SSR-Sequencing Reveals the Inter- and Intraspecific Genetic Variation and Phylogenetic Relationships among an Extensive Collection of Radish (Raphanus) Germplasm Resources

SIMPLE SUMMARY: Raphanus is an important genus of Brassicaceae and has undergone a lengthy evolutionary process. However, the inter- and intraspecific phylogenetic relationships and genetic diversity are not well understood. To elucidate these issues, we SSR-sequenced 939 wild, semi-wild and cultivated accessions, and discovered that Europe was the origin center of radishes with diverse European wild radishes, and Europe, South Asia and East Asia might be three independent domestication centers. There was considerable genetic differentiation within European cultivated radishes. European primitive cultivated radish exhibited gene flow with black radish/oil radish and rat-tail radish. Among Asian cultivated radishes, rat-tail radish was a sister to the clade of Chines big radish (including Japanese wild radish), suggesting that they may share the most recent common ancestry. Japanese wild radish had strong gene exchange with Japanese/Korea big radish, oil radish and rat-tail radish. American wild radish developed from natural hybridization between European wild radish and European small radish. All these demonstrated that European primitive cultivated type, American wild radish and Japanese wild radish might have played indispensable roles in radish evolution. Our study provides new perspectives into the origin, evolution and genetic diversity of Raphanus and facilitates the conservation and exploitation of radish germplasm resources. ABSTRACT: Raphanus has undergone a lengthy evolutionary process and has rich diversity. However, the inter- and intraspecific phylogenetic relationships and genetic diversity of this genus are not well understood. Through SSR-sequencing and multi-analysis of 939 wild, semi-wild and cultivated accessions, we discovered that the European wild radish (EWR) population is separated from cultivated radishes and has a higher genetic diversity. Frequent intraspecific genetic exchanges occurred in the whole cultivated radish (WCR) population; there was considerable genetic differentiation within the European cultivated radish (ECR) population, which could drive radish diversity formation. Among the ECR subpopulations, European primitive cultivated radishes (EPCRs) with higher genetic diversity are most closely related to the EWR population and exhibit a gene flow with rat-tail radishes (RTRs) and black radishes (BRs)/oil radishes (ORs). Among Asian cultivated radishes (ACRs), Chinese big radishes (CBRs) with a relatively high diversity are furthest from the EWR population, and most Japanese/Korean big radishes (JKBRs) are close to CBR accessions, except for a few old Japanese landraces that are closer to the EPCR. The CBR and JKBR accessions are independent of RTR accessions; however, phylogenetic analysis indicates that the RTR is sister to the clade of CBR (including JWR), which suggests that the RTR may share the most recent common ancestry with CBRs and JWRs. In addition, Japanese wild radishes (JWRs), (namely, R. sativus forma raphanistroides) are mainly scattered between CBRs and EPCRs in PCoA analysis. Moreover, JWRs have a strong gene exchange with the JKBR, OR and RTR subpopulations. American wild radishes (AWRs) are closely related to European wild and cultivated radishes, and have a gene flow with European small radishes (ESRs), suggesting that the AWR developed from natural hybridization between the EWR and the ESR. Overall, this demonstrates that Europe was the origin center of the radish, and that Europe, South Asia and East Asia appear to have been three independent domestication centers. The EPCR, AWR and JWR, as semi-wild populations, might have played indispensable transitional roles in radish evolution. Our study provides new perspectives into the origin, evolution and genetic diversity of Raphanus and facilitates the conservation and exploitation of radish germplasm resources.