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 role of barren stalk1 in the architecture of maize

Nature volume 432, pages 630–635 (2004)Cite this article

Abstract

The architecture of higher plants is established through the activity of lateral meristems—small groups of stem cells formed during vegetative and reproductive development. Lateral meristems generate branches and inflorescence structures, which define the overall form of a plant1,2,3, and are largely responsible for the evolution of different plant architectures3. Here, we report the isolation of the barren stalk1 gene, which encodes a non-canonical basic helix–loop–helix protein required for the initiation of all aerial lateral meristems in maize. barren stalk1 represents one of the earliest genes involved in the patterning of maize inflorescences, and, together with the teosinte branched1 gene4, it regulates vegetative lateral meristem development. The architecture of maize has been a major target of selection for early agriculturalists and modern farmers, because it influences harvesting, breeding strategies and mechanization. By sampling nucleotide diversity in the barren stalk1 region, we show that two haplotypes entered the maize gene pool from its wild progenitor, teosinte, and that only one was incorporated throughout modern inbreds, suggesting that barren stalk1 was selected for agronomic purposes.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Effects of ba1 mutations on maize development.
Figure 2: barren stalk1 encodes a non-canonical bHLH protein.
Figure 3: barren stalk1 expression by in situ hybridization.
Figure 4: barren stalk1 as a candidate for QTL 3L.

Similar content being viewed by others

References

  1. Weigel, D. & Jürgens, G. Stem cells that make stems. Nature 415, 751–754 (2002)

    Article  ADS  CAS  Google Scholar 

  2. Komatsu, K. et al. LAX and SPA: major regulators of shoot branching in rice. Proc. Natl Acad. Sci. USA 100, 11765–11770 (2003)

    Article  ADS  CAS  Google Scholar 

  3. Sussex, I. M. & Kerk, N. M. The evolution of plant architecture. Curr. Opin. Plant Biol. 4, 33–37 (2001)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  5. Hofmeyr, J. D. J. The Inheritance and Linkage Relationships of barren stalk-1 and barren stalk-2, Two Mature-Plant Characters of Maize. Thesis, Cornell Univ., Ithaca, New York (1931)

    Google Scholar 

  6. Ritter, M. K., Padilla, C. M. & Schmidt, R. J. The maize mutant barren stalk1 is defective in axillary meristem development. Am. J. Bot. 89, 203–210 (2002)

    Article  Google Scholar 

  7. Kapitonov, V. V. & Jurka, J. Rolling-circle transposons in eukaryotes. Proc. Natl Acad. Sci. USA 98, 8714–8719 (2001)

    Article  ADS  CAS  Google Scholar 

  8. Massari, M. E. & Murre, C. Helix-loop-helix proteins: regulators of transcription in eukaryotic organisms. Mol. Cell. Biol. 20, 429–440 (2000)

    Article  CAS  Google Scholar 

  9. Toledo-Ortiz, G. E., Huq, E. & Quail, P. H. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15, 1749–1770 (2003)

    Article  CAS  Google Scholar 

  10. Liljegren, S. J. et al. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116, 843–853 (2004)

    Article  CAS  Google Scholar 

  11. Cheng, P. C., Greyson, R. I. & Walden, D. B. Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am. J. Bot. 70, 450–462 (1983)

    Article  Google Scholar 

  12. Irish, E. E. Class II tassel seed mutations provide evidence for multiple types of inflorescence meristems in maize (Poaceae). Am. J. Bot. 84, 1502–1515 (1997)

    Article  CAS  Google Scholar 

  13. Ambrose, B. A. et al. Molecular and genetic analysis of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5, 569–579 (2000)

    Article  CAS  Google Scholar 

  14. Taguchi-Shiobara, F., Yuan, Z., Hake, S. & Jackson, D. The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15, 2755–2766 (2001)

    Article  CAS  Google Scholar 

  15. McSteen, P. & Hake, S. barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128, 2881–2891 (2001)

    CAS  PubMed  Google Scholar 

  16. Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003)

    Article  ADS  CAS  Google Scholar 

  17. Benkova, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003)

    Article  CAS  Google Scholar 

  18. Buckler, E. S. IV, Thornsberry, J. M. & Kresovich, S. Molecular diversity, structure and domestication of grasses. Genet. Res. Camb. 77, 213–218 (2001)

    Article  CAS  Google Scholar 

  19. Doebley, J., Stec, A. & Gustus, C. teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141, 333–346 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Wang, R. L., Stec, A., Hey, J., Lukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236–239 (1999)

    Article  ADS  CAS  Google Scholar 

  21. Hubbard, L., McSteen, P., Doebley, J. & Hake, S. Expression pattern and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte. Genetics 162, 1927–1935 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 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  Google Scholar 

  23. Lukens, L. & Doebley, J. Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genet. Res. Camb. 74, 291–302 (1999)

    Article  CAS  Google Scholar 

  24. Tenaillon, M. I. et al. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc. Natl Acad. Sci. USA 98, 9161–9166 (2001)

    Article  ADS  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Hudson, 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 

  27. Whitt, S. R., Wilson, L. M., Tenaillon, M. I., Gaut, B. S. & Buckler, E. S. IV Genetic diversity and selection in the maize starch pathway. Proc. Natl Acad. Sci. USA 99, 12959–12962 (2002)

    Article  ADS  CAS  Google Scholar 

  28. Bensen, R. J. et al. Cloning and characterization of the maize An1 gene. Plant Cell 7, 75–84 (1995)

    Article  CAS  Google Scholar 

  29. Dinneny, J. R., Yadegari, R., Fischer, R. L., Yanofsky, M. F. & Weigel, D. The role of JAGGED in shaping lateral organs. Development 131, 1101–1110 (2004)

    Article  CAS  Google Scholar 

  30. 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  Google Scholar 

Download references

Acknowledgements

We thank C. J. Whipple for the pictures in Figs 1m and 3b, c, and for discussions; M. Zanis and S. Jeong for critical reading of the manuscript; M. J. Galli for suggestions on quantitative PCR; E. York for assistance with SEMs at the Scripps Institution of Oceanography Analytical Facility; and A. Tsai, E. Durbin and D. Nakamura for technical help. This research was supported by NSF and NIH grants to R.J.S. and J.F.D. A.G. was also supported by MIUR, Ministero dell'Istruzione, dell'Universitá e della Ricerca, Italy.

Author information

Author notes

  1. Matthew K. Ritter

    Present address: Biological Sciences Department, California Polytechnic State University, San Luis Obispo, California, 93407, USA

Authors and Affiliations

  1. Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, California, 92093-0116, USA

    Andrea Gallavotti, Matthew K. Ritter & Robert J. Schmidt

  2. Dipartimento di Scienze Biomolecolari e Biotecnologie, Università degli Studi di Milano, 20133, Milan, Italy

    Andrea Gallavotti & M. Enrico Pè

  3. Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin, 53706, USA

    Qiong Zhao & John F. Doebley

  4. Graduate School of Agriculture and Life Science, The University of Tokyo, 113-8657, Tokyo, Japan

    Junko Kyozuka

  5. Crop Genetics Research, Pioneer-A DuPont Company, Johnston, 50131, Iowa, USA

    Robert B. Meeley

Authors
  1. Andrea Gallavotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junko Kyozuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert B. Meeley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matthew K. Ritter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John F. Doebley
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Enrico Pè
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Robert J. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert J. Schmidt.

Ethics declarations

Competing interests

The authors declare they have no competing financial interests.

Supplementary information

Supplementary Data

We provide further details about the CAPS analysis on the 86 inbred lines. (DOC 20 kb)

Supplementary Methods

We describe in detail the isolation of new ba1 alleles, the amplification of regions a, b, c and the CAPS marker analysis on the 86 inbred lines analyzed for haplotype I and II. (DOC 22 kb)

Supplementary Table 1

Supplementary Table 1 is part of the Methods section and lists all the maize and teosinte individuals sequenced at the barren stalk1 gene with the corresponding GenBank Accessions Numbers. (DOC 44 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gallavotti, A., Zhao, Q., Kyozuka, J. et al. The role of barren stalk1 in the architecture of maize. Nature 432, 630–635 (2004). https://doi.org/10.1038/nature03148

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03148

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

Advanced 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