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Parallel domestication of the Shattering1 genes in cereals

Abstract

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.

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Figure 1: Seed shattering phenotype in sorghum.
Figure 2: Map-based cloning of Sh1 in sorghum.
Figure 3: Variant alleles and association mapping at Sh1.
Figure 4: Genomic regions of Sh1 in cereals.
Figure 5: Maize Sh1 orthologs are located at seed shattering QTLs.

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Acknowledgements

This work was supported by an Agriculture and Food Research Initiative Competitive Grant (2011-03587 to J.Y. and T.T.T.) from the US Department of Agriculture (USDA) National Institute of Food and Agriculture, the Plant Genome Research Program of the National Science Foundation (DBI-0820610 to J.Y., DBI-0820619 to J.D. and DBI-1027527 to P.S.S.), the Plant Feedstock Genomics Program of the US Department of Energy (DE-SC0002259 to J.Y.), the USDA-ARS (M.L.W. and G.B.), the Targeted Excellence Program of Kansas State University and the Kansas State University Center for Sorghum Improvement.

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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.

Corresponding author

Correspondence to Jianming Yu.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4, Supplementary Tables 1–7 and Supplementary Note (PDF 899 kb)

Supplementary Table 8

Predicted genes in the syntenic block in sorghum, rice, maize, and foxtail millet (XLS 722 kb)

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Lin, Z., Li, X., Shannon, L. et al. Parallel domestication of the Shattering1 genes in cereals. Nat Genet 44, 720–724 (2012). https://doi.org/10.1038/ng.2281

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