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

Abstract

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‐70S1300S6’) 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‐70S1300S6’ line, we observed lower levels of DNA methylation in BnSCR‐6 and BnSCR‐1300 promoters. Furthermore, the overexpression of BnSMI2‐1300 in the ‘SI‐326S7S6’ 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.