Linkage and association mapping of Arabidopsis thaliana flowering time in nature.
Flowering time is a key life-history trait in the plant life cycle. Most studies to unravel the genetics of flowering time in Arabidopsis thaliana have been performed under greenhouse conditions. Here, we describe a study about the genetics of flowering time that differs from previous studies in two important ways: first, we measure flowering time in a more complex and ecologically realistic environment; and, second, we combine the advantages of genome-wide association (GWA) and traditional linkage (QTL) mapping. Our experiments involved phenotyping nearly 20,000 plants over 2 winters under field conditions, including 184 worldwide natural accessions genotyped for 216,509 SNPs and 4,366 RILs derived from 13 independent crosses chosen to maximize genetic and phenotypic diversity. Based on a photothermal time model, the flowering time variation scored in our field experiment was poorly correlated with the flowering time variation previously obtained under greenhouse conditions, reinforcing previous demonstrations of the importance of genotype by environment interactions in A. thaliana and the need to study adaptive variation under natural conditions. The use of 4,366 RILs provides great power for dissecting the genetic architecture of flowering time in A. thaliana under our specific field conditions. We describe more than 60 additive QTLs, all with relatively small to medium effects and organized in 5 major clusters. We show that QTL mapping increases our power to distinguish true from false associations in GWA mapping. QTL mapping also permits the identification of false negatives, that is, causative SNPs that are lost when applying GWA methods that control for population structure. Major genes underpinning flowering time in the greenhouse were not associated with flowering time in this study. Instead, we found a prevalence of genes involved in the regulation of the plant circadian clock. Furthermore, we identified new genomic regions lacking obvious candidate genes.
Brachi
Benjamin
B
Laboratoire Génétique et Evolution des Populations Végétales, Unité Mixte de Recherche CNRS 8016, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France.
Faure
Nathalie
N
Horton
Matt
M
Flahauw
Emilie
E
Vazquez
Adeline
A
Nordborg
Magnus
M
Bergelson
Joy
J
Cuguen
Joel
J
Roux
Fabrice
F
D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics; D002874:Chromosome Mapping; D032461:Chromosomes, Plant; D035264:Flowers / Q000235:genetics / Q000254:growth & development; D008040:Genetic Linkage; D055106:Genome-Wide Association Study; D008969:Molecular Sequence Data; D020641:Polymorphism, Single Nucleotide; D040641:Quantitative Trait Loci; D012621:Seasons
D029681:Arabidopsis Proteins
New Phytol. 2009 Aug;183(3):816-825
19594694
Theor Appl Genet. 2007 May;114(8):1457-66
17406851
Science. 2003 Nov 7;302(5647):1049-53
14605371
Mol Biol Evol. 2008 Feb;25(2):319-29
18032403
Genetics. 2004 Jun;167(2):907-17
15238539
Theor Appl Genet. 2005 Feb;110(4):742-53
15678326
J Evol Biol. 2007 Jan;20(1):349-57
17210028
Nature. 2010 Jun 3;465(7298):627-31
20336072
Genetics. 2009 Oct;183(2):723-32, 1SI-7SI
19652183
Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15670-5
15505218
Plant J. 2004 Apr;38(1):193-202
15053772
Nature. 2008 Dec 11;456(7223):720-3
19079047
Nat Genet. 2006 Jun;38(6):711-5
16732287
Genes Dev. 2006 Nov 15;20(22):3079-83
17114581
PLoS Genet. 2009 Jul;5(7):e1000551
19593375
Genome Res. 2009 May;19(5):723-33
19411597
Plant J. 2009 Oct;60(2):328-39
19566593
J Genet Genomics. 2008 Feb;35(2):119-27
18407059
PLoS Biol. 2006 May;4(5):e137
16623598
Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4712-7
15070783
Am Nat. 2007 May;169(5):E141-57
17427127
Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):17042-7
17065317
Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2460-5
15695584
Trends Plant Sci. 2006 Nov;11(11):550-8
17035069
PLoS One. 2006 Dec 27;1:e105
17205109
J Exp Bot. 2009;60(7):1979-89
19264752
J Evol Biol. 2009 Sep;22(9):1826-38
19583697
Nature. 2003 May 1;423(6935):74-7
12721627
Genetics. 2002 Dec;162(4):1875-84
12524356
Genetics. 2008 Jan;178(1):539-51
18202393
Science. 2007 Jun 29;316(5833):1840-2
17600199
Nat Rev Genet. 2005 Feb;6(2):109-18
15716907
Genetics. 2008 Apr;178(4):2253-64
18430947
Science. 2009 Feb 13;323(5916):930-4
19150810
Development. 2008 Apr;135(7):1335-45
18305006
PLoS One. 2009;4(2):e4318
19183806
Ann Bot. 2002 May;89(5):595-604
12099534
Nat Genet. 2001 Dec;29(4):435-40
11726930
Science. 2009 Aug 7;325(5941):714-8
19661422
Mol Biol Evol. 2009 Nov;26(11):2475-86
19625391
Am J Bot. 2005 Jun;92(6):960-71
21652479
Trends Plant Sci. 2006 Aug;11(8):375-81
16843035
Genetics. 2008 Apr;178(4):2433-7
18430961
Bioinformatics. 2008 Mar 1;24(5):721-3
18202029
Plant J. 2005 Feb;41(3):376-85
15659097
Genetics. 2008 Mar;178(3):1709-23
18385116
PLoS Genet. 2009 Jan;5(1):e1000331
19132132
Science. 2005 Jul 22;309(5734):630-3
16040710
Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):10102-7
12904584
Science. 2007 Jul 20;317(5836):338-42
17641193
J Exp Bot. 2009;60(11):3143-55
19436046
Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):16986-91
17940010
PLoS One. 2007 Jul 25;2(7):e651
17653278
Genetics. 2009 Sep;183(1):325-35
19581446
Genes Dev. 2003 Jan 15;17(2):256-68
12533513
Plant Physiol. 2007 Sep;145(1):160-73
17631524
Am Nat. 1997 Jun;149(6):1147-55
18811268
Plant Physiol. 2005 Jun;138(2):1163-73
15908596
Plant Cell Physiol. 2005 Aug;46(8):1340-9
15937324
Mol Biol Evol. 2008 Oct;25(10):2211-9
18669581
Am J Bot. 1999 Apr;86(4):470-5
10205066
Mol Ecol. 2006 May;15(6):1507-17
16629807
Nat Genet. 2004 May;36(5):512-7
15052271
Oecologia. 1998 Jul;115(3):293-301
28308418
Plant Mol Biol. 1999 Sep;41(2):195-206
10579487
Heredity (Edinb). 1999 Oct;83 ( Pt 4):363-72
10583537
PLoS Genet. 2007 Jan 19;3(1):e4
17238287
Nat Genet. 2006 Feb;38(2):203-8
16380716
Plant Cell. 2009 Jul;21(7):1877-96
19574434