Identification of a functional transposon insertion in the maize domestication gene tb1

Journal name:
Nature Genetics
Volume:
43,
Pages:
1160–1163
Year published:
DOI:
doi:10.1038/ng.942
Received
Accepted
Published online

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.

At a glance

Figures

  1. Teosinte and maize plants.
    Figure 1: Teosinte and maize plants.

    (a) Highly branched teosinte plant. (b) Teosinte lateral branch with terminal tassel. (c) Unbranched maize plant. (d) Maize ear shoot (that is, lateral branch).

  2. The phenotypic additive effects for seven intervals across the tb1 genomic region.
    Figure 2: The phenotypic additive effects for seven intervals across the tb1 genomic region.

    The horizontal axis represents the tb1 genomic region to scale. Base-pair positions are relative to AGPv2 position 265,745,977 of the maize reference genome sequence. The tb1 ORF and the nearest upstream predicted gene (pg3) are shown. The previously defined control region (CR)14 is shown in red and is divided into its proximal and distal components. Vertical columns represent the additive effects shown with standard error bars for each of the three traits in each of the seven intervals that were tested for an effect on phenotype. Black columns are statistically significant (P (Bonferroni) < 0.05); white bars are not statistically significant (P (Bonferroni) > 0.05).

  3. Sequence diversity in maize and teosinte across the control region.
    Figure 3: Sequence diversity in maize and teosinte across the control region.

    (a) Nucleotide diversity across the tb1 upstream control region. Base-pair positions are relative to AGPv2 position 265,745,977 of the maize reference genome sequence. P values correspond to HKA neutrality tests for regions A–D, as defined by the dotted lines. Green shading signifies evidence of neutrality, and pink shading signifies regions of non-neutral evolution. Nucleotide diversity (π) for maize (yellow line) and teosinte (green line) were calculated using a 500-bp sliding window with a 25-bp step. The distal and proximal components of the control region with four fixed sequence differences between the most common maize haplotype and teosinte haplotype are shown below. (b) A minimum spanning tree for the control region with 16 diverse maize and 17 diverse teosinte sequences. Size of the circles for each haplotype group (yellow, maize; green, teosinte) is proportional to the number of individuals within that haplotype.

  4. Constructs and corresponding normalized luciferase expression levels.
    Figure 4: Constructs and corresponding normalized luciferase expression levels.

    Transient assays were performed in maize leaf protoplast. Each construct is drawn to scale. The construct backbone consists of the minimal promoter from the cauliflower mosaic virus (mpCaMV, gray box), luciferase ORF (luc, white box) and the nopaline synthase terminator (black box). Portions of the proximal and distal components of the control region (hatched boxes) from maize and teosinte were cloned into restriction sites upstream of the minimal promoter. “Δ” denotes the excision of either the Tourist or Hopscotch element from the maize construct. Horizontal green bars show the normalized mean with s.e.m. for each construct.

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Author information

Affiliations

  1. Department of Genetics, University of Wisconsin–Madison, Madison, Wisconsin, USA.

    • Anthony Studer,
    • Qiong Zhao &
    • John Doebley
  2. Department of Plant Sciences, University of California, Davis, California, USA.

    • Jeffrey Ross-Ibarra
  3. The Genome Center, University of California, Davis, California, USA.

    • Jeffrey Ross-Ibarra

Contributions

A.S. and J.D. designed the experiments and wrote the paper. A.S., J.R.-I. and Q.Z. performed population genetic analyses. Genetic mapping, transient assays, sequencing and informatics were done by A.S.

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The authors declare no competing financial interests.

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