Genetic diversity created by transposable elements is an important source of functional variation upon which selection acts during evolution1,2,3,4,5,6. Transposable elements are associated with adaptation to temperate climates in Drosophila7, a SINE element is associated with the domestication of small dog breeds from the gray wolf8 and there is evidence that transposable elements were targets of selection during human evolution9. Although the list of examples of transposable elements associated with host gene function continues to grow, proof that transposable elements are causative and not just correlated with functional variation is limited. Here we show that a transposable element (Hopscotch) inserted in a regulatory region of the maize domestication gene, teosinte branched1 (tb1), acts as an enhancer of gene expression and partially explains the increased apical dominance in maize compared to its progenitor, teosinte. Molecular dating indicates that the Hopscotch insertion predates maize domestication by at least 10,000 years, indicating that selection acted on standing variation rather than new mutation.
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Naito, K. et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461, 1130–1134 (2009).
Xiao, H., Jiang, N., Schaffner, E., Stockinger, E.J. & van der Knaap, E. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319, 1527–1530 (2008).
White, S.E., Habera, L.F. & Wessler, S.R. Retrotransposons in the flanking regions of normal plant genes: A role for copia-like elements in the evolution of gene structure and expression. Proc. Natl. Acad. Sci. USA 91, 11792–11796 (1994).
Bejerano, G. et al. A distal enhancer and an ultraconserved exon are derived from a novel retrotransposon. Nature 441, 87–90 (2006).
Mackay, T.F.C., Lyman, R.F. & Jackson, M.S. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics 130, 315–332 (1992).
Torkamanzehi, A., Moran, C. & Nicholas, F.W. P element transposition contributes substantial new variation for a quantitative trait in Drosophila melanogaster. Genetics 131, 73–78 (1992).
González, J., Karasov, T.L., Messer, P.W. & Petrov, D.A. Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet. 6, e1000905 (2010).
Gray, M.M., Sutter, N.B., Ostrander, E.A. & Wayne, R.K. The IGF1 small dog haplotype is derived from Middle Eastern grey wolves. BMC Biol. 8, 16 (2010).
Britten, R.J. Transposable element insertions have strongly affected human evolution. Proc. Natl. Acad. Sci. USA 107, 19945–19948 (2010).
Doebley, J. The genetics of maize evolution. Annu. Rev. Genet. 38, 37–59 (2004).
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).
Cubas, P., Lauter, N., Doebley, J. & Coen, E. The TCP domain: a motif found in proteins regulating plant growth and development. Plant J. 18, 215–222 (1999).
Doebley, J., Stec, A. & Hubbard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997).
Clark, R.M., Nussbaum Wagler, T., Quijada, P. & Doebley, J. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat. Genet. 38, 594–597 (2006).
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).
Hudson, R.R., Kreitman, M. & Aguade, M. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159 (1987).
Zhao, Q. Molecular Population Genetics of Maize Regulatory Genes During Maize Evolution. PhD Thesis, University of Wisconsin–Madison (2006).
Fukunaga, K. et al. Genetic diversity and population structure of teosinte. Genetics 169, 2241–2254 (2005).
Thomson, R. et al. Recent common ancestry of human Y chromosomes: Evidence from DNA sequence data. Proc. Natl. Acad. Sci. USA 97, 7360–7365 (2000).
Hudson, R.R. The variance of coalescent time estimates from DNA sequences. J. Mol. Evol. 64, 702–705 (2007).
Clark, R.M., Tavare, S. & Doebley, J. Estimating a nucleotide substitution rate for maize from polymorphism at a major domestication locus. Mol. Biol. Evol. 22, 2304–2312 (2005).
Pi, W. et al. Long-range function of an intergenic retrotransposon. Proc. Natl. Acad. Sci. USA 107, 12992–12997 (2010).
Chung, H. et al. Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 175, 1071–1077 (2007).
Schmidt, J.M. et al. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet. 6, e1000998 (2010).
McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984).
Tenaillon, M.I. et al. Patterns of DNA sequence polymorphism along chromsome 1 of maize (Zea mays ssp. mays L). Proc. Natl. Acad. Sci. USA 98, 9161–9166 (2001).
Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).
Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X., Rozas, R. & Dna, S.P. DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497 (2003).
Zhao, Q., Weber, A.L., McMullen, M.D., Guill, K. & Doebley, J. MADS-box genes of maize: frequent targets of selection during domestication. Genet. Res. (Camb.) 93, 65–75 (2011).
Excoffier, L. & Lischer, H.E.L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).
Teacher, A.G.F. & Griffiths, D.J. HapStar: automated haplotype network layout and visualization. Mol. Ecol. Resour. 11, 151–153 (2011).
Thornton, K. Libsequence: a C. class library for evolutionary genetic analysis. Bioinformatics 19, 2325–2327 (2003).
Benfey, P.N. & Chua, N. The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250, 959–966 (1990).
We thank members of the Doebley laboratory for technical assistance, especially H. Wang. We also thank A.J. Eckert, K. Thornton, G. Coop and R.A. Cartwright for helpful discussion and J. Holland for statistical advice. This work is supported by US Department of Agriculture Hatch grant MSN101593 and US National Science Foundation grant DBI0820619.
The authors declare no competing financial interests.
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Studer, A., Zhao, Q., Ross-Ibarra, J. et al. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43, 1160–1163 (2011). https://doi.org/10.1038/ng.942
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