Parallel domestication of the Shattering1 genes in cereals

Journal name:
Nature Genetics
Volume:
44,
Pages:
720–724
Year published:
DOI:
doi:10.1038/ng.2281
Received
Accepted
Published online

A key step during crop domestication is the loss of seed shattering. Here, we show that seed shattering in sorghum is controlled by a single gene, Shattering1 (Sh1), which encodes a YABBY transcription factor. Domesticated sorghums harbor three different mutations at the Sh1 locus. Variants at regulatory sites in the promoter and intronic regions lead to a low level of expression, a 2.2-kb deletion causes a truncated transcript that lacks exons 2 and 3, and a GT-to-GG splice-site variant in the intron 4 results in removal of the exon 4. The distributions of these non-shattering haplotypes among sorghum landraces suggest three independent origins. The function of the rice ortholog (OsSh1) was subsequently validated with a shattering-resistant mutant, and two maize orthologs (ZmSh1-1 and ZmSh1-5.1+ZmSh1-5.2) were verified with a large mapping population. Our results indicate that Sh1 genes for seed shattering were under parallel selection during sorghum, rice and maize domestication.

At a glance

Figures

  1. Seed shattering phenotype in sorghum.
    Figure 1: Seed shattering phenotype in sorghum.

    (a,b) Seeds were scattered everywhere from the top of the wild sorghum SV plant (a), whereas seeds were firmly retained on the head of the domesticated sorghum Tx430 plant (b, shown only from a panicle branch) at maturity after vigorous shaking. (c,d) Larger views of spikelets in a and b are shown for SV (c) and Tx430 (d) plants after shaking. (e,f) Abscission layers (of curved shape) were present at the junction between the hull and pedicel on SV plants (e), whereas no abscission layer was observed on Tx430 plants (f). AL, abscission layer; scale bars, 50 μm.

  2. Map-based cloning of Sh1 in sorghum.
    Figure 2: Map-based cloning of Sh1 in sorghum.

    (a) DNA chip screening across 94 F2 plants mapped the Sh1 gene onto sorghum chromosome 1. Significant SNPs are marked as red dots; the red dashed line represents the 5% significance threshold with Bonferroni correction for 90 tests. (b) Genetic mapping of Sh1 with 286 F2 plants. Genetic distance between flanking pairwise molecular markers is shown. (c) High-resolution mapping of Sh1 with 15,000 F2 plants. The genotypes of two F2 recombinant plants are shown; the F3 progenies of both F2 recombinant plants are segregated by phenotype. Gray bar, heterozygous region of Tx430; white bar, homozygous region of Tx430; R, recombinant plant. (d) The Propinquum BAC clone 25K18 was identified by the two flanking markers of Sh1, and two genes were predicted within the candidate region between these markers. Gray arrow, a hypothetical gene specifically expressed in pollen; red arrow, YABBY-like gene.

  3. Variant alleles and association mapping at Sh1.
    Figure 3: Variant alleles and association mapping at Sh1.

    (a) Gene structure and haplotype analysis of Sh1. —SV-like, SC265-like, Tx430-like and Tx623-like haplotypes were identified on the basis of ten variants of the Sh1 gene. The positions of these ten variants are shown using the Sh1 gene sequence of SV as reference, with the start codon designated as position 0. The SV-like haplotype is highlighted in yellow. Splicing mutation from GT to GG at 6,608 in the SC265-like haplotype (blue), four specific variants at −1,194, −1,185, 4,881 and 5,076 in the Tx430-like haplotype (red) and a 2.2-kb deletion from 3,985 to 6,251 in the Tx623-like haplotype (green) are indicated. Arrow bar, promoter region; thick bar, downstream region after the stop codon; blank box, exon; thin line, intron; ATG, start codon; TAA, stop codon; adjacent unfilled boxes on a dashed line, 2.2-kb deletion; SH, shattering; NS, non-shattering. (b) Association testing at sites of ten variants and two fine-mapping markers P6 and SNP1. Black dots, ten variants of Sh1; blue dots, P6 (left) and SNP1 (right); red dot, supposed synthetic association site; red dashed line, 5% significance threshold. (c) Amino-acid sequence alignment for different haplotypes. Two domains, zinc finger (blue) and YABBY (red), are indicated. (d) There was strong transcription of Sh1 in Propinquum and SV, whereas there was weak transcription in Tx430 and truncated transcripts for Tx623 and SC265.

  4. Genomic regions of Sh1 in cereals.
    Figure 4: Genomic regions of Sh1 in cereals.

    (a) Genomic regions corresponding to Sh1 were conserved in sorghum (Sorghum bicolor), maize (Zea mays), rice (Oryza sativa) and foxtail millet (Setaria italica). The genomic collinearity map was plotted on the basis of the BLASTP result of pairwise genome analysis from CoGe; dot plot alignment indicates the collinearity of genomic regions. (b) Sh1 gene structure comparison. Sh1 gene structure is conserved, except for one extremely large intron (19.3 kb) that was present only in the Sh1 ortholog on maize chromosome 1 (ZmSh1-1) and a gene fusion that occurred in one of two Sh1 orthologs on maize chromosome 5 (ZmSh1-5.1).

  5. Maize Sh1 orthologs are located at seed shattering QTLs.
    Figure 5: Maize Sh1 orthologs are located at seed shattering QTLs.

    (a) Two QTLs explaining 3.5% and 23.1% of the phenotypic variation of shattering were detected on maize chromosomes 1 and 5, respectively, using a large mapping population. Physical positions of the QTL confidence intervals and the maize Sh1 orthologs are indicated below the chromosome axes. LOD, logarithm of odds. (b) Assembly of structural variation for the Sh1 orthologs on maize chromosomes 1 and 5. ZmSh1-5.1 consists of a gene fusion that retains only the first three exons of the YABBY-like gene and two exons from an unknown gene. The replacement of exons 4–6 in ZmSh1-5.1 causes loss of the YABBY domain. A large (23-kb) insertion is present between ZmSh1-5.1 and ZmSh1-5.2. Solid/dashed red triangle, presence/absence of large insertion; solid/dashed red arrow, presence/absence of 83-bp insertion in exon 3 of ZmSh1-1.

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Author information

Affiliations

  1. Department of Agronomy, Kansas State University, Manhattan, Kansas, USA.

    • Zhongwei Lin,
    • Xianran Li,
    • Guihua Bai,
    • Tesfaye T Tesso &
    • Jianming Yu
  2. Department of Genetics, University of Wisconsin, Madison, Wisconsin, USA.

    • Laura M Shannon &
    • John Doebley
  3. Center for Plant Genomics, Iowa State University, Ames, Iowa, USA.

    • Cheng-Ting Yeh &
    • Patrick S Schnable
  4. Department of Agronomy, Iowa State University, Ames, Iowa, USA.

    • Cheng-Ting Yeh &
    • Patrick S Schnable
  5. US Department of Agriculture–Agricultural Research Service (USDA-ARS), Griffin, Georgia, USA.

    • Ming L Wang
  6. USDA-ARS, Manhattan, Kansas, USA.

    • Guihua Bai
  7. Department of Plant Pathology, Kansas State University, Manhattan, Kansas, USA.

    • Zhao Peng,
    • Jiarui Li,
    • Harold N Trick &
    • Frank White
  8. Center for Plant Science Innovation, University of Nebraska, Lincoln, Nebraska, USA.

    • Thomas E Clemente
  9. Department of Agronomy, Purdue University, West Lafayette, Indiana, USA.

    • Mitchell R Tuinstra

Contributions

J.Y., F.W., T.T.T. and M.R.T. designed research. Z.L., X.L., L.M.S., C.-T.Y., Z.P. and J.L. carried out the research. M.L.W., G.B., H.N.T., T.E.C., J.D. and P.S.S. contributed new reagents. Z.L., X.L., L.M.S. and C.-T.Y. analyzed data. Z.L. and J.Y. wrote the manuscript with input from all other coauthors.

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The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Text and Figures (922K)

    Supplementary Figures 1–4, Supplementary Tables 1–7 and Supplementary Note

Excel files

  1. Supplementary Table 8 (741K)

    Predicted genes in the syntenic block in sorghum, rice, maize, and foxtail millet

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