Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice

Understanding the genetic basis of reproductive barriers between species has been a central issue in evolutionary biology. The S-1 locus in rice causes hybrid sterility and is a major reproductive barrier between two rice species, Oryza sativa and Oryza glaberrima. The O. glaberrima-derived allele (denoted S-1(g)) on the S-1 locus causes preferential abortion of gametes with its allelic alternative (denoted S-1(s)) in S-1(g)/S-1(s) heterozygotes. Here, we used mutagenesis and screening of fertile hybrid plants to isolate a mutant with an allele, S-1(mut), which does not confer sterility in the S-1(mut)/S-1(g) and S-1(mut)/S-1(s) hybrids. We found that the causal mutation of the S-1(mut) allele was a deletion in the peptidase-coding gene (denoted SSP) in the S-1 locus of O. glaberrima. No orthologous genes of SSP were found in the O. sativa genome. Transformation experiments indicated that the introduction of SSP in carriers of the S-1(s) allele did not induce sterility. In S-1(mut)/S-1(s) heterozygotes, the insertion of SSP led to sterility, suggesting that SSP complemented the loss of the functional phenotype of the mutant and that multiple factors are involved in the phenomenon. The polymorphisms caused by the lineage-specific acquisition or loss of the SSP gene were implicated in the generation of hybrid sterility. Our results demonstrated that artificial disruption of a single gene for the reproductive barrier creates a neutral allele, which facilitates interspecific hybridization for breeding programs.