Gene duplication drove the loss of awn in sorghum

Loss of the awn in some cereals, including sorghum, is a key transition during cereal domestication or improvement that has facilitated grain harvest and storage. The genetic basis of awn loss in sorghum during domestication or improvement remains unknown. Here, we identified the awn1 gene encoding a transcription factor with the ALOG domain that is responsible for awn loss during sorghum domestication or improvement. awn1 arose from a gene duplication on chromosome 10 that translocated to chromosome 3, recruiting a new promoter from the neighboring intergenic region filled with “noncoding DNA” and recreating the first exon and intron. awn1 acquired high expression after duplication and represses the elongation of awns in domesticated sorghum. Comparative mapping revealed high collinearity at the awn1 paralog locus on chromosome 10 across cereals, and awn growth and development were successfully reactivated on the rice spikelet by inactivating the rice awn1 ortholog. RNA-seq and DAP-seq revealed that as a transcriptional repressor, AWN1 bound directly to a motif in the regulatory regions of three MADS genes related to flower development and two genes, DL and LKS2, involved in awn development. AWN1 downregulates the expression of these genes, thereby repressing awn elongation. The preexistence of regulatory elements in the neighboring intergenic region of awn1 before domestication implicates that noncoding DNA may serve as a treasure trove for evolution during sorghum adaptation to a changing world. Taken together, our results suggest that gene duplication can rapidly drive the evolution of gene regulatory networks in plants. Loss of the awn facilitates seed harvest and storage in sorghum. The awn1 gene arose from a duplication on chromosome 10 that translocated to chromosome 3; it became active after recruiting a new promoter from the neighboring region and repressed awn outgrowth, thereby driving awn loss in sorghum.