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A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture

Nature Genetics volume 38, pages 594–597 (2006)Cite this article

Abstract

Although quantitative trait locus (QTL) mapping has been successful in describing the genetic architecture of complex traits1,2,3,4, the molecular basis of quantitative variation is less well understood, especially in plants such as maize that have large genome sizes. Regulatory changes at the teosinte branched1 (tb1) gene have been proposed to underlie QTLs of large effect for morphological differences that distinguish maize (Zea mays ssp. mays) from its wild ancestors, the teosintes (Z. mays ssp. parviglumis and mexicana)1,5,6,7. We used a fine mapping approach to show that intergenic sequences ∼58–69 kb 5′ to the tb1 cDNA confer pleiotropic effects on Z. mays morphology. Moreover, using an allele-specific expression assay, we found that sequences >41 kb upstream of tb1 act in cis to alter tb1 transcription. Our findings show that the large stretches of noncoding DNA that comprise the majority of many plant genomes can be a source of variation affecting gene expression and quantitative phenotypes.

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Figure 1: Introgression lines and effects on traits.
Figure 2: Allele-specific tb1 expression assay.

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Mackay, T.F. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35, 303–339 (2001).

    Article  CAS  PubMed  Google Scholar 

  3. Mackay, T.F. The genetic architecture of quantitative traits: lessons from Drosophila. Curr. Opin. Genet. Dev. 14, 253–257 (2004).

    Article  CAS  PubMed  Google Scholar 

  4. Tanksley, S.D. The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16 (Suppl.), S181–S189 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Alonso-Blanco, C., Mendez-Vigo, B. & Koornneef, M. From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. Int. J. Dev. Biol. 49, 717–732 (2005).

    Article  CAS  PubMed  Google Scholar 

  9. Salvi, S. & Tuberosa, R. To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci. 10, 297–304 (2005).

    Article  CAS  PubMed  Google Scholar 

  10. Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).

    Article  CAS  PubMed  Google Scholar 

  11. Koornneef, M., Alonso-Blanco, C. & Vreugdenhil, D. Naturally occurring genetic variation in Arabidopsis thaliana. Annu. Rev. Plant Biol. 55, 141–172 (2004).

    Article  CAS  PubMed  Google Scholar 

  12. SanMiguel, P. et al. Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765–768 (1996).

    Article  CAS  PubMed  Google Scholar 

  13. Meagher, T.R. & Vassiliadis, C. Phenotypic impacts of repetitive DNA in flowering plants. New Phytol. 168, 71–80 (2005).

    Article  CAS  PubMed  Google Scholar 

  14. Doebley, J. & Stec, A. Genetic analysis of the morphological differences between maize and teosinte. Genetics 129, 285–295 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Doebley, J., Stec, A., Wendel, J. & Edwards, M. Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. Proc. Natl. Acad. Sci. USA 87, 9888–9892 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. 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  CAS  PubMed  Google Scholar 

  18. Thornsberry, J.M. et al. Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 28, 286–289 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Sheehan, M.J., Farmer, P.R. & Brutnell, T.P. Structure and expression of maize phytochrome family homeologs. Genetics 167, 1395–1405 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Simons, K.J. et al. Molecular characterization of the major wheat domestication gene. Q. Genetics 172, 547–555 (2006).

    Article  CAS  PubMed  Google Scholar 

  21. Wang, H. et al. The origin of the naked grains of maize. Nature 436, 714–719 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Stam, M. et al. The regulatory regions required for B′ paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 162, 917–930 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Wendel, J.F., Cronn, R.C., Johnston, J.S. & Price, H.J. Feast and famine in plant genomes. Genetica 115, 37–47 (2002).

    Article  CAS  PubMed  Google Scholar 

  24. Bennetzen, J.L., Ma, J. & Devos, K.M. Mechanisms of recent genome size variation in flowering plants. Ann. Bot. (Lond.) 95, 127–132 (2005).

    Article  CAS  Google Scholar 

  25. Rostoks, N. et al. Genomic sequencing reveals gene content, genomic organization, and recombination relationships in barley. Funct. Integr. Genomics 2, 51–59 (2002).

    Article  CAS  PubMed  Google Scholar 

  26. Wicker, T. et al. Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J. 26, 307–316 (2001).

    Article  CAS  PubMed  Google Scholar 

  27. Wicker, T. et al. A detailed look at 7 million years of genome evolution in a 439 kb contiguous sequence at the barley Hv-eIF4E locus: recombination, rearrangements and repeats. Plant J. 41, 184–194 (2005).

    Article  CAS  PubMed  Google Scholar 

  28. Ihaka, R. & Gentleman, R.R. A language for data analysis and graphics. J. Comput. Graph. Stat. 5, 299–314 (1996).

    Google Scholar 

  29. 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 

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Acknowledgements

We thank L. Rentmeester, B. Oldham, A.-C. Thuillet, K. Bomblies, Y. Vigouroux and other laboratory members for help with fieldwork and for suggestions that improved the experimental design, and K. Bomblies and S. Balasubramanian for comments on the manuscript. This work was supported by US National Institutes of Health grant GM-58816 (to J.D.) and National Institutes of Health award F32 GM-65008 (to R.M.C.).

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  1. Richard M Clark

    Present address: Max Planck Institute for Developmental Biology, D-72076, Tübingen, Germany

Authors and Affiliations

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

    Richard M Clark, Tina Nussbaum Wagler, Pablo Quijada & John Doebley

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  1. Richard M Clark
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  2. Tina Nussbaum Wagler
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  3. Pablo Quijada
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Correspondence to John Doebley.

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Supplementary information

Supplementary Fig. 1

Recombination breakpoints in the tb1 to PG3 region. (PDF 399 kb)

Supplementary Fig. 2

Trait means, sample sizes, and direction of effects. (PDF 936 kb)

Supplementary Table 1

Genealogies of Panindicuaro chromosome segments (PDF 39 kb)

Supplementary Table 2

P-values of tests for phenotypic differences in the means among genotypic classes within families segregating for Panindicuaro chromosome segments (PDF 43 kb)

Supplementary Table 3

Peak area measurements and adjusted expression ratios for allele-specific expression assay (PDF 64 kb)

Supplementary Table 4

Primers used for allele-specific PCR, genotyping, and localization of recombination breakpoints (PDF 48 kb)

Supplementary Table 5

Primers, polymorphisms, and loci used for genotyping Panindicuaro introgressions (PDF 38 kb)

Supplementary Methods (PDF 95 kb)

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Clark, R., Wagler, T., Quijada, P. et al. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 38, 594–597 (2006). https://doi.org/10.1038/ng1784

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