Origin, loss, and regain of self-incompatibility in angiosperms

• Published in: The Plant cell 2022-01, Vol.34 (1), p.579-596
• Main Authors: Zhao, Hong, Zhang, Yue, Zhang, Hui, Song, Yanzhai, Zhao, Fei, Zhang, Yu'e, Zhu, Sihui, Zhang, Hongkui, Zhou, Zhendiao, Guo, Han, Li, Miaomiao, Li, Junhui, Gao, Qiang, Han, Qianqian, Huang, Huaqiu, Copsey, Lucy, Li, Qun, Chen, Hua, Coen, Enrico, Zhang, Yijing, Xue, Yongbiao
• Format: Article
• Language: English
• Subjects: Biological Evolution; Germ Cells, Plant - physiology; Magnoliopsida - physiology; Regular Issue; Self-Incompatibility in Flowering Plants - genetics
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1093/plcell/koab266

The self-incompatibility (SI) system with the broadest taxonomic distribution in angiosperms is based on multiple S-locus F-box genes (SLFs) tightly linked to an S-RNase termed type-1. Multiple SLFs collaborate to detoxify nonself S-RNases while being unable to detoxify self S-RNases. However, it is unclear how such a system evolved, because in an ancestral system with a single SLF, many nonself S-RNases would not be detoxified, giving low cross-fertilization rates. In addition, how the system has been maintained in the face of whole-genome duplications (WGDs) or lost in other lineages remains unclear. Here we show that SLFs from a broad range of species can detoxify S-RNases from Petunia with a high detoxification probability, suggestive of an ancestral feature enabling cross-fertilization and subsequently modified as additional SLFs evolved. We further show, based on its genomic signatures, that type-1 was likely maintained in many lineages, despite WGD, through deletion of duplicate S-loci. In other lineages, SI was lost either through S-locus deletions or by retaining duplications. Two deletion lineages regained SI through type-2 (Brassicaceae) or type-4 (Primulaceae), and one duplication lineage through type-3 (Papaveraceae) mechanisms. Thus, our results reveal a highly dynamic process behind the origin, maintenance, loss, and regain of SI.