Positive selection on hotspot and reinforcing regulatory alleles contributed to hexaploid bread wheat improvement.

Background Genetic variation of regulatory alleles plays a key role in evolution and breeding. In polyploids, regulatory differences may preferentially affect genes on homoeologous chromosomes or sub-genomes. Selection in plant breeding may act upon total transcript dosage across homoeologous genes and on alleles that have strong effects on the transcriptome. Results To investigate these questions, we identified regulatory polymorphisms between an old and a recent hexaploid bread wheat cultivar (Triticum aestivum, 2n=6x=42, AABBDD). The recent cultivar was the product of decades of selection for grain yield and quality. Regulatory allele polymorphisms preferentially affected genes on homoeologous chromosomes but rarely affected genes on specific sub-genomes. The chromosomal distributions of regulatory alleles indicated that past selection had acted upon them, and the effect of selection differed between alleles targeting environmental response genes and genes involved in other processes. Modern cultivar alleles that affected many genes' transcripts corresponded to known selection targets and improved field crop performance. Modern cultivar alleles also had significant effects on homoeologous genes, and these alleles also improved crop performance. Conclusions Polyploid breeding across many species has been and will continue to be the key factor in plant improvement. By enhancing the favorability of strong regulatory alleles and by expanding the range of gene transcript abundances, genome duplications enable breeding progress.