Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes

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Abstract
Sterility is common in hybrids between divergent populations, such as the indica and japonica subspecies of Asian cultivated rice ( Oryza sativa ). Although multiple loci for plant hybrid sterility have been identified, it remains unknown how alleles of the loci interact at the molecular level. Here we show that a locus for indica-japonica hybrid male sterility, Sa , comprises two adjacent genes, SaM and SaF , encoding a small ubiquitin-like modifier E3 ligase-like protein and an F-box protein, respectively. Most indica cultivars contain a haplotype SaM + SaF + , whereas all japonica cultivars have SaM − SaF − that diverged by nucleotide variations in wild rice. Male semi-sterility in this heterozygous complex locus is caused by abortion of pollen carrying SaM − . This allele-specific gamete elimination results from a selective interaction of SaF + with SaM − , a truncated protein, but not with SaM + because of the presence of an inhibitory domain, although SaM + is required for this male sterility. Lack of any one of the three alleles in recombinant plants does not produce male sterility. We propose a two-gene/three-component interaction model for this hybrid male sterility system. The findings have implications for overcoming male sterility in inter-subspecific hybrid rice breeding.