Divergent selection and genetic introgression shape the genome landscape of heterosis in hybrid rice

Zechuan Lin, Peng Qin, Xuanwen Zhang, Chenjian Fu, Hanchao Deng, Xingxue Fu, Zhen Huang, Shuqin Jiang, Chen Li, Xiaoyan Tang, Xiangfeng Wang, Guangming He, Yuanzhu Yang, Hang He, and  View ORCID ProfileXing Wang Deng

PNAS March 3, 2020 117 (9) 4623-4631

Significance

The application of heterosis (hybrid vigor) in hybrid rice since the 1970s has tremendously improved rice productivity worldwide. But how breeders construct hybrid parents to obtain hybrid rice heterosis remains unclear. Here, by genome analysis, we found that breeders introduced different introgressed exogenous genomes of other rice subpopulations to construct male and female parents. The differentiated introgression in parents shaped heterotic loci in the hybrid rice. Genetic origin analysis revealed that heterotic loci existed in wild rice and were divergently selected among rice subpopulations. Our results traced the origin of heterotic loci of hybrid rice and uncovered genetic change of heterotic loci across rice evolution and breeding stages, which could facilitate the future breeding of more superior hybrid rice varieties.

Abstract

The successful application of heterosis in hybrid rice has dramatically improved rice productivity, but the genetic mechanism for heterosis in the hybrid rice remains unclear. In this study, we generated two populations of rice F₁ hybrids with present-day commercial hybrid parents, genotyped the parents with 50k SNP chip and genome resequencing, and recorded the phenotype of ∼2,000 hybrids at three field trials. By integrating these data with the collected genotypes of ∼4,200 rice landraces and improved varieties that were reported previously, we found that the male and female parents have different levels of genome introgressions from other rice subpopulations, including indica, aus, and japonica, therefore shaping heterotic loci in the hybrids. Among the introgressed exogenous genome, we found that heterotic loci, including Ghd8/DTH8, Gn1a, and IPA1 existed in wild rice, but were significantly divergently selected among the rice subpopulations, suggesting these loci were subject to environmental adaptation. During modern rice hybrid breeding, heterotic loci were further selected by removing loci with negative effect and fixing loci with positive effect and pyramid breeding. Our results provide insight into the genetic basis underlying the heterosis of elite hybrid rice varieties, which could facilitate a better understanding of heterosis and rice hybrid breeding.

See https://www.pnas.org/content/117/9/4623

Fig. 1:

A genomewide association study was used to identify potential heterotic loci in the hybrids. (A) Chromosomal distribution of heterotic loci identified in the 2014CS trial. Ellipses indicate the heterotic loci detected using the dominant/overdominant model, while rectangles represent those detected using the additive model. Different colors represent different traits. (B–D) Distribution of the degree of dominance of heterotic loci in the 2014CS (B), 2015CS (C), and 2015HF (D) trials. Only loci representing all three genotypes (one heterozygous and two homozygous genotypes) in the hybrids were investigated.