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

Abstract

Understanding the genetic basis of reproductive barriers between species has been a central issue in evolutionary biology. The <i>S</i>_<i>1</i> locus in rice causes hybrid sterility and is a major reproductive barrier between two rice species, <i>Oryza sativa</i> and <i>Oryza glaberrima</i> The <i>O. glaberrima</i>-derived allele (denoted <i>S₁</i>^g) on the <i>S</i>_<i>1</i> locus causes preferential abortion of gametes with its allelic alternative (denoted <i>S₁</i>^s) in <i>S</i>_<i>1</i>^g/<i>S</i>_<i>1</i>^s heterozygotes. Here, we used mutagenesis and screening of fertile hybrid plants to isolate a mutant with an allele, <i>S</i>_<i>1</i>^mut, which does not confer sterility in the <i>S</i>_<i>1</i>^mut/<i>S</i>_<i>1</i>^g and <i>S</i>_<i>1</i>^mut/<i>S</i>_<i>1</i>^s hybrids. We found that the causal mutation of the <i>S</i>_<i>1</i>^mut allele was a deletion in the peptidase-coding gene (denoted "<i>SSP</i>") in the <i>S</i>_<i>1</i> locus of <i>O. glaberrima</i> No orthologous genes of <i>SSP</i> were found in the <i>O. sativa</i> genome. Transformation experiments indicated that the introduction of <i>SSP</i> in carriers of the <i>S</i>_<i>1</i>^s allele did not induce sterility. In <i>S</i>_<i>1</i>^mut/<i>S</i>_<i>1</i>^s heterozygotes, the insertion of <i>SSP</i> led to sterility, suggesting that <i>SSP</i> 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 <i>SSP</i> 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.