Analysis of historical selection in winter wheat

KEY MESSAGE: Modeling of the distribution of allele frequency over year of variety release identifies major loci involved in historical breeding of winter wheat. ABSTRACT: Winter wheat is a major crop with a rich selection history in the modern era of crop breeding. Genetic gains across economically important traits like yield have been well characterized and are the major force driving its production. Winter wheat is also an excellent model for analyzing historical genetic selection. As a proof of concept, we analyze two major collections of winter wheat varieties that were bred in Western Europe from 1916 to 2010, namely the Triticeae Genome (TG) and WAGTAIL panels, which include 333 and 403 varieties, respectively. We develop and apply a selection mapping approach, Regression of Alleles on Years (RALLY), in these panels, as well as in simulated populations. RALLY maps loci under sustained historical selection by using a simple logistic model to regress allele counts on years of variety release. To control for drift-induced allele frequency change, we develop a hybrid approach of genomic control and delta control. Within the TG panel, we identify 22 significant RALLY quantitative selection loci (QSLs) and estimate the local heritabilities for 12 traits across these QSLs. By correlating predicted marker effects with RALLY regression estimates, we show that alleles whose frequencies have increased over time are heavily biased toward conferring positive yield effect, but negative effects in flowering time, lodging, plant height and grain protein content. Altogether, our results (1) demonstrate the use of RALLY to identify selected genomic regions while controlling for drift, and (2) reveal key patterns in the historical selection in winter wheat and guide its future breeding. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00122-022-04163-3

Analysis of historical selection in winter wheat

KEY MESSAGE: Modeling of the distribution of allele frequency over year of variety release identifies major loci involved in historical breeding of winter wheat. Winter wheat is a major crop with a rich selection history in the modern era of crop breeding. Genetic gains across economically important traits like yield have been well characterized and are the major force driving its production. Winter wheat is also an excellent model for analyzing historical genetic selection. As a proof of concept, we analyze two major collections of winter wheat varieties that were bred in Western Europe from 1916 to 2010, namely the Triticeae Genome (TG) and WAGTAIL panels, which include 333 and 403 varieties, respectively. We develop and apply a selection mapping approach, Regression of Alleles on Years (RALLY), in these panels, as well as in simulated populations. RALLY maps loci under sustained historical selection by using a simple logistic model to regress allele counts on years of variety release. To control for drift-induced allele frequency change, we develop a hybrid approach of genomic control and delta control. Within the TG panel, we identify 22 significant RALLY quantitative selection loci (QSLs) and estimate the local heritabilities for 12 traits across these QSLs. By correlating predicted marker effects with RALLY regression estimates, we show that alleles whose frequencies have increased over time are heavily biased toward conferring positive yield effect, but negative effects in flowering time, lodging, plant height and grain protein content. Altogether, our results (1) demonstrate the use of RALLY to identify selected genomic regions while controlling for drift, and (2) reveal key patterns in the historical selection in winter wheat and guide its future breeding

Maximizing the potential of multi-parental crop populations.

Most agriculturally significant crop traits are quantitatively inherited which limits the ease and efficiency of trait dissection. Multi-parent populations overcome the limitations of traditional trait mapping and offer new potential to accurately define the genetic basis of complex crop traits. The increasing popularity and use of nested association mapping (NAM) and multi-parent advanced generation intercross (MAGIC) populations raises questions about the optimal design and allocation of resources in their creation. In this paper we review strategies for the creation of multi-parent populations and describe two complementary in silico studies addressing the design and construction of NAM and MAGIC populations. The first simulates the selection of diverse founder parents and the second the influence of multi-parent crossing schemes (and number of founders) on haplotype creation and diversity. We present and apply two open software resources to simulate alternate strategies for the development of multi-parent populations

Reference Genome Anchoring of High-Density Markers for Association Mapping and Genomic Prediction in European Winter Wheat.

In this study, we anchored genotyping-by-sequencing data to the International Wheat Genome Sequencing Consortium Reference Sequence v1.0 assembly to generate over 40,000 high quality single nucleotide polymorphism markers on a panel of 376 elite European winter wheat varieties released between 1946 and 2007. We compared association mapping and genomic prediction accuracy for a range of productivity traits with previous results based on lower density dominant DArT markers. The results demonstrate that the availability of RefSeq v1.0 supports higher precision trait mapping and provides the density of markers required to obtain accurate predictions of traits controlled by multiple small effect loci, including grain yield

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

Background Selection has dramatically shaped genetic and phenotypic variation in bread wheat. We can assess the genomic basis of historical phenotypic changes, and the potential for future improvement, using experimental populations that attempt to undo selection through the randomizing effects of recombination. Results We bred the NIAB Diverse MAGIC multi-parent population comprising over 500 recombinant inbred lines, descended from sixteen historical UK bread wheat varieties released between 1935 and 2004. We sequence the founders’ genes and promoters by capture, and the MAGIC population by low-coverage whole-genome sequencing. We impute 1.1 M high-quality SNPs that are over 99% concordant with array genotypes. Imputation accuracy only marginally improves when including the founders’ genomes as a haplotype reference panel. Despite capturing 73% of global wheat genetic polymorphism, 83% of genes cluster into no more than three haplotypes. We phenotype 47 agronomic traits over 2 years and map 136 genome-wide significant associations, concentrated at 42 genetic loci with large and often pleiotropic effects. Around half of these overlap known quantitative trait loci. Most traits exhibit extensive polygenicity, as revealed by multi-locus shrinkage modelling. Conclusions Our results are consistent with a gene pool of low haplotypic diversity, containing few novel loci of large effect. Most past, and projected future, phenotypic changes arising from existing variation involve fine-scale shuffling of a few haplotypes to recombine dozens of polygenic alleles of small effect. Moreover, extensive pleiotropy means selection on one trait will have unintended consequences, exemplified by the negative trade-off between yield and protein content, unless selection and recombination can break unfavorable trait-trait associations

Testing new genetic and genomic approaches for trait mapping and prediction in wheat (Triticum aestivum) and rice (Oryza spp)

Advances in molecular marker technologies have led to the development of high throughput genotyping techniques such as Genotyping by Sequencing (GBS), driving the application of genomics in crop research and breeding. They have also supported the use of novel mapping approaches, including Multi-parent Advanced Generation Inter-Cross (MAGIC) populations which have increased precision in identifying markers to inform plant breeding practices. In the first part of this thesis, a high density physical map derived from GBS was used to identify QTLs controlling key agronomic traits of wheat in a genome-wide association study (GWAS) and to demonstrate the practicability of genomic selection for predicting the trait values. The results from GBS were compared to a previous study conducted on the same association mapping panel using a less dense physical map derived from diversity arrays technology (DArT) markers. GBS detected more QTLs than DArT markers although some of the QTLs were detected by DArT markers alone. Prediction accuracies from the two marker platforms were mostly similar and largely dependent on trait genetic architecture. The second part of this thesis focused on MAGIC populations, which incorporate diversity and novel allelic combinations from several generations of recombination. Pedigrees representing a wild rice MAGIC population were used to model MAGIC populations by simulation to assess the level of recombination and creation of novel haplotypes. The wild rice species are an important reservoir of beneficial genes that have been variously introgressed into rice varieties using bi-parental population approaches. The level of recombination was found to be highly dependent on the number of crosses made and on the resulting population size. Creation of MAGIC populations require adequate planning in order to make sufficient number of crosses that capture optimal haplotype diversity. The third part of the thesis considers models that have been proposed for genomic prediction. The ridge regression best linear unbiased prediction (RR-BLUP) is based on the assumption that all genotyped molecular markers make equal contributions to the variations of a phenotype. Information from underlying candidate molecular markers are however of greater significance and can be used to improve the accuracy of prediction. Here, an existing Differentially Penalized Regression (DiPR) model which uses modifications to a standard RR-BLUP package and allows two or more marker sets from different platforms to be independently weighted was used. The DiPR model performed better than single or combined marker sets for predicting most of the traits both in a MAGIC population and an association mapping panel. Overall the work presented in this thesis shows that while these techniques have great promise, they should be carefully evaluated before introduction into breeding programmes

Reference Genome Anchoring of High-Density Markers for Association Mapping and Genomic Prediction in European Winter Wheat.

In this study, we anchored genotyping-by-sequencing data to the International Wheat Genome Sequencing Consortium Reference Sequence v1.0 assembly to generate over 40,000 high quality single nucleotide polymorphism markers on a panel of 376 elite European winter wheat varieties released between 1946 and 2007. We compared association mapping and genomic prediction accuracy for a range of productivity traits with previous results based on lower density dominant DArT markers. The results demonstrate that the availability of RefSeq v1.0 supports higher precision trait mapping and provides the density of markers required to obtain accurate predictions of traits controlled by multiple small effect loci, including grain yield