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

Marker-assisted selection (MAS) and genomic selection (GS) breeding have greatly improved the efficiency of rice breeding. Due to the influence of epistasis and gene pleiotropy, how to ensure the actual breeding effect of MAS and GS is still a difficult problem to overcome. In this study, 113 indicarice varieties (V) and their 565 testcross hybrids (TC) were used as materials to investigate the genetic basis of 12 quality traits and 9 agronomic traits. The original traits and general combining ability of parents, as well as the original traits and mid-parent heterosis of testcross hybrids were subjected to genome-wide association analysis. In total, 381 primary significantly associated loci (SAL) and 1759 secondary SALs that had epistatic interaction with these primary SALs were detected. 322 candidate genes located within or nearby the SALs were screened, of which 204 were cloned genes. A total of 39 MAS molecular modules that are beneficial for trait improvement was identified by pyramiding the superior haplotype of candidate genes and desirable epistatic allele of 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 parent varieties and testcross hybrids by incorporating no SALs, primary SALs, secondary SALs or epistatic effect SALs as covariates. Although the prediction accuracy of the four models was mostly not significantly different in the TC dataset, the incorporation of primary SALs, secondary SALs, and epistatic effect SALs significantly improved the prediction accuracy 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 additive genotype can provide considerable predictive power for parental lines. These results provide insights into the genetic basis of complex traits and valuable information for molecular breeding in rice.