A distorter-restorer system drives quantitative reproductive isolation in rice

Hybrid sterility and segregation distortion are the major forms of postzygotic reproductive isolation in rice, yet the molecular basis of their quantitative variation remains unclear. Here we identify S44, a natural distorter-restorer system in Oryza longistaminata/Asian cultivated rice hybrids, comprising four tightly linked elements-Reproductive Isolation Distorter (RID), Reproductive Isolation Restorer (RIR), Reproductive Isolation Activator (RIA) and Reproductive Isolation Suppressor (RIS)-which collectively regulate hybrid male sterility and segregation distortion. The distorter RID triggers the elimination of O. sativa cultivar RD23 pollen, whereas the restorer RIR selectively safeguards O. longistaminata gametes, thereby preferentially transmitting its allele into the progeny. RIS and RIA fine-tune segregation distortion. We further demonstrate that the allelic conflicts at the S44 locus drive quantitative reproductive isolation between O. longistaminata and other rice lineages, and CRISPR-engineered RID knockout can universally overcome S44-mediated reproductive barriers in the AA genome, enabling revolutionary cross-species breeding. This distorter-restorer system provides a unique genetic module for deciphering speciation mechanisms and advancing crop breeding strategies.