Large scale genomic and transcriptomic profiles of rice hybrids revealed a novel universal mechanism underlying yield heterosis

Abstract The utilization of heterosis (or hybrid vigor) is a revolutionary technology in agricultural. However, its genetic mechanisms are still unclear in plants. Here we develop, sequence and record the phenotypes of 418 hybrids from crosses between two testers and a diverse mini core collection. Phenotypic analysis showed that heterosis is an extensive but not necessary phenomenon, which varied by combinations and environments. Evidence from both GWAS on the 418 hybrids and their parents and transcriptomics of the traditional rice hybrid Liangyoupei 9, indicated that dominance and overdominance are the main genetic contributions to heterosis. Furthermore, cumulation or complementation of repulsive genetic factors may account for 37.8% of the overdominant QTL and nearly half of the genes with overdominant expression pattern. We systematically compared non-additive and additive factors and observed a common phenomenon that non-additive factors are more sensitive to background than that of additive ones across species, phenotypes, QTLs and transcription levels, further evidence from both simulations and experiment demonstrated a novel universal molecular mechanism underlying heterosis, i.e. homo-insufficiency under insufficient background (HoIIB), which expounds that heterosis in most cases is not the heterozygote advantage but the homozygote disadvantage under the insufficient genetic background. The HoIIB model can explain most known hypotheses and phenomena about heterosis, thus provides a novel theory for future hybrid rice breeding.