Epistasis-aware genome-wide association studies provide insights into the efficient breeding of high-yield and high-quality rice

Abstract

Marker-assisted selection (MAS) and genomic selection (GS) breeding have greatly improved the efficiency of rice breeding. Due to the influences of epistasis and gene pleiotropy, ensuring the actual breeding effect of MAS and GS is still a difficult challenge to overcome. In this study, 113 indica rice varieties (V) and their 565 testcross hybrids (TC) were used as the materials to investigate the genetic basis of 12 quality traits and nine agronomic traits. The original traits and general combining ability of the parents, as well as the original traits and mid-parent heterosis of TC, were subjected to genome-wide association analysis. In total, 381 primary significantly associated loci (SAL) and 1,759 secondary SALs that had epistatic interactions with these primary SALs were detected. Among these loci, 322 candidate genes located within or nearby the SALs were screened, 204 of which were cloned genes. A total of 39 MAS molecular modules that are beneficial for trait improvement were identified by pyramiding the superior haplotypes of candidate genes and desirable epistatic alleles of the secondary SALs. All the SALs were used to construct genetic networks, in which 91 pleiotropic loci were investigated. Additionally, we estimated the accuracy of genomic prediction in the parent V and TC by incorporating either no SALs, primary SALs, secondary SALs or epistatic effect SALs as covariates. Although the prediction accuracies of the four models were generally not significantly different in the TC dataset, the incorporation of primary SALs, secondary SALs, and epistatic effect SALs significantly improved the prediction accuracies of 5 (26%), 3 (16%), and 11 (58%) traits in the V dataset, respectively. These results suggested that SALs and epistatic effect SALs identified based on an additive genotype can provide considerable predictive power for the parental lines. They also provide insights into the genetic basis of complex traits and valuable information for molecular breeding in rice.