Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica)

Abstract

Foxtail millet (Setaria italica) is an important grain crop that is grown in arid regions. Here we sequenced 916 diverse foxtail millet varieties, identified 2.58 million SNPs and used 0.8 million common SNPs to construct a haplotype map of the foxtail millet genome. We classified the foxtail millet varieties into two divergent groups that are strongly correlated with early and late flowering times. We phenotyped the 916 varieties under five different environments and identified 512 loci associated with 47 agronomic traits by genome-wide association studies. We performed a de novo assembly of deeply sequenced genomes of a Setaria viridis accession (the wild progenitor of S. italica) and an S. italica variety and identified complex interspecies and intraspecies variants. We also identified 36 selective sweeps that seem to have occurred during modern breeding. This study provides fundamental resources for genetics research and genetic improvement in foxtail millet.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Geographic distribution and genetic structures of 916 foxtail millet varieties.
Figure 2: Regions of the genome showing association signals underlying multiple agronomic traits.
Figure 3: Whole-genome screening and functional annotations of selective sweeps during modern breeding.

Accession codes

Primary accessions

European Nucleotide Archive

References

  1. Barton, L. et al. Agricultural origins and the isotopic identity of domestication in northern China. Proc. Natl. Acad. Sci. USA 106, 5523–5528 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bettinger, R.L., Barton, L. & Morgan, C. The origins of food production in north China: a different kind of agricultural revolution. Evol. Anthropol. 19, 9–21 (2010).

    Article  Google Scholar 

  3. Doust, A.N., Kellogg, E.A., Devos, K.M. & Bennetzen, J.L. Foxtail millet: a sequence-driven grass model system. Plant Physiol. 149, 137–141 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Brutnell, T.P. et al. Setaria viridis: a model for C4 photosynthesis. Plant Cell 22, 2537–2544 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Li, P. & Brutnell, T.P. Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses. J. Exp. Bot. 62, 3031–3037 (2011).

    Article  CAS  PubMed  Google Scholar 

  6. Lata, C., Gupta, S. & Prasad, M. Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses. Crit. Rev. Biotechnol. published online, http://dx.doi.org/10.3109/07388551.2012.716809 (18 September 2012).

  7. Doust, A.N., Devos, K.M., Gadberry, M.D., Gale, M.D. & Kellogg, E.A. Genetic control of branching in foxtail millet. Proc. Natl. Acad. Sci. USA 101, 9045–9050 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Doust, A.N., Devos, K.M., Gadberry, M.D., Gale, M.D. & Kellogg, E.A. The genetic basis for inflorescence variation between foxtail and green millet (poaceae). Genetics 169, 1659–1672 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wang, C. et al. Population genetics of foxtail millet and its wild ancestor. BMC Genet. 11, 90 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wang, C. et al. Genetic diversity and population structure of Chinese foxtail millet (Setaria italica (L.) Beauv.) landraces. G3 (Bethesda) 2, 769–777 (2012).

    Article  CAS  Google Scholar 

  11. Bennetzen, J.L. et al. Reference genome sequence of the model plant Setaria. Nat. Biotechnol. 30, 555–561 (2012).

    Article  CAS  PubMed  Google Scholar 

  12. Zhang, G. et al. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat. Biotechnol. 30, 549–554 (2012).

    Article  CAS  PubMed  Google Scholar 

  13. Weigel, D. & Mott, R. The 1001 genomes project for Arabidopsis thaliana. Genome Biol. 10, 107 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Schneeberger, K. et al. Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proc. Natl. Acad. Sci. USA 108, 10249–10254 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961–967 (2010).

    Article  CAS  PubMed  Google Scholar 

  17. Huang, X. et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat. Genet. 44, 32–39 (2012).

    Article  Google Scholar 

  18. Lin, Z. et al. Parallel domestication of the Shattering1 genes in cereals. Nat. Genet. 44, 720–724 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kang, H.M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348–354 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Buckler, E.S. et al. The genetic architecture of maize flowering time. Science 325, 714–718 (2009).

    Article  CAS  PubMed  Google Scholar 

  21. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Higgins, J.A., Bailey, P.C. & Laurie, D.A. Comparative genomics of flowering time pathway using Brachypodium distachyon as model for the temperate grasses. PLoS ONE 5, e10065 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Singh, M. et al. Activator mutagenesis of the pink scutellum1/viviparous7 locus of maize. Plant Cell 15, 874–884 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Saitoh, K., Onishi, K., Mikami, I., Thidar, K. & Sano, Y. Allelic diversification at the C (OsC1) locus of wild and cultivated rice: nucleotide changes associated with phenotypes. Genetics 168, 997–1007 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Radicella, J.P., Turks, D. & Chandler, V.L. Cloning and nucleotide sequence of a cDNA encoding B-Peru, a regulatory protein of the anthocyanin pathway in maize. Plant Mol. Biol. 17, 127–130 (1991).

    Article  CAS  PubMed  Google Scholar 

  26. Yano, M. et al. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473–2484 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Morrell, P.L., Buckler, E.S. & Ross-Ibarra, J. Crop genomics: advances and applications. Nat. Rev. Genet. 13, 85–96 (2011).

    Article  PubMed  Google Scholar 

  28. Hufford, M.B. et al. Comparative population genomics of maize domestication and improvement. Nat. Genet. 44, 808–811 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Konishi, S. et al. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392–1396 (2006).

    Article  CAS  PubMed  Google Scholar 

  31. Meuwissen, T.H.E., Hayes, B.J. & Goddard, M.E. Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 1819–1829 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Kozarewa, I. et al. Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat. Methods 6, 291–295 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mullikin, J.C. & Ning, Z. The phusion assembler. Genome Res. 13, 81–90 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. de la Bastide, M. & McCombie, W.R. Assembling genomic DNA sequences with PHRAP. Curr. Protoc. Bioinformatics Chap. 11 unit 11.14 (2007).

  35. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277 (2000).

    Article  CAS  PubMed  Google Scholar 

  37. Barrett, J.C., Fry, B., Maller, J. & Daly, M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265 (2005).

    Article  CAS  PubMed  Google Scholar 

  38. Churchill, G.A. & Doerge, R.W. Empirical threshold values for quantitative trait mapping. Genetics 138, 963–971 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Felsenstein, J. PHYLIP: Phylogeny Inference Package (version 3.2). Cladistics 5, 164–166 (1989).

    Google Scholar 

Download references

Acknowledgements

We thank J. Chen from the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, for discussion about the manuscript. We thank Z. Ning for assistance with sequence alignment. This work was supported by the China Agricultural Research System (CARS07-12.5-A02), the National Natural Science Foundation of China (31171560, 30630045 and 31121063), the National High Technology Research and Development Program of China (863 Program) (2013AA102603), the National Fund for Genetically Modified Organisms of China (2009ZX08009-093B), the Ministry of Agriculture of China (2011ZX08009-002) and the Chinese Academy of Sciences.

Author information

Authors and Affiliations

Authors

Contributions

B.H., X.D. and J. Li conceived the project and its components. H.Z., P.L., B. Zhao and X.D. collected samples. H.Z., G.J., H. Liu, Y.C., Y. Li, E.G., Shujun Wang, J.L., Suying Wang, W.Z., G.C., B. Zhang, L.Y., H.H., Y.W., Wei Li, N.Z. and H. Li performed the phenotyping. L.Z. contributed to evolutionary and functional analyses. G.J., Wenjun Li, Y.G., Y. Lu, C. Zhou, D.F., Q.W. and Q.F. performed the genome sequencing. X.H. and Y.Z. performed GWAS and population genetics analysis. Q.Z., K.L., H. Lu, C. Zhu, T.H., L.Z. and T.L. performed genome data analysis. Y.Z. and X.H. prepared figures and tables. X.H., X.D. and B.H. analyzed the total data and wrote the paper.

Corresponding authors

Correspondence to Jiayang Li, Xianmin Diao or Bin Han.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–54, Supplementary Tables 2–15 (PDF 15733 kb)

Supplementary Table 1

The list of 916 foxtail millet accessions (Setaria italica) sampled in the collection. (XLS 163 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Jia, G., Huang, X., Zhi, H. et al. A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 45, 957–961 (2013). https://doi.org/10.1038/ng.2673

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.2673

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing