Dissecting the genetics underlying the relationship between protein content and grain yield in a large hybrid wheat population.

KEY MESSAGE: Additive and dominance effect QTL for grain yield and protein content display antagonistic pleiotropic effects, making genomic selection based on the index grain protein deviation a promising method to alleviate the negative correlation between these traits in wheat breeding. Grain yield and quality-related traits such as protein content and sedimentation volume are key traits in wheat breeding. In this study, we used a large population of 1604 hybrids and their 135 parental components to investigate the genetics and metabolomics underlying the negative relationship of grain yield and quality, and evaluated approaches for their joint improvement. We identified a total of nine trait-associated metabolites and show that prediction using genomic data alone resulted in the highest prediction ability for all traits. We dissected the genetic architecture of grain yield and quality-determining traits and show results of the first mapping of the derived trait grain protein deviation. Further, we provide a genetic analysis of the antagonistic relation of grain yield and protein content and dissect the mode of gene action (pleiotropy vs linkage) of identified QTL. Lastly, we demonstrate that the composition of the training set for genomic prediction is crucial when considering different quality classes in wheat breeding.

Genome-based establishment of a high-yielding heterotic pattern for hybrid wheat breeding.

Hybrid breeding promises to boost yield and stability. The single most important element in implementing hybrid breeding is the recognition of a high-yielding heterotic pattern. We have developed a three-step strategy for identifying heterotic patterns for hybrid breeding comprising the following elements. First, the full hybrid performance matrix is compiled using genomic prediction. Second, a high-yielding heterotic pattern is searched based on a developed simulated annealing algorithm. Third, the long-term success of the identified heterotic pattern is assessed by estimating the usefulness, selection limit, and representativeness of the heterotic pattern with respect to a defined base population. This three-step approach was successfully implemented and evaluated using a phenotypic and genomic wheat dataset comprising 1,604 hybrids and their 135 parents. Integration of metabolomic-based prediction was not as powerful as genomic prediction. We show that hybrid wheat breeding based on the identified heterotic pattern can boost grain yield through the exploitation of heterosis and enhance recurrent selection gain. Our strategy represents a key step forward in hybrid breeding and is relevant for self-pollinating crops, which are currently shifting from pure-line to high-yielding and resilient hybrid varieties.

Genome-metabolite associations revealed low heritability, high genetic complexity, and causal relations for leaf metabolites in winter wheat (Triticum aestivum).

We investigated associations between the metabolic phenotype, consisting of quantitative data of 76 metabolites from 135 contrasting winter wheat (Triticum aestivum) lines, and 17 372 single nucleotide polymorphism (SNP) markers. Metabolite profiles were generated from flag leaves of plants from three different environments, with average repeatabilities of 0.5-0.6. The average heritability of 0.25 was unaffected by the heading date. Correlations among metabolites reflected their functional grouping, highlighting the strict coordination of various routes of the citric acid cycle. Genome-wide association studies identified significant associations for six metabolic traits, namely oxalic acid, ornithine, L-arginine, pentose alcohol III, L-tyrosine, and a sugar oligomer (oligo II), with between one and 17 associated SNPs. Notable associations with genes regulating transcription or translation explained between 2.8% and 32.5% of the genotypic variance (pG). Further candidate genes comprised metabolite carriers (pG 32.5-38.1%), regulatory proteins (pG 0.3-11.1%), and metabolic enzymes (pG 2.5-32.5%). The combinatorial use of genomic and metabolic data to construct partially directed networks revealed causal inferences in the correlated metabolite traits and associated SNPs. The evaluated causal relationships will provide a basis for predicting the effects of genetic interferences on groups of correlated metabolic traits, and thus on specific metabolic phenotypes.

Dissecting the genetic architecture of frost tolerance in Central European winter wheat.

Abiotic stress tolerance in plants is pivotal to increase yield stability, but its genetic basis is still poorly understood. To gain insight into the genetic architecture of frost tolerance, this work evaluated a large mapping population of 1739 wheat (Triticum aestivum L.) lines and hybrids adapted to Central Europe in field trials in Germany and fingerprinted the lines with a 9000 single-nucleotide polymorphism array. Additive effects prevailed over dominance effects. A two-dimensional genome scan revealed the presence of epistatic effects. Genome-wide association mapping in combination with a robust cross-validation strategy identified one frost tolerance locus with a major effect located on chromosome 5B. This locus was not in linkage disequilibrium with the known frost loci Fr-B1 and Fr-B2. The use of the detected diagnostic markers on chromosome 5B, however, does not allow prediction of frost tolerance with high accuracy. Application of genome-wide selection approaches that take into account also loci with small effect sizes considerably improved prediction of the genetic variation of frost tolerance in wheat. The developed prediction model is valuable for improving frost tolerance because this trait displays a wide variation in occurrence across years and is therefore a difficult target for conventional phenotypic selection.

Population structure, genetic diversity and linkage disequilibrium in elite winter wheat assessed with SNP and SSR markers.

Modern genomics approaches rely on the availability of high-throughput and high-density genotyping platforms. A major breakthrough in wheat genotyping was the development of an SNP array. In this study, we used a diverse panel of 172 elite European winter wheat lines to evaluate the utility of the SNP array for genomic analyses in wheat germplasm derived from breeding programs. We investigated population structure and genetic relatedness and found that the results obtained with SNP and SSR markers differ. This suggests that additional research is required to determine the optimum approach for the investigation of population structure and kinship. Our analysis of linkage disequilibrium (LD) showed that LD decays within approximately 5-10 cM. Moreover, we found that LD is variable along chromosomes. Our results suggest that the number of SNPs needs to be increased further to obtain a higher coverage of the chromosomes. Taken together, SNPs can be a valuable tool for genomics approaches and for a knowledge-based improvement of wheat.

Hybrid wheat: quantitative genetic parameters and consequences for the design of breeding programs.

KEY MESSAGE: Commercial heterosis for grain yield is present in hybrid wheat but long-term competiveness of hybrid versus line breeding depends on the development of heterotic groups to improve hybrid prediction. Detailed knowledge of the amount of heterosis and quantitative genetic parameters are of paramount importance to assess the potential of hybrid breeding. Our objectives were to (1) examine the extent of midparent, better-parent and commercial heterosis in a vast population of 1,604 wheat (Triticum aestivum L.) hybrids and their parental elite inbred lines and (2) discuss the consequences of relevant quantitative parameters for the design of hybrid wheat breeding programs. Fifteen male lines were crossed in a factorial mating design with 120 female lines, resulting in 1,604 of the 1,800 potential single-cross hybrid combinations. The hybrids, their parents, and ten commercial wheat varieties were evaluated in multi-location field experiments for grain yield, plant height, heading time and susceptibility to frost, lodging, septoria tritici blotch, yellow rust, leaf rust, and powdery mildew at up to five locations. We observed that hybrids were superior to the mean of their parents for grain yield (10.7 %) and susceptibility to frost (-7.2 %), leaf rust (-8.4 %) and septoria tritici blotch (-9.3 %). Moreover, 69 hybrids significantly (P < 0.05) outyielded the best commercial inbred line variety underlining the potential of hybrid wheat breeding. The estimated quantitative genetic parameters suggest that the establishment of reciprocal recurrent selection programs is pivotal for a successful long-term hybrid wheat breeding.

Negative dominance and dominance-by-dominance epistatic effects reduce grain-yield heterosis in wide crosses in wheat.

The genetics underlying heterosis, the difference in performance of crosses compared with midparents, is hypothesized to vary with relatedness between parents. We established a unique germplasm comprising three hybrid wheat sets differing in the degree of divergence between parents and devised a genetic distance measure giving weight to heterotic loci. Heterosis increased steadily with heterotic genetic distance for all 1903 hybrids. Midparent heterosis, however, was significantly lower in the hybrids including crosses between elite and exotic lines than in crosses among elite lines. The analysis of the genetic architecture of heterosis revealed this to be caused by a higher portion of negative dominance and dominance-by-dominance epistatic effects. Collectively, these results expand our understanding of heterosis in crops, an important pillar toward global food security.

A novel hybrid seed system for plants.

A two-component hybrid seed system has been developed that is broadly applicable and provides for effective generation and maintenance of the male-sterile parent, hybrid seed production and full restoration of fertility in the hybrid seed. The technology is based on the functional interaction of two loci that are inserted in the same position on two homologous chromosomes, and thus are 'linked in repulsion', and that jointly code for male sterility and herbicide resistance, both traits being expressed in heterozygous plants only. The localization to the same locus on a chromosome is achieved by the genetic transformation of plants with a construct containing both genetic elements (loci), and subsequent derivatization from the primary pro-locus of the two precursor lines using site-specific deletions. The functional interaction of the two loci is achieved through intein-based trans-splicing of two pairs of complementary protein fragments that provide for male sterility and herbicide resistance. Unlike the hybrid seed systems that are currently in use, the technology relies on the genetic modification of just one parent, and is therefore much simpler to develop and use. Arabidopsis has been used for the proof of principle presented here, but the essential elements of the technology are generic and have been shown to work in many crop species.