Chloroplast genome and haplotype relationships unravel the genetic introgression and complex evolutionary history of East Asian Rosa section Synstylae roses (Rosaceae)

Abstract Background The section Synstylae of the genus Rosa (Rosaceae) is predominantly distributed across the Eastern Asiatic Floristic Region and is characterized by increased species diversity and natural hybrids. These characteristics render species within this section exemplary for studying phenotypic variability and easy crossbreeding, which hold potential for advancements in the rose-breeding industry. However, genetic introgression and hybridization have posed challenges to our understanding of their phylogenetic relationships. Despite recurrent interspecific introgression, chloroplast DNA can still aid in phylogenetic inference within the section Synstylae due to its uniparental inheritance and high conservation. Results Phylogenetic inferences and haplotype network analysis identified seven distinct chloroplast haplotype groups within the East Asian Synstylae. Clear differentiation was observed between the chloroplast haplotypes of the Sino-Himalayan series Brunonianae and Sino-Japanese series Multiflorae lineages. The chloroplast haplotypes within each lineage aligned more closely with geographic gradients than with species boundaries. Consequently, various chloroplast haplotypes were shared among Sino-Japanese Synstylae species with broader distributions, whereas unique haplotypes were found in the species with restricted distribution ranges. Similarly, geographically specific haplotype groups were identified in the Japanese Archipelago, Taiwan, and Eastern China of the Sino-Japanese Subregion, respectively. Conclusions The chloroplast genomes of Sino-Japanese Synstylae species may have diverged along geographic gradients, influenced by the geographical and ecological complexity of East Asia and the climate oscillations during the Pleistocene. The recurring cycles of fragmentation and rejoining in Sino-Japanese Synstylae populations have allowed founder effects and genetic drift to drive divergence and diversification of their chloroplast genomes along these geographic gradients. The substantial incongruence between the chloroplast and nuclear phylogenies evidenced the prevalent genetic introgression within the Sino-Japanese Synstylae lineage. Additionally, two putative hybrid speciation events highlighted the role of genetic introgression in species diversification of the East Asian Synstylae lineage. This study substantiates the value of chloroplast genomes in elucidating genetic introgression and the unique evolutionary history of recently diverged and closely related East Asian Synstylae species.