The snapdragon genomes reveal the evolutionary dynamics of the S locus supergene

The multi-allelic S-locus, containing a pistil S-RNase and dozens of S-locus F-box (SLF), underlies genetic control of self-incompatibility (SI) in Antirrhinum hispanicum. The genus Antirrhinum, harboring such a SI system has been used as a model to study self-incompatibility extensively. However, there have been limited studies on the genomic organization of the S-locus supergene due to a lack of high-quality genomic data. Here, we present the chromosome-level reference and haplotype-resolved genome assemblies of a self-incompatible Antirrhinum hispanicum line, AhS7S8. Alongside with the draft genome of Misopates orontium, comparative genomics reveals that A.hispanicum diverged from its self-compatible cousin 12.3 million years ago (Mya). Expanded gene families enriched in distinct functional terms implied different evolutionary trajectories of outcrossing and selfing species. For the first time, two complete A.hispanicum S-haplotypes spanning [~]1.2Mb and containing 32 SLFs were reconstructed, while most of the SLFs derived from retroelement-mediated proximal or tandem duplication approximately 122 Mya. Moreover, we detected a candidate cis-transcription factor associated with regulating SLFs expression, and two miRNAs may control the expression of this transcription factor. Inter-specific S-locus and intra-specific S-haplotype comparisons revealed the dynamic nature and polymorphism of the S-locus supergene mediated by continuous gene duplication, segmental translocation or loss, and TE-involved transposition events. Our data provides an excellent resource for future research on the evolutionary studies on S-RNase-based self-incompatibility system.