title: Linkage and association mapping of Arabidopsis thaliana flowering time in nature.
abstract: 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.
authors.affiliation: 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.
authors.forename: Benjamin
authors.initials: B
authors.lastname: Brachi
authors.forename: Nathalie
authors.initials: N
authors.lastname: Faure
authors.forename: Matt
authors.initials: M
authors.lastname: Horton
authors.forename: Emilie
authors.initials: E
authors.lastname: Flahauw
authors.forename: Adeline
authors.initials: A
authors.lastname: Vazquez
authors.forename: Magnus
authors.initials: M
authors.lastname: Nordborg
authors.forename: Joy
authors.initials: J
authors.lastname: Bergelson
authors.forename: Joel
authors.initials: J
authors.lastname: Cuguen
authors.forename: Fabrice
authors.initials: F
authors.lastname: Roux
mesh_terms: 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
chemical_list: D029681:Arabidopsis Proteins
references.citation: New Phytol. 2009 Aug;183(3):816-825
references.pmid: 19594694
references.citation: Theor Appl Genet. 2007 May;114(8):1457-66
references.pmid: 17406851
references.citation: Science. 2003 Nov 7;302(5647):1049-53
references.pmid: 14605371
references.citation: Mol Biol Evol. 2008 Feb;25(2):319-29
references.pmid: 18032403
references.citation: Genetics. 2004 Jun;167(2):907-17
references.pmid: 15238539
references.citation: Theor Appl Genet. 2005 Feb;110(4):742-53
references.pmid: 15678326
references.citation: J Evol Biol. 2007 Jan;20(1):349-57
references.pmid: 17210028
references.citation: Nature. 2010 Jun 3;465(7298):627-31
references.pmid: 20336072
references.citation: Genetics. 2009 Oct;183(2):723-32, 1SI-7SI
references.pmid: 19652183
references.citation: Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15670-5
references.pmid: 15505218
references.citation: Plant J. 2004 Apr;38(1):193-202
references.pmid: 15053772
references.citation: Nature. 2008 Dec 11;456(7223):720-3
references.pmid: 19079047
references.citation: Nat Genet. 2006 Jun;38(6):711-5
references.pmid: 16732287
references.citation: Genes Dev. 2006 Nov 15;20(22):3079-83
references.pmid: 17114581
references.citation: PLoS Genet. 2009 Jul;5(7):e1000551
references.pmid: 19593375
references.citation: Genome Res. 2009 May;19(5):723-33
references.pmid: 19411597
references.citation: Plant J. 2009 Oct;60(2):328-39
references.pmid: 19566593
references.citation: J Genet Genomics. 2008 Feb;35(2):119-27
references.pmid: 18407059
references.citation: PLoS Biol. 2006 May;4(5):e137
references.pmid: 16623598
references.citation: Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4712-7
references.pmid: 15070783
references.citation: Am Nat. 2007 May;169(5):E141-57
references.pmid: 17427127
references.citation: Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):17042-7
references.pmid: 17065317
references.citation: Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2460-5
references.pmid: 15695584
references.citation: Trends Plant Sci. 2006 Nov;11(11):550-8
references.pmid: 17035069
references.citation: PLoS One. 2006 Dec 27;1:e105
references.pmid: 17205109
references.citation: J Exp Bot. 2009;60(7):1979-89
references.pmid: 19264752
references.citation: J Evol Biol. 2009 Sep;22(9):1826-38
references.pmid: 19583697
references.citation: Nature. 2003 May 1;423(6935):74-7
references.pmid: 12721627
references.citation: Genetics. 2002 Dec;162(4):1875-84
references.pmid: 12524356
references.citation: Genetics. 2008 Jan;178(1):539-51
references.pmid: 18202393
references.citation: Science. 2007 Jun 29;316(5833):1840-2
references.pmid: 17600199
references.citation: Nat Rev Genet. 2005 Feb;6(2):109-18
references.pmid: 15716907
references.citation: Genetics. 2008 Apr;178(4):2253-64
references.pmid: 18430947
references.citation: Science. 2009 Feb 13;323(5916):930-4
references.pmid: 19150810
references.citation: Development. 2008 Apr;135(7):1335-45
references.pmid: 18305006
references.citation: PLoS One. 2009;4(2):e4318
references.pmid: 19183806
references.citation: Ann Bot. 2002 May;89(5):595-604
references.pmid: 12099534
references.citation: Nat Genet. 2001 Dec;29(4):435-40
references.pmid: 11726930
references.citation: Science. 2009 Aug 7;325(5941):714-8
references.pmid: 19661422
references.citation: Mol Biol Evol. 2009 Nov;26(11):2475-86
references.pmid: 19625391
references.citation: Am J Bot. 2005 Jun;92(6):960-71
references.pmid: 21652479
references.citation: Trends Plant Sci. 2006 Aug;11(8):375-81
references.pmid: 16843035
references.citation: Genetics. 2008 Apr;178(4):2433-7
references.pmid: 18430961
references.citation: Bioinformatics. 2008 Mar 1;24(5):721-3
references.pmid: 18202029
references.citation: Plant J. 2005 Feb;41(3):376-85
references.pmid: 15659097
references.citation: Genetics. 2008 Mar;178(3):1709-23
references.pmid: 18385116
references.citation: PLoS Genet. 2009 Jan;5(1):e1000331
references.pmid: 19132132
references.citation: Science. 2005 Jul 22;309(5734):630-3
references.pmid: 16040710
references.citation: Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):10102-7
references.pmid: 12904584
references.citation: Science. 2007 Jul 20;317(5836):338-42
references.pmid: 17641193
references.citation: J Exp Bot. 2009;60(11):3143-55
references.pmid: 19436046
references.citation: Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):16986-91
references.pmid: 17940010
references.citation: PLoS One. 2007 Jul 25;2(7):e651
references.pmid: 17653278
references.citation: Genetics. 2009 Sep;183(1):325-35
references.pmid: 19581446
references.citation: Genes Dev. 2003 Jan 15;17(2):256-68
references.pmid: 12533513
references.citation: Plant Physiol. 2007 Sep;145(1):160-73
references.pmid: 17631524
references.citation: Am Nat. 1997 Jun;149(6):1147-55
references.pmid: 18811268
references.citation: Plant Physiol. 2005 Jun;138(2):1163-73
references.pmid: 15908596
references.citation: Plant Cell Physiol. 2005 Aug;46(8):1340-9
references.pmid: 15937324
references.citation: Mol Biol Evol. 2008 Oct;25(10):2211-9
references.pmid: 18669581
references.citation: Am J Bot. 1999 Apr;86(4):470-5
references.pmid: 10205066
references.citation: Mol Ecol. 2006 May;15(6):1507-17
references.pmid: 16629807
references.citation: Nat Genet. 2004 May;36(5):512-7
references.pmid: 15052271
references.citation: Oecologia. 1998 Jul;115(3):293-301
references.pmid: 28308418
references.citation: Plant Mol Biol. 1999 Sep;41(2):195-206
references.pmid: 10579487
references.citation: Heredity (Edinb). 1999 Oct;83 ( Pt 4):363-72
references.pmid: 10583537
references.citation: PLoS Genet. 2007 Jan 19;3(1):e4
references.pmid: 17238287
references.citation: Nat Genet. 2006 Feb;38(2):203-8
references.pmid: 16380716
references.citation: Plant Cell. 2009 Jul;21(7):1877-96
references.pmid: 19574434