Cited by 1,780Genetic Mapping and Diversity in Plants and AnimalsGenetic Associations and EpidemiologyGenetic and phenotypic traits in livestock

Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines

Open access
Atwell, Susanna, Huang, Yu S., Vilhjálmsson, Bjarni J., Willems, Glenda, Horton, Matthew, Li, Yan, Meng, Dazhe, Platt, Alexander +28 more·2010·Nature

Abstract

Although pioneered by human geneticists as a potential solution to the challenging problem of finding the genetic basis of common human diseases, genome-wide association (GWA) studies have, owing to advances in genotyping and sequencing technology, become an obvious general approach for studying the genetics of natural variation and traits of agricultural importance. They are particularly useful when inbred lines are available, because once these lines have been genotyped they can be phenotyped multiple times, making it possible (as well as extremely cost effective) to study many different traits in many different environments, while replicating the phenotypic measurements to reduce environmental noise. Here we demonstrate the power of this approach by carrying out a GWA study of 107 phenotypes in Arabidopsis thaliana, a widely distributed, predominantly self-fertilizing model plant known to harbour considerable genetic variation for many adaptively important traits. Our results are dramatically different from those of human GWA studies, in that we identify many common alleles of major effect, but they are also, in many cases, harder to interpret because confounding by complex genetics and population structure make it difficult to distinguish true associations from false. However, a-priori candidates are significantly over-represented among these associations as well, making many of them excellent candidates for follow-up experiments. Our study demonstrates the feasibility of GWA studies in A. thaliana and suggests that the approach will be appropriate for many other organisms.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/nature08800

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Glucosinolates may also regulate circadian clock and flowering time.

    “Apart from growth and stomatal opening, glucosinolates may also regulate the circadian clock and flowering time.”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Atwell et al., 2010

    The paper’s flowering-related results (Abstract section; page unavailable) discuss associations involving FRI, FLC, and DOG1, but do not link glucosinolates to flowering time. Searches for glucosinolates, the circadian clock, and flowering together found no passage addressing the claimed regulatory role. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 25

  1. [1]Hirschhorn JN Daly MJ Genome-wide association studies for common diseases and complex traits Nat Rev Genet 6 95 108 2005 15716906
  2. [2]Wellcome Trust Case-Control Consortium Genome-wide association study of 14,000 cases of seven common diseases. 3,000 shared controls Nature 447 661 678 2007 17554300 PMC2719288
  3. [3]Koornneef M Alonso-Blanco C Vreugdenhil D Naturally occurring genetic variation in Arabidopsis thaliana Annu Rev Plant Biol 55 141 172 2004 15377217
  4. [4]Nordborg M The pattern of polymorphism in Arabidopsis thaliana PLoS Biol 3 e196 2005 15907155 PMC1135296
  5. [5]Shindo C Role of FRIGIDA and FLC in determining variation in flowering time of Arabidopsis thaliana Plant Physiol 138 1163 1173 2005 15908596 PMC1150429
  6. [6]Kim S Recombination and linkage disequilibrium in Arabidopsis thaliana Nature Genet 39 1151 1155 2007 17676040
  7. [7]Nordborg M The extent of linkage disequilibrium in Arabidopsis thaliana Nature Genet 30 190 193 2002 11780140
  8. [8]Aranzana MJ Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes PLoS Genet 1 e60 2005 16292355 PMC1283159
  9. [9]Zhao K An Arabidopsis example of association mapping in structured samples PLoS Genet 3 e4 2007 17238287 PMC1779303
  10. [10]Pritchard JK Stephens M Rosenberg NA Donnelly P Association mapping in structured populations Am J Hum Genet 67 170 181 2000 10827107 PMC1287075
  11. [11]Price AL Principal components analysis corrects for stratification in genome-wide association studies Nat Genet 38 904 909 2006 16862161
  12. [12]Yu J A unified mixed-model method for association mapping that accounts for multiple levels of relatedness Nat Genet 38 203 208 2006 16380716
  13. [13]Kang HM Efficient control of population structure in model organism association mapping Genetics 178 1709 1723 2008 18385116 PMC2278096
  14. [14]Grant MR Structure of the Arabidopsis Rpm1 gene enabling dual-specificity disease resistance Science 269 843 846 1995 7638602
  15. [15]Johanson U Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time Science 290 344 347 2000 11030654
  16. [16]Toomajian C A non-parametric test reveals selection for rapid flowering in the Arabidopsis genome PLoS Biol 4 e137 2006 16623598 PMC1440937
  17. [17]Michaels SD Amasino RM FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering Plant Cell 11 949 956 1999 10330478 PMC144226
  18. [18]Bentsink L Jowett J Hanhart CJ Koornneef M Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis Proc Natl Acad Sci USA 103 17042 17047 2006 17065317 PMC1636575
  19. [19]Rus A Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis Plos Genetics 2 1964 1973 2006 PMC1665649 17140289
  20. [20]Baxter I Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1) Plos Genetics 4 2008 PMC2265440 18454190
  21. [21]Hilscher J Schlötterer C Hauser M-T A single amino acid replacement in ETC2 acts as major modifier of trichome patterning in natural Arabidopsis populations Current Biology 2009 To appear PMC2864576 19818620
  22. [22]Lu H Rate DN Song JT Greenberg JT ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response Plant Cell 15 2408 2420 2003 14507999 PMC197305
  23. [23]Todesco M A single locus causing major pleiotropic tradeoffs in Arabidopsis thaliana accessions Under review for Nature 2009
  24. [28]Rosenberg N Nordborg M A general population-genetic model for the production by population structure of spurious genotype-phenotype associations in discrete, admixed, or spatially distributed populations Genetics 173 1665 1678 2006 16582435 PMC1526699
  25. [29]Nordborg M Weigel D Next-generation genetics in plants Nature 456 720 723 2008 19079047

Cited by

Sorted by citations

Authors
Atwell, S., Huang, Y. S., Vilhjálmsson, B. J., Willems, G., Horton, M., Li, Y., Meng, D., 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., Todesco, M., Traw, M. B., Weigel, D., Marjoram, P., Borevitz, J. O., Bergelson, J., & Nordborg, M.
Affiliations
  • University of Southern California (US)
  • University of Chicago (US)
  • Centre National de la Recherche Scientifique (FR)
  • Salk Institute for Biological Studies (US)
  • John Innes Centre (GB)
  • Max Planck Institute for Plant Breeding Research (DE)
  • Sainsbury Laboratory (GB)
  • Purdue University West Lafayette (US)
  • Max Planck Institute for Developmental Biology (DE)
  • Gregor Mendel Institute of Molecular Plant Biology (AT)
Corresponding author
Nordborg, Magnus
Venue
Nature
Published
2010-03-24
Volume
465
Issue
7298
Pages
627-631
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2137797806
Cited by
1,780
References
4
Citations by year
2026: 48 · 2025: 58 · 2024: 90 · 2023: 77 · 2022: 123 · 2021: 111 · 2020: 112 · 2019: 105 · 2018: 115 · 2017: 126 · 2016: 146 · 2015: 137 · 2014: 124 · 2013: 136 · 2012: 124
FWCI
73.10
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • HAL (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • Max Planck Digital Library (submittedVersion)
  • ANU Open Research (Australian National University) (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • Biotechnology and Biological Sciences Research Council (BBS/E/J/000CA355)
  • National Institute of General Medical Sciences (GM073822, R01GM057994, GM057994, GM 62932, R01GM073822, GM078536, R01GM078536, R01GM062932)
  • National Institute of Environmental Health Sciences (P42ES007373)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
Keywords
genome-wide association study, Arabidopsis thaliana, inbred lines, natural genetic variation, phenotypic variability, population structure, major-effect loci, disease resistance, vegetative growth, forward genetics, candidate genes, plant genetics, false positive association
MeSH terms
Alleles, Genotype, Immunity, Innate, Inbreeding, Phenotype, Genes, Plant, Arabidopsis, Genome, Plant, Polymorphism, Single Nucleotide, Arabidopsis Proteins, Flowers, Genome-Wide Association Study, Genetic Loci

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review