Chromosomal structural variation loci HSS1 and HSS6 lead to hybrid sterility in rice

Chromosomal structural variation leads to rice hybrid sterility, and this study has established a new inheritance model and offers a novel insight into hybrid sterility in rice. The utilization of heterosis among different species significantly enhances rice yield. However, the direct application of this advantage is hindered by hybrid sterility (HS). Here we identify a stable semi-sterile inbred line (SSIL) in the hybridization between rice species O. sativa indica and wild rice O. longistaminata. Both pollen and spikelet fertility in heterozygous SSIL plants are semi-sterile, and the homozygous plants show normal fertility. Interestingly, unlike previously reported hybrid sterility loci, SSIL does not induce segregation distortion in progeny. The genotypes of chromosome 1 (Chr.1) exhibit tight pseudo-linkage on Chr.6 in SSIL population. HSS1 and HSS6 are named as the two loci of Chr.1 and Chr.6. Cytological observations revealed abnormalities in male and female gametes during meiosis, ultimately resulting in semi-sterile pollen and spikelet. HSS1 was narrowed down to a 190.6-kb interval and HSS6 to a 1391.6-kb region using an SSIL population of 10,393 plants. Through high-throughput sequencing and observation of chromosomal behavior during meiosis, a reciprocal translocation between the short arm of Chr.1 and the end of Chr.6 in the translocated RD23-type (R^T-type) gamete in SSIL was discovered. The presence of R^T-type gametes in SSIL is the direct causative factor for semi-sterility in both male and female gametes. This translocation led to abnormal SSIL-R^T/L synapses and the formation of tetravalent ring structures in chromosomes during pachynema. Our findings have uncovered a pair of reciprocal chromosome translocations that control reproductive isolation in rice. These insights offer valuable guidance for optimizing hybrid breeding applications, ultimately enhancing the benefits of heterosis.