Review Article | Published:

Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis

Naturevolume 441pages947952 (2006) | Download Citation

Subjects

Abstract

Genomic studies of natural variation in model organisms provide a bridge between molecular analyses of gene function and evolutionary investigations of adaptation and natural selection. In the model plant species Arabidopsis thaliana, recent studies of natural variation have led to the identification of genes underlying ecologically important complex traits, and provided new insights about the processes of genome evolution, geographic population structure, and the selective mechanisms shaping complex trait variation in natural populations. These advances illustrate the potential for a new synthesis to elucidate mechanisms for the adaptive evolution of complex traits from nucleotide sequences to real-world environments.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Alonso-Blanco, C., Mendez-Vigo, B. & Koornneef, M. From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. Int. J. Dev. Biol. 49, 717–732 (2005)

  2. 2

    Hoffmann, M. H. Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). J. Biogeogr. 29, 125–134 (2002)

  3. 3

    Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005)

  4. 4

    Schmid, K. J., Ramos-Onsins, S., Ringys-Beckstein, H., Weisshaar, B. & Mitchell-Olds, T. A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism. Genetics 169, 1601–1615 (2005)

  5. 5

    Wright, S. I. & Gaut, B. S. Molecular population genetics and the search for adaptive evolution in plants. Mol. Biol. Evol. 22, 506–519 (2005)

  6. 6

    Ometto, L., Glinka, S., De Lorenzo, D. & Stephan, W. Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosome-wide scan of DNA variation. Mol. Biol. Evol. 22, 2119–2130 (2005)

  7. 7

    Akey, J. M. et al. Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2, e286 (2004)

  8. 8

    Abbott, R. J. & Gomes, M. F. Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. Heredity 62, 411–418 (1989)

  9. 9

    Bustamante, C. D. et al. The cost of inbreeding in Arabidopsis. Nature 416, 531–534 (2002)

  10. 10

    Shimizu, K. K. et al. Darwinian selection on a selfing locus. Science 306, 2081–2084 (2004)

  11. 11

    Cork, J. M. & Purugganan, M. D. High-diversity genes in the Arabidopsis genome. Genetics 170, 1897–1911 (2005)

  12. 12

    Kroymann, J., Donnerhacke, S., Schnabelrauch, D. & Mitchell-Olds, T. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc. Natl Acad. Sci. USA 100, 14587–14592 (2003)

  13. 13

    Tian, D., Araki, H., Stahl, E., Bergelson, J. & Kreitman, M. Signature of balancing selection in Arabidopsis. Proc. Natl Acad. Sci. USA 99, 11525–11530 (2002)

  14. 14

    Turelli, M. & Barton, N. H. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G × E interactions. Genetics 166, 1053–1079 (2004)

  15. 15

    Schmid, K. et al. Evidence for a large-scale population structure of Arabidopsis thaliana from genome-wide single nucleotide polymorphism markers. Theor. Appl. Genet. 112, 1104–1114 (2006)

  16. 16

    Jorgensen, S. & Mauricio, R. Neutral genetic variation among wild North American populations of the weedy plant Arabidopsis thaliana is not geographically structured. Mol. Ecol. 13, 3403–3413 (2004)

  17. 17

    Bakker, E. G. et al. Distribution of genetic variation within and among local populations of Arabidopsis thaliana over its species range. Mol. Ecol. 15, 1405–1418 (2006)

  18. 18

    Le Corre, V. Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits. Mol. Ecol. 14, 4181–4192 (2005)

  19. 19

    Stenoien, H. K., Fenster, C. B., Tonteri, A. & Savolainen, O. Genetic variability in natural populations of Arabidopsis thaliana in northern Europe. Mol. Ecol. 14, 137–148 (2005)

  20. 20

    Koornneef, M., Alonso-Blanco, C. & Vreugdenhil, D. Naturally occurring genetic variation in Arabidopsis thaliana. Annu. Rev. Plant Biol. 55, 141–172 (2004)

  21. 21

    Bouche, N. & Bouchez, D. Arabidopsis gene knockout: phenotypes wanted. Curr. Opin. Plant Biol. 4, 111–117 (2001)

  22. 22

    Schmid, M. et al. A gene expression map of Arabidopsis thaliana development. Nature Genet. 37, 501–506 (2005)

  23. 23

    Lempe, J. et al. Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genetics 1, e6 (2005)

  24. 24

    Mackay, T. F. C. The genetic architecture of quantitative traits: lessons from Drosophila. Curr. Opin. Genet. Dev. 14, 253–257 (2004)

  25. 25

    Kroymann, J. & Mitchell-Olds, T. Epistasis and balanced polymorphism influencing complex trait variation. Nature 435, 95–98 (2005)

  26. 26

    Fishman, L., Kelly, A. & Willis, J. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56, 2138–2155 (2002)

  27. 27

    Gachon, C. M. M., Langlois-Meurinne, M., Henry, Y. & Saindrenan, P. Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications. Plant Mol. Biol. 58, 229–245 (2005)

  28. 28

    Kliebenstein, D. J. et al. Genomic survey of gene expression diversity in Arabidopsis thaliana. Genetics 172, 1179–1189 (2006)

  29. 29

    Vuylsteke, M., van Eeuwijk, F., Van Hummelen, P., Kuiper, M. & Zabeau, M. Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics 171, 1267–1275 (2005)

  30. 30

    DeCook, R., Lall, S., Nettleton, D. & Howell, S. H. Genetic regulation of gene expression during shoot development in Arabidopsis. Genetics 172, 1155–1164 (2006)

  31. 31

    de Meaux, J., Goebel, U., Pop, A. & Mitchell-Olds, T. Allele-specific assay reveals functional variation in the Chalcone Synthase promoter of Arabidopsis thaliana that is compatible with neutral evolution. Plant Cell 17, 676–690 (2005)

  32. 32

    Gibson, G. & Weir, B. The quantitative genetics of transcription. Trends Genet. 21, 616–623 (2005)

  33. 33

    Ungerer, M. C., Halldorsdottir, S. S., Purugganan, M. D. & Mackay, T. F. C. Genotype–environment interactions at quantitative trait loci affecting inflorescence development in Arabidopsis thaliana. Genetics 165, 353–365 (2003)

  34. 34

    Juenger, T. E., Sen, S., Stowe, K. A. & Simms, E. L. Epistasis and genotype–environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica 123, 87–105 (2005)

  35. 35

    Dilda, C. L. & Mackay, T. F. C. The genetic architecture of Drosophila sensory bristle number. Genetics 162, 1655–1674 (2002)

  36. 36

    Weinreich, D., Watson, R. & Chao, L. Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59, 1165–1174 (2005)

  37. 37

    Syed, N. H. & Chen, Z. J. Molecular marker genotypes, heterozygosity and genetic interactions explain heterosis in Arabidopsis thaliana. Heredity 94, 295–304 (2004)

  38. 38

    Hausmann, N. J. et al. Quantitative trait loci affecting delta C-13 and response to differential water availability in Arabidopsis thaliana. Evolution 59, 81–96 (2005)

  39. 39

    Kearsey, M., Pooni, H. & Syed, N. Genetics of quantitative traits in Arabidopsis thaliana. Heredity 91, 456–464 (2003)

  40. 40

    Malmberg, R. L., Held, S., Waits, A. & Mauricio, R. Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse. Genetics 171, 2013–2027 (2005)

  41. 41

    Michaels, S. D. & Amasino, R. M. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13, 935–942 (2001)

  42. 42

    Johanson, U. et al. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347 (2000)

  43. 43

    Weigel, D. & Nordborg, M. Natural variation in Arabidopsis. How do we find the causal genes? Plant Physiol. 138, 567–568 (2005)

  44. 44

    El-Assal, S. E.-D., Alonso-Blanco, C., Peeters, A. J. M., Raz, V. & Koornneef, M. A. QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nature Genet. 29, 435–440 (2001)

  45. 45

    Werner, J. D. et al. Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proc. Natl Acad. Sci. USA 102, 2460–2465 (2005)

  46. 46

    Puchta, H. & Hohn, B. Green light for gene targeting in plants. Proc. Natl Acad. Sci. USA 102, 11961–11962 (2005)

  47. 47

    Tian, D., Traw, M., Chen, J., Kreitman, M. & Bergelson, J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74–77 (2003)

  48. 48

    Werner, J. D. et al. FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170, 1197–1207 (2005)

  49. 49

    Hoffmann, M. H. Evolution of the realized climatic niche in the genus Arabidopsis (Brassicaceae). Evolution 59, 1425–1436 (2005)

  50. 50

    Pigliucci, M. in The Arabidopsis Book (eds Somerville, C. R. & Meyerowitz, E. M.) (American Society of Plant Biologists, Rockville, Maryland, 2002) doi:10.1199/tab.0009 (2002)

  51. 51

    Shindo, C. et al. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol. 138, 1163–1173 (2005)

  52. 52

    Thompson, L. The spatiotemporal effects of nitrogen and litter on the population dynamics of Arabidopsis thaliana. J. Ecol. 82, 63–68 (1994)

  53. 53

    Simpson, G. G. & Dean, C. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289 (2002)

  54. 54

    Michaels, S. D., He, Y., Scortecci, K. C. & Amasino, R. M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 10102–10107 (2003)

  55. 55

    Maloof, J. N. et al. Natural variation in light sensitivity of Arabidopsis. Nature Genet. 29, 441–446 (2001)

  56. 56

    Michael, T. P. et al. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302, 1049–1053 (2003)

  57. 57

    Stenoien, H. K., Fenster, C. B., Kuittinen, H. & Savolainen, O. Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 89, 1604–1608 (2002)

  58. 58

    Stinchcombe, J. R. et al. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc. Natl Acad. Sci. USA 101, 4712–4717 (2004)

  59. 59

    Kawecki, T. J. & Ebert, D. Conceptual issues in local adaptation. Ecol. Lett. 7, 1225–1241 (2004)

  60. 60

    Callahan, H. S. & Pigliucci, M. Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. Ecology 83, 1965–1980 (2002)

  61. 61

    Rausher, M. D. The measurement of selection on quantitative traits—biases due to environmental covariances between traits and fitness. Evolution 46, 616–626 (1992)

  62. 62

    Wade, M. J. & Kalisz, S. The causes of natural selection. Evolution 44, 1947–1955 (1990)

  63. 63

    Donohue, K. et al. The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59, 758–770 (2005)

  64. 64

    Callahan, H. S., Dhanoolal, N. & Ungerer, M. C. Plasticity genes and plasticity costs: a new approach using an Arabidopsis recombinant inbred population. New Phytol. 166, 129–139 (2005)

  65. 65

    Weinig, C. et al. Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165, 321–329 (2003)

  66. 66

    Verhoeven, K. J. F., Vanhala, T. K., Biere, A., Nevo, E. & Van Damme, J. M. M. The genetic basis of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats. Evolution 58, 270–283 (2004)

  67. 67

    Mauricio, R. et al. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163, 735–746 (2003)

  68. 68

    Shen, J., Araki, H., Chen, L., Chen, J.-Q. & Tian, D. Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172, 1243–1250 (2006)

  69. 69

    Korves, T. & Bergelson, J. A novel cost of R gene resistance in the presence of disease. Am. Nat. 163, 489–504 (2004)

  70. 70

    Siegal, M. L. & Hartl, D. L. Transgene coplacement and high efficiency site-specific recombination with the Cre/loxP system in Drosophila. Genetics 144, 715–726 (1996)

  71. 71

    Plagnol, V., Padhukasahasram, B., Wall, J. D., Marjoram, P. & Nordborg, M. Relative influences of crossing-over and gene conversion on the pattern of linkage disequilibrium in Arabidopsis thaliana. Genetics 172, 2441–2448 (2005)

  72. 72

    Yu, J. et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genet. 38, 203–208 (2006)

  73. 73

    Remington, D. L. et al. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl Acad. Sci. USA 98, 11479–11484 (2001)

  74. 74

    Aranzana, M. et al. Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genetics 1, e60 (2005)

  75. 75

    Schlotterer, C. Hitchhiking mapping—functional genomics from the population genetics perspective. Trends Genet. 19, 32–38 (2003)

Download references

Acknowledgements

We thank M. Noor, M. Nordborg and our collaborators and laboratory members for discussion and comments. T.M.-O. and J.S. were supported by Duke University and the National Science Foundation, respectively.

Author information

Affiliations

  1. Department of Biology, Duke University, PO Box 91000, North Carolina, 27708, Durham, USA

    • Thomas Mitchell-Olds
  2. Department of Ecology and Evolutionary Biology, Box G-W, Brown University, Providence, Rhode Island, 02912, USA

    • Johanna Schmitt

Authors

  1. Search for Thomas Mitchell-Olds in:

  2. Search for Johanna Schmitt in:

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding author

Correspondence to Thomas Mitchell-Olds.

About this article

Publication history

Issue Date

DOI

https://doi.org/10.1038/nature04878

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.