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.

  • Letter
  • Published:

The origin of the naked grains of maize

Abstract

The most critical step in maize (Zea mays ssp. mays) domestication was the liberation of the kernel from the hardened, protective casing that envelops the kernel in the maize progenitor, teosinte1. This evolutionary step exposed the kernel on the surface of the ear, such that it could readily be used by humans as a food source. Here we show that this key event in maize domestication is controlled by a single gene (teosinte glume architecture or tga1), belonging to the SBP-domain family2 of transcriptional regulators. The factor controlling the phenotypic difference between maize and teosinte maps to a 1-kilobase region, within which maize and teosinte show only seven fixed differences in their DNA sequences. One of these differences encodes a non-conservative amino acid substitution and may affect protein function, and the other six differences potentially affect gene regulation. Molecular evolution analyses show that this region was the target of selection during maize domestication. Our results demonstrate that modest genetic changes in single genes can induce dramatic changes in phenotype during domestication and evolution.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Phenotypes.
Figure 2: The tga1 locus.
Figure 3: Molecular analysis of tga1.
Figure 4: Tissue in situ hybridizations.
Figure 5: Molecular evolution.

Similar content being viewed by others

References

  1. Dorweiler, J., Stec, A., Kermicle, J. & Doebley, J. Teosinte glume architecture1: A genetic locus controlling a key step in maize evolution. Science 262, 233–235 (1993)

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Klein, J., Saedler, H. & Huijser, P. A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol. Gen. Genet. 250, 7–16 (1996)

    CAS  PubMed  Google Scholar 

  3. Doebley, J. The genetics of maize evolution. Annu. Rev. Genet. 38, 37–59 (2004)

    Article  CAS  PubMed  Google Scholar 

  4. Maynard Smith, J. Macroevolution. Nature 289, 13–14 (1981)

    Article  Google Scholar 

  5. Mangelsdorf, P. C. & Reeves, R. G. The origin of maize. Proc. Natl Acad. Sci. USA 24, 303–312 (1938)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wilkes, H. G. Teosinte: The Closest Relative of Maize (Bussey Institution of Harvard Univ., Cambridge, 1967)

    Google Scholar 

  7. Dorweiler, J. & Doebley, J. Developmental analysis of teosinte glume architecture1: a key locus in the evolution of maize (Poaceae). Am. J. Bot. 84, 1313–1322 (1997)

    Article  CAS  PubMed  Google Scholar 

  8. Doebley, J. & Stec, A. Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134, 559–570 (1993)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Tenaillon, M. I., U'Ren, J., Tenaillon, O. & Gaut, B. S. Selection versus demography: A multilocus investigation of the domestication process in maize. Mol. Biol. Evol. 21, 1214–1225 (2004)

    Article  CAS  PubMed  Google Scholar 

  10. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989)

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Hudson, R. R., Kreitman, M. & Aguade, M. A. test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. White, S. E. & Doebley, J. F. The molecular evolution of terminal ear1, a regulatory gene in the genus Zea. Genetics 153, 1455–1462 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Clark, R. M., Linton, E., Messing, J. & Doebley, J. F. Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc. Natl Acad. Sci. USA 101, 700–707 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Kim, Y. & Stephan, W. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160, 765–777 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Przeworski, M. Estimating the time since the fixation of a beneficial allele. Genetics 164, 1667–1676 (2003)

    PubMed  PubMed Central  Google Scholar 

  16. Beadle, G. W. Teosinte and the origin of maize. J. Hered. 30, 245–247 (1939)

    Article  Google Scholar 

  17. Cong, B., Liu, J. & Tanksley, S. D. Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proc. Natl Acad. Sci. USA 99, 13606–13611 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  18. Doebley, J., Stec, A. & Hubbard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997)

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Nesbitt, T. C. & Tanksley, S. D. Comparative sequencing in the genus Lycopersicon. Implications for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162, 365–379 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Purugganan, M. D., Boyles, A. L. & Suddith, J. I. Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics 155, 855–862 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Darwin, C. On The Origin of Species by Means of Natural Selection (John Murray, London, 1859)

    Google Scholar 

  22. Gottlieb, L. D. Genetics and morphological evolution in plants. Am. Naturalist 123, 681–709 (1984)

    Article  Google Scholar 

  23. Lande, R. The response to selection on major and minor mutations affecting a metrical trait. Heredity 50, 47–65 (1983)

    Article  Google Scholar 

  24. Jackson, D. in Plant Molecular Pathology: A Practical Approach (eds Gurr, S. J., McPherson, M. J. & Bowles, D. J.) 163–174 (Oxford Univ. Press, Oxford, 1992)

    Google Scholar 

  25. Rozas, J. & Rozas, R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175 (1999)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank D. Baum and J. Wendel for comments, R. Clark for helpful discussions; E. Ananiev, K. Fengler and M. Morgante for help with screening and identifying BAC contigs; the DuPont sequencing group for BAC sequencing; and P. Rose for assistance with genetic mapping. This research was supported in part by grants from the National Institutes of Health and the USDA Hatch program (to J.F.D.), a Howard Hughes Medical Institute predoctoral fellowship (to K.B.), and an Environmental Protection Agency predoctoral fellowship (to L.L).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John F. Doebley.

Ethics declarations

Competing interests

All sequences have been deposited in GenBank under accession numbers AY883436–AY883568. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

Includes Supplementary Methods, Supplementary Results, Supplementary Tables S1-S3 and Supplementary Figures. (DOC 519 kb)

Supplementary Figure S1

An enlarged version of Figures 1f-h from the main text. (PDF 47 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, H., Nussbaum-Wagler, T., Li, B. et al. The origin of the naked grains of maize. Nature 436, 714–719 (2005). https://doi.org/10.1038/nature03863

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03863

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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