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Whole-genome duplication as a key factor in crop domestication

Nature Plants volume 2, Article number: 16115 (2016) Cite this article

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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 crops1–4. Furthermore, the genetic consequences of polyploidy5–7 might have increased the adaptive plasticity of those plants, enabling successful domestication6–8. 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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Figure 1: Polyploidy frequency across different categories of commodity use.

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References

  1. Meyer, R. S., DuVal, A. E. & Jensen, H. R. Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol. 196, 29–48 (2012).

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  4. Ross-Ibarra, J., Morrell, P. L. & Gaut, B. S. Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc. Natl Acad. Sci. USA 104, 8641–8648 (2007).

    Article  CAS  Google Scholar 

  5. Pecinka, A., Fang, W., Rehmsmeier, M., Levy, A. A. & Scheid, O. M. Polyploidization increases meiotic recombination frequency in Arabidopsis. BMC Biol. 9, 24 (2011).

    Article  Google Scholar 

  6. Renny-Byfield, S. & Wendel, J. F. Doubling down on genomes: polyploidy and crop plants. Am. J. Bot. 101, 1711–1725 (2014).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Udall, J. A. & Wendel, J. F. Polyploidy and crop improvement. Crop Sci. 46, S-3–S-14 (2006).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  11. Emshwiller, E. 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).

    Google Scholar 

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

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Plant DNA C-values database. http://data.kew.org/cvalues (2012).

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  22. Ramsey, J. & Schemske, D. W. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33, 589–639 (2002).

    Article  Google Scholar 

  23. Fuller, D. Q. & Harvey, E. L. The archaeobotany of Indian pulses: identification, processing and evidence for cultivation. Environ. Archaeol. 11, 219–246 (2006).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  26. Dempewolf, H., Hodgins, K. A., Rummell, S. E., Ellstrand, N. C. & Rieseberg, L. H. Reproductive isolation during domestication. Plant Cell 24, 2710–2717 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Huelsenbeck, J. P., Nielsen, R. & Bollback, J. P. Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003).

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  31. R Foundation for Statistical Computing. A Language and Environment for Statistical Computing (R Core Team, 2013); https://www.R-project.org/

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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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.

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Author notes

  1. Ayelet Salman-Minkov and Niv Sabath: These authors contributed equally to this work.

Authors and 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. Ayelet Salman-Minkov
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  2. Niv Sabath
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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.

Corresponding author

Correspondence to Itay Mayrose.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figure 1, Supplementary Tables 1 and 2, Supplementary References (PDF 441 kb)

Supplementary Figure 2

Inference of the temporal order of polyploidy and domestication events for all genera (PDF 272 kb)

Supplementary Table 3

Table of crop species by FAO commodity groups (XLSX 19 kb)

Supplementary Table 4

Table of loci used for each genus in reconstructing the phylogenetic trees (XLSX 20 kb)

Supplementary Table 5

Table of species names and categories (XLSX 199 kb)

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" (ZIP 127013 kb)

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Salman-Minkov, A., Sabath, N. & Mayrose, I. Whole-genome duplication as a key factor in crop domestication. Nature Plants 2, 16115 (2016). https://doi.org/10.1038/nplants.2016.115

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