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

Abstract

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.

Fig. 1. Genetic diversity is maximized in the hybrid wheat parents.

The 217 parents of the Elite set, 98 Historic parents, and 69 Exotic parents were analyzed for linkage disequilibrium (LD) and population structure parameters. (A) Decay of LD (r²) with genetic map distance in the three sets and persistence of the LD phase based on pairwise correlations of LD phase between the three sets. Vertical dotted lines show the decay of LD below 0.1. (B) Neighbor-joining tree based on the results of F_ST statistics for the three sets. (C) Neighbor-joining tree based on modified Rogers’ distances. (D) Principal coordinate analysis based on modified Rogers’ distances. Percentages in parentheses refer to the proportion of genotypic variance explained by the first and second principal coordinates.

Fig. 2. Associations between grain-yield heterosis and midparent value for grain yield or genetic distance.

(A) Distribution of midparent heterosis (MPH) for grain yield for the Elite (1655), Historic×Elite (96), and Exotic×Elite (152) hybrids. The vertical dashed line indicates the mean. (B) Association between MPH and midparent value for grain yield. (C) Association between MPH and heterotic genetic distance (f_RD) or Rogers’ distance (RD). The colored trendlines are locally weighted regression lines for the Elite (blue) and Exotic×Elite sets (red).

Fig. 3. Genetic architecture of midparent heterosis for grain yield in wheat differs between Elite and Exotic×Elite hybrids.

Results are shown for the Elite (A to C and G) and Exotic×Elite hybrids (D to F and H). (A to F) The 21 chromosomes are indicated as bars in the inner circle; gray shadings differentiate the A, B, and D genomes. The genetic map positions of SNPs are given by gray connector lines. Colored links in the centers of the circles represent significant digenic epistatic interactions: additive-by-additive interactions (Aa and Da), additive-by-dominance interactions (B) and E), and dominance-by-dominance interactions (C and F). Manhattan plots for the dominance effects (Ab and Db) and the heterotic effects (Ac and Dc) from genome wide association mapping (GWAS). Significance thresholds are indicated as red dashed lines. (G and H) Partitioning of variance of heterosis for grain yield into its components (${\mathrm{\sigma }}_d^2$, dominance variance; ${\mathrm{\sigma }}_{a\times a}^2$, additive-by-additive variance; ${\mathrm{\sigma }}_{a\times d}^2$, additive-by-dominance variance; ${\mathrm{\sigma }}_{d\times d}^2$, dominance-by-dominance variance). (I) Venn diagram showing the number of overlapping heterotic QTL between the Elite and Exotic×Elite sets and the study by Jiang et al. (3).

Fig. 4. Negative dominance effects are more abundant in Exotic×Elite hybrids.

(A) Portion of positive and negative dominance effects in the Elite and Exotic×Elite hybrids, identified at a threshold of P < 0.001. (B) Histograms of these dominance effects.