Comparative population genomics of maize domestication and improvement

Abstract

Domestication and plant breeding are ongoing 10,000-year-old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution1,2, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines3. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes4,5. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.

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Figure 1: Neighbor-joining tree and changing morphology of domesticated maize and its wild relatives.
Figure 2: Genome-wide analysis of nucleotide diversity and selection.
Figure 3: Domestication and improvement candidate genes in relation to two pathways in rice.

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Acknowledgements

The authors would like to thank T. Kono, S. Watson and M. Watson for photographs of inflorescences, P. Brown for help with QTL delineation, B.S. Gaut, A.M. Gonzales and two anonymous reviewers for comments on an earlier version of the manuscript and M. Grote for statistical advice. This work was supported by funding to the maize diversity project from the US National Science Foundation (NSF; IOS-0820619 to E.S.B., J.D. and M.D.M.) and USDA-ARS (to E.S.B., M.D.M. and D.W.), as well as from USDA Hatch Funds (to P.T. and N.M.S.), the Chinese 973 program (2007CB815701 to J.W.), the Chinese Ministry of Agriculture 984 program (2010-Z13 to G.Z.), the Shenzhen Municipal Government Basic Research Program (to J.W.), the US DOE Great Lakes Bioenergy Research Center (DOE Office of Science; BER DE-FC02-07ER64494), the Office of Science of the US DOE (contract DE-AC02-05CH11231 to the US DOE Joint Genome Institute) and by grants from the US NSF (IOS-0922703 to J.R.-I.) and the USDA–National Institute of Food and Agriculture (2009-01864 to J.R.-I.).

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Contributions

J.D., M.D.M., E.S.B., D.W. and J.R.-I. designed the project. M.B.H., J.v.H., T.P. and J.R.-I. performed most data analyses. J.D. developed wild and landrace inbred lines. E.S.B., S.M.K., J.L., M.D.M. and D.W. contributed sequence data for inbred maize and parviglumis. K.E.G. and R.J.E. developed libraries and managed sequencing for inbred maize and parviglumis. X.X., S.Y., J.W. and G.Z. directed sequencing for landrace maize, mexicana and Tripsacum. E.S.B., J.R.-I., D.W. and X.X. directed bioinformatics analyses. J.-M.C. and C.S. performed read mapping, SNP calling and annotation, and analysis of coding sequence. E.S.B., J.-M.C. and J.C.G. performed quality control filtering of SNPs. N.M.S., R.A.S.-W. and P.T. generated Nimblegen expression data for maize and parviglumis. S.M.K. provided early access expression data. L.M.S. reanalyzed QTL data for domestication traits. R.A.C. analyzed site frequency spectra. M.B.H., J.v.H., T.P., P.L.M. and J.R.-I. wrote the manuscript.

Corresponding authors

Correspondence to Edward S Buckler or Shuang Yang or Jeffrey Ross-Ibarra.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Note, Supplementary Tables 1–5, 8 and 9 and Supplementary Figures 1–15 (PDF 10057 kb)

Supplementary Table 6

Domestication candidates (XLSX 189 kb)

Supplementary Table 7

Improvement candidates (XLSX 163 kb)

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Hufford, M., Xu, X., van Heerwaarden, J. et al. Comparative population genomics of maize domestication and improvement. Nat Genet 44, 808–811 (2012). https://doi.org/10.1038/ng.2309

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