Letter

Whole-genome duplication as a key factor in crop domestication

  • Nature Plants 2, Article number: 16115 (2016)
  • doi:10.1038/nplants.2016.115
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Abstract

Polyploidy is commonly thought to be associated with the domestication process because of its concurrence with agriculturally favourable traits and because it is widespread among the major plant crops1,​2,​3,​4. Furthermore, the genetic consequences of polyploidy5,​6,​7 might have increased the adaptive plasticity of those plants, enabling successful domestication6,​7,​8. Nevertheless, a detailed phylogenetic analysis regarding the association of polyploidy with the domestication process, and the temporal order of these distinct events, has been lacking3. Here, we have gathered a comprehensive data set including dozens of genera, each containing one or more major crop species and for which sufficient sequence and chromosome number data exist. Using probabilistic inference of ploidy levels conducted within a phylogenetic framework, we have examined the incidence of polyploidization events within each genus. We found that domesticated plants have gone through more polyploidy events than their wild relatives, with monocots exhibiting the most profound difference: 54% of the crops are polyploids versus 40% of the wild species. We then examined whether the preponderance of polyploidy among crop species is the result of two, non-mutually-exclusive hypotheses: (1) polyploidy followed by domestication, and (2) domestication followed by polyploidy. We found support for the first hypothesis, whereby polyploid species were more likely to be domesticated than their wild relatives, suggesting that the genetic consequences of polyploidy have conferred genetic preconditions for successful domestication on many of these plants.

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References

  1. 1.

    , & Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol. 196, 29–48 (2012).

  2. 2.

    in Plant Breeding Reviews: Long-term Selection: Crops, Animals, and Bacteria Vol. 24 (ed. Janick, J.) 1–44 (John Wiley & Sons, Inc., 2004).

  3. 3.

    Perspectives on polyploidy in plants–ancient and neo. Biol. J. Linn. Soc. Lond. 82, 411–423 (2004).

  4. 4.

    , & Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc. Natl Acad. Sci. USA 104, 8641–8648 (2007).

  5. 5.

    , , , & Polyploidization increases meiotic recombination frequency in Arabidopsis. BMC Biol. 9, 24 (2011).

  6. 6.

    & Doubling down on genomes: polyploidy and crop plants. Am. J. Bot. 101, 1711–1725 (2014).

  7. 7.

    Polyploidy, evolutionary opportunity, and crop adaptation. Genetica 123, 191–196 (2005).

  8. 8.

    & Polyploidy and crop improvement. Crop Sci. 46, S-3–S-14 (2006).

  9. 9.

    Evolution, consequences and future of plant and animal domestication. Nature 418, 700–707 (2002).

  10. 10.

    The domestication syndrome. Die Kulturpflanze 32, 11–34 (1984).

  11. 11.

    in Documenting Domestication: New Genetic And Archaeological Paradigms (eds Zeder, M. A., Bradley, D., Emshwiller, E. & Smith, B. D.) Ch. 12 (Univ. of California Press, 2006).

  12. 12.

    in Polyploidy: biological relevance (ed. Lewis, W. H.) 385–407 (Plenum, 1980).

  13. 13.

    Contributions of domesticated plant studies to our understanding of plant evolution. Ann. Bot. 96, 953–963 (2005).

  14. 14.

    Polyploidy and the evolution of domesticated plants. Am. J. Bot. 1494–1499 (1993).

  15. 15.

    et al. The chromosome counts database (CCDB)–a community resource of plant chromosome numbers. New Phytol. 206, 19–26 (2015).

  16. 16.

    & ChromEvol: assessing the pattern of chromosome number evolution and the inference of polyploidy along a phylogeny. Mol. Biol. Evol. 31, 1914–1922 (2014).

  17. 17.

    Plant DNA C-values database. (2012).

  18. 18.

    et al. The frequency of polyploid speciation in vascular plants. Proc. Natl Acad. Sci. USA 106, 13875–13879 (2009).

  19. 19.

    Cytological characteristics associated with the different growth habits in the dicotyledons. Am. J. Bot. 25, 189–198 (1938).

  20. 20.

    Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Ann. Bot. 100, 903–924 (2007).

  21. 21.

    in Grass Systematics and Evolution (eds Soderstorm, T. R., Hilu, K. W., Campbell, C. S. & Barkworth, M. A.) 188–194 (Smithsonian Institution Press, 1987).

  22. 22.

    & Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33, 589–639 (2002).

  23. 23.

    & The archaeobotany of Indian pulses: identification, processing and evidence for cultivation. Environ. Archaeol. 11, 219–246 (2006).

  24. 24.

    et al. Induced polyploidy dramatically increases the size and alters the shape of fruit in Actinidia chinensis. Ann. Bot. 109, 169–179 (2012).

  25. 25.

    et al. The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19–45 (2011).

  26. 26.

    , , , & Reproductive isolation during domestication. Plant Cell 24, 2710–2717 (2012).

  27. 27.

    et al. Serendipitous backyard hybridization and the origin of crops. Proc. Natl Acad. Sci. USA 104, 14389–14394 (2007).

  28. 28.

    , & Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003).

  29. 29.

    Guns, Germs, and Steel. The Fates of Human Societies (WW Norton & Company, 1999).

  30. 30.

    et al. Polyploidy can drive rapid adaptation in yeast. Nature 519, 349–352 (2015).

  31. 31.

    R Foundation for Statistical Computing. A Language and Environment for Statistical Computing (R Core Team, 2013);

  32. 32.

    Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084–1092 (2012).

  33. 33.

    et al. Karyotypic changes through dysploidy persist longer over evolutionary time than polyploid changes. PLoS ONE 9, e85266 (2014).

  34. 34.

    et al. Recently formed polyploid plants diversify at lower rates. Science 333, 1257–1257 (2011).

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Acknowledgements

We thank A. A. Levy and A. Rice for helpful discussions and suggestions. This study was supported by a post-doctoral fellowship to N.S. from the Edmond J. Safra postdoctoral fellowship and the Israel Science Foundation (1265/12) to I.M.

Author information

Author notes

    • Ayelet Salman-Minkov
    •  & Niv Sabath

    These authors contributed equally to this work.

Affiliations

  1. Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, Israel

    • Ayelet Salman-Minkov
    • , Niv Sabath
    •  & Itay Mayrose

Authors

  1. Search for Ayelet Salman-Minkov in:

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Contributions

The authors contributed in the following ways: conceptualization, I.M.; methodology, A.S.-M., N.S. and I.M.; software, N.S.; validation, A.S.-M. and I.M.; formal analysis, A.S.-M. and N.S.; investigation, A.S.-M. and N.S.; writing, A.S.-M., N.S. and I.M.; supervision, I.M.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Itay Mayrose.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Methods, Supplementary Figure 1, Supplementary Tables 1 and 2, Supplementary References

  2. 2.

    Supplementary Figure 2

    Inference of the temporal order of polyploidy and domestication events for all genera

Excel files

  1. 1.

    Supplementary Table 3

    Table of crop species by FAO commodity groups

  2. 2.

    Supplementary Table 4

    Table of loci used for each genus in reconstructing the phylogenetic trees

  3. 3.

    Supplementary Table 5

    Table of species names and categories

Zip files

  1. 1.

    Supplementary Data

    MSAs - The multiple sequence alignments for each genus. Trees - The set of bayesian phylogenetic trees reconstructed for each genus. analysis_script.R - This R script executes the temporal order of polyploidy and domestication analysis. Fragaria.RData - This is an RData file that contains the data for the genus Fragaria for example. It can be used for running the R script "analysis_script.R"