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A quantitative genetic framework highlights the role of epistatic effects for grain-yield heterosis in bread wheat

Nature Genetics volume 49, pages 1741–1746 (2017)Cite this article

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Abstract

Increasing wheat yield is a key global challenge to producing sufficient food for a growing human population. Wheat grain yield can be boosted by exploiting heterosis, the superior performance of hybrids compared with midparents. Here we present a tailored quantitative genetic framework to study the genetic basis of midparent heterosis in hybrid populations derived from crosses among diverse parents. We applied this framework to an extensive data set assembled for winter wheat. Grain yield was assessed for 1,604 hybrids and their 135 parental elite breeding lines in 11 environments. The hybrids outperformed the midparents by 10% on average, representing approximately 15 years of breeding progress in wheat, thus further substantiating the remarkable potential of hybrid-wheat breeding. Genome-wide prediction and association mapping implemented through the developed quantitative genetic framework showed that dominance effects played a less prominent role than epistatic effects in grain-yield heterosis in wheat.

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Figure 1: Strategy to define, estimate and test the heterotic effect of a QTL.
Figure 2: Grain-yield performance and midparent heterosis for grain yield.
Figure 3
Figure 4: Genetic architecture of midparent heterosis for grain yield in wheat.
Figure 5: Proportion of phenotypic variance of grain-yield heterosis explained by heterotic QTL effects.

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Acknowledgements

The Federal Ministry of Education and Research of Germany is acknowledged for funding (grant FKZ031B0184A (Y.J.)).

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Authors and Affiliations

  1. Department of Breeding Research, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany

    Yong Jiang, Renate H Schmidt, Yusheng Zhao & Jochen C Reif

Authors
  1. Yong Jiang
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  2. Renate H Schmidt
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  3. Yusheng Zhao
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  4. Jochen C Reif
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Contributions

J.C.R. and Y.Z. supervised the study. Y.J. derived the analytical results and performed statistical analysis. J.C.R., R.H.S., and Y.J. wrote the paper.

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Correspondence to Jochen C Reif.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 The factorial mating design of the population of hybrids.

Rows corresponding to male parental lines and columns representing female parental lines were ordered via hierarchical clustering. The red and blue boxes indicate the presence and absence of the corresponding hybrids used in this study, respectively.

Supplementary Figure 2 Hierarchical clustering analysis of 135 parental lines.

Male and female lines were labeled red and blue, respectively. The clustering analysis was performed based on Rogers’ distance.

Supplementary Figure 3 Probability distribution of linkage disequilibrium (LD) measured as r2 between adjacent SNPs.

Supplementary Figure 4 Distribution of best linear unbiased estimates (BLUEs) for grain yield of the parental lines and hybrids.

Supplementary Figure 5 Distribution of relative midparent heterosis values for grain yield.

Supplementary Figure 6 Quantile–quantile plots of the expected and observed –log(P) values in association mapping.

Results were shown for (a) dominance; (b) additive-by-additive; (c) additive-by-dominance and (d) dominance-by-dominance effects. Red lines reflect the trends expected assuming absence of marker-trait associations.

Supplementary Figure 7 Cumulative proportion of variance explained by the principal components for marker pairs showing significant epistatic effects.

Results were shown for (a) the 681 pairs of markers showing significant additive-by-additive epistatic effects, (b) the 205 pairs of markers displaying significant additive-by-dominance epistatic effects, and (c) the 380 pairs of markers revealing significant dominance-by-dominance epistatic effects. The dashed vertical lines indicate the number of PCs needed to explain 99% of the variance, which are 34 in (a), 15 in (b) and 46 in (c). The principal component analysis was performed based on the matrix whose columns consist of element-wise products of the vectors of relevant marker pairs.

Supplementary Figure 8 Distribution of linkage disequilibrium (r2) between pairs of markers showing significant digenic epistatic effects.

Results were shown for markers showing significant additive-by-additive (aa), additive-by-dominance (ad), and dominance-by-dominance (dd) epistatic effects.

Supplementary Figure 9 Distribution of –log(P) values in the association mapping of dominance effects.

Results were shown for (a) markers with a minor allele frequency higher than 0.05, and (b) markers with a minor allele frequency smaller than 0.05.

Supplementary Figure 10 Manhattan plots of the genome-wide association mapping for additive and dominance effects for grain yield in different populations.

Results were shown for additive effects in the populations of (a) 135 parental lines and (b) 1,604 hybrids, as well as (c) for dominance effects for grain yield in the population of 1,604 hybrids. The red horizontal lines refer to significance thresholds of P < 0.05 correcting for multiple testing with the Bonferroni-Holm procedure36.

Supplementary Figure 11 Distribution of minor allele frequencies for markers showing significant epistatic effects.

Results were shown for (a) significant additive-by-additive epistatic effects, (b) significant additive-by-dominance epistatic effects, (c) significant dominance-by-dominance epistatic effects, and (d) all markers.

Supplementary Figure 12 The distribution of minor two-locus genotype frequencies for all marker pairs and those showing significant epistatic effects.

The distribution of minor two-locus double homozygote genotype frequencies for (a) all pairs of markers and (b) those showing significant additive-by-additive epistatic effects, the distribution of minor two-locus single heterozygote genotype frequencies for (c) all pairs of markers and (d) those revealing significant additive-by-dominance epistatic effects, as well as the distribution of two-locus double heterozygote genotype frequencies for (e) all pairs of markers and (f) those displaying significant dominance-by-dominance epistatic effects.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–12, Supplementary Tables 1, 2 and 5, and Supplementary Note

Life Sciences Reporting Summary

Supplementary Table 3

List of marker pairs showing significant epistatic effects contributing to midparent heterosis

axa: additive-by-additive effects; axd: additive-by-dominance effects; dxd: dominance-by-dominance effects; R2 : proportion of explained phenotypic variance

Supplementary Table 4

List of markers showing significant heterotic effects

R2 : proportion of explained phenotypic variance

Supplementary Data 1

Sample R codes for implementing genomic prediction, genomewide association mapping for dominance, epistatic and heterotic effects for midparent heterosis

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Jiang, Y., Schmidt, R., Zhao, Y. et al. A quantitative genetic framework highlights the role of epistatic effects for grain-yield heterosis in bread wheat. Nat Genet 49, 1741–1746 (2017). https://doi.org/10.1038/ng.3974

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