The self‐compatibility is acquired after polyploidization: a case study of Brassica napus self‐incompatible trilinear hybrid breeding system

Summary Self‐incompatibility plays a vital role in angiosperms, by preventing inbreeding depression and maintaining genetic diversity within populations. Following polyploidization, many angiosperm species transition from self‐incompatibility to self‐compatibility. Here, we investigated the S ‐locus in Brassicaceae and identified distinct origins for the sRNA loci, SMI and SMI2 ( SCR Methylation Inducer 1 and 2 ), within the S ‐locus. The SMI loci were found to be widespread in Cruciferae, whereas the SMI2 loci were exclusive to Brassica species. Additionally, we discovered four major S ‐haplotypes ( BnS‐1 , BnS‐6 , BnS‐7 , and BnS‐1300 ) in rapeseed. Overexpression of BnSMI‐1 in self‐incompatible Brassica napus (‘S‐70 S1300S6 ’) resulted in a significant increase in DNA methylation in the promoter regions of BnSCR‐6 and BnSCR‐1300 , leading to self‐compatibility. Conversely, by overexpressing a point mutation of BnSmi‐1 in the ‘S‐70 S1300S6 ’ line, we observed lower levels of DNA methylation in BnSCR‐6 and BnSCR‐1300 promoters. Furthermore, the overexpression of BnSMI2‐1300 in the ‘SI‐326 S7S6 ’ line inhibited the expression of BnSCR‐7 through transcriptional repression of the Smi2 sRNA from the BnS‐1300 haplotype. Our study demonstrates that the self‐compatibility of rapeseed is determined by S ‐locus sRNA‐mediated silencing of SCR after polyploidization, which helps to further breed self‐incompatible or self‐compatible rapeseed lines, thereby facilitating the utilization of heterosis.