Key Points
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Identifying the genetic basis of ecologically important characters is a first step in retracing the trajectory of adaptive traits in natural populations of plants as well as in potentially improving crop yield and quality.
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Genome-wide association (GWA) mapping is a highly effective means of gene discovery in Arabidopsis thaliana, with a substantial fraction of phenotypic variation being explained by few quantitative trait loci (QTLs).
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Dual linkage and association mapping clearly outperforms each method in isolation.
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The scale of adaptation, which depends on the ecological factors acting as selective pressures, will determine the scale at which GWA mapping populations should be constructed.
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Combining genotypic and epigenetic information will help to tease apart the effect of DNA sequence variants from that of DNA methylation variants.
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The genetic basis of genotype–environment interactions remains to be determined in A. thaliana.
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The heterogeneity encountered by A. thaliana suggests that the phenotyping of ecologically relevant traits should be performed in natural populations, not only in the greenhouse.
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The current revolution in next-generation sequencing facilitates a direct access to the causal mutations that underlie adaptive trait variation.
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The next challenge for dissecting the genetic bases of adaptive variation is the high-throughput phenotyping of complex traits under natural conditions.
Abstract
A major challenge in evolutionary biology and plant breeding is to identify the genetic basis of complex quantitative traits, including those that contribute to adaptive variation. Here we review the development of new methods and resources to fine-map intraspecific genetic variation that underlies natural phenotypic variation in plants. In particular, the analysis of 107 quantitative traits reported in the first genome-wide association mapping study in Arabidopsis thaliana sets the stage for an exciting time in our understanding of plant adaptation. We also argue for the need to place phenotype–genotype association studies in an ecological context if one is to predict the evolutionary trajectories of plant species.
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Acknowledgements
The authors give special thanks to M. Horton and B. Brachi for stimulating discussions on placing GWA mapping studies in an ecological context, to O. Loudet for links to automated platforms of phenotyping and to E. Xing for links to the GenAMap platform for structured GWA mapping. We are grateful for funding from the US National Science Foundation (MCB-0603515), the US National Institutes of Health (GM083068) and the French l'Agence Nationale de la Recherche (NT09_473214).
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Arabidopsis Tiling Array information (Borevitz laboratory)
Arabidopsis Tiling Array information (Nordborg laboratory)
Ecological Genomics of Arabidopsis Development
GenAMap (an integrated analytic and visualization platform for eQTL and GWA study analysis)
Genomic analysis of the genotype–phenotype map
International Plant Phenomics Network
Nature Reviews Genetics series on Genome-wide association studies
Glossary
- Adaptive walk
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The evolutionary path taken by a population towards a new phenotypic optimum; it is defined by the number, phenotypic size and temporal sequence of genetic changes.
- Life history
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Life history traits are closely related to fitness traits, such as number and size of offspring, age at first reproduction, and reproductive lifespan and ageing.
- Quantitative trait locus
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Genomic region containing one or more genes that affect the variation of a quantitative trait.
- Genome-wide association
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Whole-genome scans that test the association between the genotypes at each locus and a given phenotype.
- Seed dormancy
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Mechanism that prevents seed germination, even under conditions that promote germination.
- Ionomics
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The study of the composition of mineral nutrients and trace elements in living organisms.
- Genotype–environment interaction
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An effect of a locus that changes in magnitude or direction across environments.
- Trade-off
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Negative genetic and phenotypic correlation between two traits arising from the need of the individual to allocate resources to alternative functions.
- Genetic map
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Representation of the position of genetic markers relative to each other, with distances between loci expressed in terms of recombination frequency.
- Recombinant inbred lines
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Quasi-homozygous lines produced from an initial cross between two individuals, followed by six to eight generations of selfing.
- Population structure
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Differentiation in allele frequencies among multiple populations.
- Linkage disequilibrium
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Nonrandom allelic association such that two alleles at two or more loci are more or less frequently associated than predicted by their individual frequencies.
- SNP-tiling array
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A microarray platform combining SNP genotyping and whole-genome tiling; it contains probes for each allele and each strand of several thousands of SNPs.
- Non-singleton SNP
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A SNP polymorphism that is present in at least two individuals.
- Genetic heterogeneity
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The same phenotypic value caused by different mutations at different genes.
- Allelic heterogeneity
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The same phenotypic value caused by different mutations at the same gene.
- Crypsis
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Capacity of an organism to avoid detection by other organisms by blending into the environment.
- Balancing selection
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Evolutionary processes that maintain genetic diversity within a population for longer than expected under neutrality. Processes include heterozygote advantage, frequency-dependent selection and variation of fitness in space and time.
- Epigenetic RILs
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Quasi-homozygous lines that are almost identical at the genetic level but segregate at the DNA methylation level. EpiRILs are produced from an initial cross between two individuals with few DNA sequence differences but contrasting DNA methylation profiles, followed by six to eight generations of selfing.
- Non-parametric methods
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Statistical methods, also called distribution free methods, that are not based on a normal distribution of data.
- Mixed linear model
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Statistical model containing both fixed effects and random effects.
- Multi-task regularized regression
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Joint association analysis of multiple populations with a multi-population group lasso using L1/L2 regression.
- T-DNA
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Transferred DNA of the tumour-inducing (Ti) plasmid of some bacterial species into the nuclear DNA genome of the host plant.
- Unimutant collection
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A collection of 31,033 publically available homozygous T-DNA insertion lines in Arabidopsis thaliana representing 18,506 individual genes; produced by the Salk Institute.
- AmiRNA
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Artificial microRNAs that target specific genes for silencing.
- Cre–lox
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Transgenic technology creating isolines with identical genomes, except for the gene of interest. The resulting paired isolines are created by first introducing the gene of interest with a selectable marker into the genome and then excising the gene of interest. Modifications of this approach can be used to create allelic series.
- Environmental grain
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The scale of temporal and spatial environmental variation that is perceived by an organism.
- Phenotypic plasticity
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The ability of an organism to develop a phenotypic state, depending on its external and internal environment.
- Reaction norm
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The set of phenotypes expressed by a genotype under different environmental conditions.
- Path analysis
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A statistical method that provides estimates of the magnitude and significance of causal relationships between two or more variables.
- Pleiotropy
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The effect of a gene on more than one phenotypic trait.
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Cite this article
Bergelson, J., Roux, F. Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 11, 867–879 (2010). https://doi.org/10.1038/nrg2896
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DOI: https://doi.org/10.1038/nrg2896
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