Wheat breeding history reveals synergistic selection of pleiotropic genomic sites for plant architecture and grain yield

Diversity surveys of crop germplasm are important for gaining insights into the genomic basis for plant architecture and grain yield improvement, which is still poorly understood in wheat. In this study, we exome sequenced 287 wheat accessions that were collected in the past 100 years. Population genetics analysis identified that 6.7% of the wheat genome falls within the selective sweeps between landraces and cultivars, which harbors the genes known for yield improvement. These regions were asymmetrically distributed on the A and B subgenomes with regulatory genes being favorably selected. Genome-wide association study (GWAS) identified genomic loci associated with traits for yield potential, and two underlying genes, TaARF12 encoding an auxin response factor and TaDEP1 encoding the G-protein γ-subunit, were located and characterized to pleiotropically regulate both plant height and grain weight. Elite single-nucleotide haplotypes with increased allele frequency in cultivars relative to the landraces were identified and found to have accumulated over the course of breeding. Interestingly, we found that TaARF12 and TaDEP1 function in epistasis with the classical plant height Rht-1 locus, leading to propose a “Green Revolution”-based working model for historical wheat breeding. Collectively, our study identifies selection signatures that fine-tune the gibberellin pathway during modern wheat breeding and provides a wealth of genomic diversity resources for the wheat research community.