Parallel domestication of the Shattering1 genes in cereals

Abstract

A key step in domestication of cereals was loss of seed shattering. Jianming Yu and colleagues show that seed shattering is controlled by alleles at Sh1 in sorghum. The authors also identify an insertion in the ortholog of Sh1 in a shattering-resistant mutant in rice and orthologs of Sh1 located in two narrow quantitative trait locus (QTL) intervals that regulate shattering in maize. The data suggest parallel selection on Sh1 in the domestication of cereals. 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.