Two Tightly Linked Genes at the hsa1 Locus Cause Both F₁ and F₂ Hybrid Sterility in Rice

Molecular mechanisms of hybrid breakdown associated with sterility (F₂ sterility) are poorly understood as compared with those of F₁ hybrid sterility. Previously, we characterized three unlinked epistatic loci, hybrid sterility-a1 (hsa1), hsa2, and hsa3, responsible for the F₂ sterility in a cross between Oryza sativa ssp. indica and japonica. In this study, we identified that the hsa1 locus contains two interacting genes, HSA1a and HSA1b, within a 30-kb region. HSA1a-j (japonica allele) encodes a highly conserved plant-specific domain of unknown function protein (DUF1618), whereas the indica allele (HSA1a-i^s) has two deletion mutations that cause disruption of domain structure. The second gene, HSA1b-i^s, encodes an uncharacterized protein with some similarity to a nucleotide-binding protein. Homozygous introgression of indica HSA1a-i^s–HSA1b-i^s alleles into japonica showed female gamete abortion at an early mitotic stage. The fact that the recombinant haplotype HSA1a-j–HSA1b-i^s caused semi-sterility in the heterozygous state with the HSA1a-i^s–HSA1b-i^s haplotype suggests that variation in the hsa1 locus is a possible cause of the wide-spectrum sterility barriers seen in F₁ hybrids and successive generations in rice. We propose a simple genetic model to explain how a single causal mechanism can drive both F₁ and F₂ hybrid sterility.