Z, Ersoz E, Lai CQ, Todhunter RJ,
Tiwari HK, Gore MA, Bradbury PJ, Yu J,
Arnett DK, Ordovas JM, Buckler ES (2010)
Mixed linear model approach adapted for
genome-wide association studies. Nat Genet
42(4):355–360. https://doi.org/10.1038/
ng.546
13. Lee T, Lee I (2018) araGWAB: Network-based
boosting of genome-wide association studies in
Arabidopsis thaliana. Sci Rep 8(1):2925.
https://doi.org/10.1038/s41598-01821301-4
14. Chan EK, Rowe HC, Corwin JA, Joseph B,
Kliebenstein DJ (2011) Combining genomewide association mapping and transcriptional
networks to identify novel genes controlling
glucosinolates in Arabidopsis thaliana. PLoS
Biol 9(8):e1001125. https://doi.org/10.
1371/journal.pbio.1001125
15. Zhu C, Li X, Yu J (2011) Integrating rarevariant testing, function prediction, and gene
network in composite resequencing-based
genome-wide
association
studies
(CR-GWAS). G3 (Bethesda) 1(3):233–243.
https://doi.org/10.1534/g3.111.000364
16. Jimenez-Gomez JM, Wallace AD, Maloof JN
(2010) Network analysis identifies ELF3 as a
QTL for the shade avoidance response in Arabidopsis. PLoS Genet 6(9):e1001100. https://
doi.org/10.1371/journal.pgen.1001100
17. Schaefer RJ, Michno JM, Jeffers J,
Hoekenga O, Dilkes B, Baxter I, Myers CL
(2018) Integrating coexpression networks
with GWAS to prioritize causal genes in
maize.
Plant
Cell
30(12):2922–2942.
https://doi.org/10.1105/tpc.18.00299
18. Purcell S, Neale B, Todd-Brown K, Thomas L,
Ferreira MA, Bender D, Maller J, Sklar P, de
Bakker PI, Daly MJ, Sham PC (2007) PLINK:
a tool set for whole-genome association and
population-based linkage analyses. Am J Hum
Genet 81(3):559–575. https://doi.org/10.
1086/519795
19. Turner SD (2014) qqman: an R package for
visualizing GWAS results using Q-Q and manhattan plots. biorxiv. https://doi.org/10.
1101/005165
20. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet
2(12):e190. https://doi.org/10.1371/jour
nal.pgen.0020190
Genome-Wide Association Studies in Arabidopsis
209
10.1186/1746-4811-9-29
4. 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(5):e60. https://doi.org/
10.1371/journal.pgen.0010060
5. Atwell S, Huang YS, Vilhjalmsson BJ,
Willems G, Horton M, Li Y, Meng D,
Platt A, Tarone AM, Hu TT, Jiang R, Muliyati
NW, Zhang X, Amer MA, Baxter I, Brachi B,
Chory J, Dean C, Debieu M, de Meaux J,
Ecker JR, Faure N, Kniskern JM, Jones JD,
Michael T, Nemri A, Roux F, Salt DE,
Tang C, Todesco M, Traw MB, Weigel D,
Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association
study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465(7298):627–631.
https://doi.org/10.1038/nature08800
6. Kim S, Plagnol V, Hu TT, Toomajian C, Clark
RM, Ossowski S, Ecker JR, Weigel D, Nordborg M (2007) Recombination and linkage
disequilibrium in Arabidopsis thaliana. Nat
Genet 39(9):1151–1155. https://doi.org/10.
1038/ng2115
7. Horton MW, Hancock AM, Huang YS,
Toomajian C, Atwell S, Auton A, Muliyati
NW, Platt A, Sperone FG, Vilhjalmsson BJ,
Nordborg M, Borevitz JO, Bergelson J
(2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat Genet 44
(2):212–216. https://doi.org/10.1038/ng.
1042
8. Genomes Consortium
Electronic address
mngoaa, Genomes C (2016) 1,135 genomes
reveal the global pattern of polymorphism in
Arabidopsis thaliana. Cell 166(2):481–491.
https://doi.org/10.1016/j.cell.2016.05.063
9. 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(2):203–208. https://doi.org/
10.1038/ng1702
10. 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
(3):1709–1723. https://doi.org/10.1534/
genetics.107.080101
11. Kang HM, Sul JH, Service SK, Zaitlen NA,
Kong SY, Freimer NB, Sabatti C, Eskin E
(2010) Variance component model to account
for sample structure in genome-wide association studies. Nat Genet 42(4):348–354.
https://doi.org/10.1038/ng.548
12. Zhang Z, Ersoz E, Lai CQ, Todhunter RJ,
Tiwari HK, Gore MA, Bradbury PJ, Yu J,
Arnett DK, Ordovas JM, Buckler ES (2010)
Mixed linear model approach adapted for
genome-wide association studies. Nat Genet
42(4):355–360. https://doi.org/10.1038/
ng.546
13. Lee T, Lee I (2018) araGWAB: Network-based
boosting of genome-wide association studies in
Arabidopsis thaliana. Sci Rep 8(1):2925.
https://doi.org/10.1038/s41598-01821301-4
14. Chan EK, Rowe HC, Corwin JA, Joseph B,
Kliebenstein DJ (2011) Combining genomewide association mapping and transcriptional
networks to identify novel genes controlling
glucosinolates in Arabidopsis thaliana. PLoS
Biol 9(8):e1001125. https://doi.org/10.
1371/journal.pbio.1001125
15. Zhu C, Li X, Yu J (2011) Integrating rarevariant testing, function prediction, and gene
network in composite resequencing-based
genome-wide
association
studies
(CR-GWAS). G3 (Bethesda) 1(3):233–243.
https://doi.org/10.1534/g3.111.000364
16. Jimenez-Gomez JM, Wallace AD, Maloof JN
(2010) Network analysis identifies ELF3 as a
QTL for the shade avoidance response in Arabidopsis. PLoS Genet 6(9):e1001100. https://
doi.org/10.1371/journal.pgen.1001100
17. Schaefer RJ, Michno JM, Jeffers J,
Hoekenga O, Dilkes B, Baxter I, Myers CL
(2018) Integrating coexpression networks
with GWAS to prioritize causal genes in
maize.
Plant
Cell
30(12):2922–2942.
https://doi.org/10.1105/tpc.18.00299
18. Purcell S, Neale B, Todd-Brown K, Thomas L,
Ferreira MA, Bender D, Maller J, Sklar P, de
Bakker PI, Daly MJ, Sham PC (2007) PLINK:
a tool set for whole-genome association and
population-based linkage analyses. Am J Hum
Genet 81(3):559–575. https://doi.org/10.
1086/519795
19. Turner SD (2014) qqman: an R package for
visualizing GWAS results using Q-Q and manhattan plots. biorxiv. https://doi.org/10.
1101/005165
20. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet
2(12):e190. https://doi.org/10.1371/jour
nal.pgen.0020190
Genome-Wide Association Studies in Arabidopsis
209