Comparative population genomics of maize domestication and improvement

Journal name:
Nature Genetics
Volume:
44,
Pages:
808–811
Year published:
DOI:
doi:10.1038/ng.2309
Received
Accepted
Published online

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.

At a glance

Figures

  1. Neighbor-joining tree and changing morphology of domesticated maize and its wild relatives.
    Figure 1: Neighbor-joining tree and changing morphology of domesticated maize and its wild relatives.

    Taxa in the neighbor-joining tree (right) are represented by different colors: parviglumis (green), landraces (red), improved lines (blue), mexicana (yellow) and Tripsacum (brown). Morphological changes (left) are shown for female inflorescences and plant architecture during domestication and improvement.

  2. Genome-wide analysis of nucleotide diversity and selection.
    Figure 2: Genome-wide analysis of nucleotide diversity and selection.

    (a) LOWESS curves of nucleotide diversity (π) along chromosome 1 in parviglumis (green), landraces (red) and improved lines (blue). (b,c) Genome-wide likelihood (XP-CLR) values for selection during domestication (b) and improvement (c), with chromosome number indicated along the x axis. (d,e) Distributions of feature size (d) and gene counts within features (e) in domestication and improvement scans. Whiskers indicate maximum and minimum of data, boxes span the interquartile range, and the solid line indicates the median.

  3. Domestication and improvement candidate genes in relation to two pathways in rice.
    Figure 3: Domestication and improvement candidate genes in relation to two pathways in rice.

    Z. mays genes are shown in boxes above the proteins encoded by their rice orthologs (filled blue circles). Candidate genes are on a gray background, and genes within a selected feature are in a dotted box. Negative regulation is indicated by a circle at the end of an arrow. (ac) Domestication candidate genes. (a) The flowering time pathway30, including GRMZM2G448355 and zagl1. (b) Seedling expression pattern of GRMZM2G448355 in parviglumis and maize inbreds. (c) XP-CLR and relative diversity near GRMZM2G448355; gene orientation is indicated by the arrow. (d) The gibberellin (GA) biosynthesis pathway31. The high-yielding rice variety IR8 has a mutation in GA20ox (shown on a green background)23. (e,f) XP-CLR values near the improvement candidates GRMZM2G152354 (e) and dwarf1 (f); gene orientation is indicated by the arrows.

Accession codes

Primary accessions

Gene Expression Omnibus

References

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Author information

  1. These authors contributed equally to this work.

    • Matthew B Hufford,
    • Xun Xu,
    • Joost van Heerwaarden &
    • Tanja Pyhäjärvi

Affiliations

  1. Department of Plant Sciences, University of California, Davis, California, USA.

    • Matthew B Hufford,
    • Joost van Heerwaarden,
    • Tanja Pyhäjärvi &
    • Jeffrey Ross-Ibarra
  2. BGI-Shenzhen, Shenzhen, China.

    • Xun Xu,
    • Chi Song,
    • Jun Wang,
    • Gengyun Zhang &
    • Shuang Yang
  3. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

    • Jer-Ming Chia &
    • Doreen Ware
  4. Center for Evolutionary Medicine and Informatics, Biodesign Institute, Arizona State University, Tempe, Arizona, USA.

    • Reed A Cartwright
  5. School of Life Sciences, Arizona State University, Tempe, Arizona, USA.

    • Reed A Cartwright
  6. Institute for Genomic Diversity, Cornell University, Ithaca, New York, USA.

    • Robert J Elshire,
    • Jeffrey C Glaubitz &
    • Edward S Buckler
  7. US Department of Agriculture–Agriculture Research Service (USDA-ARS).

    • Kate E Guill,
    • Michael D McMullen,
    • Doreen Ware &
    • Edward S Buckler
  8. Division of Plant Sciences, University of Missouri, Columbia, Missouri, USA.

    • Kate E Guill &
    • Michael D McMullen
  9. Department of Energy (DOE) Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin, USA.

    • Shawn M Kaeppler
  10. Department of Agronomy, University of Wisconsin, Madison, Wisconsin, USA.

    • Shawn M Kaeppler
  11. State Key Laboratory of Agrobiotechnology, China Agricultural University, Beijing, China.

    • Jinsheng Lai
  12. Department of Agronomy & Plant Genetics, University of Minnesota, St Paul, Minnesota, USA.

    • Peter L Morrell
  13. Department of Genetics, University of Wisconsin, Madison, Wisconsin, USA.

    • Laura M Shannon &
    • John Doebley
  14. Department of Plant Biology, University of Minnesota, St Paul, Minnesota, USA.

    • Nathan M Springer,
    • Ruth A Swanson-Wagner &
    • Peter Tiffin
  15. The Genome Center, University of California, Davis, California, USA.

    • Jeffrey Ross-Ibarra
  16. The Center for Population Biology, University of California, Davis, California, USA.

    • Jeffrey Ross-Ibarra

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

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Supplementary information

PDF files

  1. Supplementary Text and Figures (10 MB)

    Supplementary Note, Supplementary Tables 1–5, 8 and 9 and Supplementary Figures 1–15

Excel files

  1. Supplementary Table 6 (190 KB)

    Domestication candidates

  2. Supplementary Table 7 (168 KB)

    Improvement candidates

Additional data