Limited haplotype diversity underlies polygenic trait architecture across 70 years of wheat breeding

Background Breeding has helped improve bread wheat yield significantly over the last century. Understanding the potential for future crop improvement depends on relating segregating genetic variation to agronomic traits. Results We bred NIAB Diverse MAGIC population, comprising over 500 recombinant inbred lines, descended from sixteen bread wheat varieties released between 1935-2004. We sequenced the founders’ exomes and promotors by capture. Despite being highly representative of North-West European wheat and capturing 73% of global polymorphism, we found 89% of genes contained no more than three haplotypes. We sequenced each line with 0.3x coverage whole-genome sequencing, and imputed 1.1M high-quality SNPs that were over 99% concordant with array genotypes. Imputation accuracy remained high at coverage as low as 0.076x, with or without the use of founder genomes as reference panels. We created a genotype-phenotype map for 47 traits over two years. We found 136 genome-wide significant associations, concentrated at 42 genetic loci with large and often pleiotropic effects. Outside of these loci most traits are polygenic, as revealed by multi-locus shrinkage modelling. Conclusions Historically, wheat breeding has reshuffled a limited palette of haplotypes; continued improvement will require selection at dozens of loci of diminishing effect, as most of the major loci we mapped are known. Breeding to optimise one trait generates correlated trait changes, exemplified by the negative trade-off between yield and protein content, unless selection and recombination can break critical unfavourable trait-trait associations. Finally, low coverage whole genome sequencing of bread wheat populations is an economical and accurate genotyping strategy.