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Summary: Plant breeding is constrained by trade‐offs among different agronomic traits by the pleiotropic nature of many genes. Genes that contribute to two or more favourable traits with no penalty on yield are rarely reported, especially in wheat. Here, we describe the editing of a wheat auxin response factor TaARF12 by using CRISPR/Cas9 that rendered shorter plant height with larger spikes. Changes in plant architecture enhanced grain number per spike up to 14.7% with significantly higher thousand‐grain weight and up to 11.1% of yield increase under field trials. Weighted Gene Co‐Expression Network Analysis (WGCNA) of spatial–temporal transcriptome profiles revealed two hub genes: RhtL1, a DELLA domain‐free Rht‐1 paralog, which was up‐regulated in peduncle, and TaNGR5, an organ size regulator that was up‐regulated in rachis, in taarf12 plants. The up‐regulation of RhtL1 in peduncle suggested the repression of GA signalling, whereas up‐regulation of TaNGR5 in spike may promote GA response, a working model supported by differential expression patterns of GA biogenesis genes in the two tissues. Thus, TaARF12 complemented plant height reduction with larger spikes that gave higher grain yield. Manipulation of TaARF12 may represent a new strategy in trait pyramiding for yield improvement in wheat. [ABSTRACT FROM AUTHOR]

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. Exome sequencing of 287 wheat accessions representing a collection from the past 100 years in China and genome-wide association study identified epistatically interacting pleiotropic genomic loci for yield potential. Selection signatures identified suggest that the gibberellin pathway is fine-tuned in post-Green Revolution breeding efforts. This rich genomic diversity resource will be useful for the wheat research community. [ABSTRACT FROM AUTHOR]