Two chromosome‐level genome assemblies of Rhodiola shed new light on genome evolution in rapid radiation and evolution of the biosynthetic pathway of salidroside

SUMMARY Rhodiola L. is a genus that has undergone rapid radiation in the mid‐Miocene and may represent a typic case of adaptive radiation. Many species of Rhodiola have also been widely used as an important adaptogen in traditional medicines for centuries. However, a lack of high‐quality chromosome‐level genomes hinders in‐depth study of its evolution and biosynthetic pathway of secondary metabolites. Here, we assembled two chromosome‐level genomes for two Rhodiola species with different chromosome number and sexual system. The assembled genome size of R. chrysanthemifolia (2n = 14; hermaphrodite) and R. kirilowii (2n = 22; dioecious) were of 402.67 and 653.62 Mb, respectively, with approximately 57.60% and 69.22% of transposable elements (TEs). The size difference between the two genomes was mostly due to proliferation of long terminal repeat‐retrotransposons (LTR‐RTs) in the R. kirilowii genome. Comparative genomic analysis revealed possible gene families responsible for high‐altitude adaptation of Rhodiola, including a homolog of plant cysteine oxidase 2 gene of Arabidopsis thaliana (AtPCO2), which is part of the core molecular reaction to hypoxia and contributes to the stability of Group VII ethylene response factors (ERF‐VII). We found extensive chromosome fusion/fission events and structural variations between the two genomes, which might have facilitated the initial rapid radiation of Rhodiola. We also identified candidate genes in the biosynthetic pathway of salidroside. Overall, our results provide important insights into genome evolution in plant rapid radiations, and possible roles of chromosome fusion/fission and structure variation played in rapid speciation. Significance Statement We assembled two chromosome‐level genomes for two Rhodiola species with different chromosome number and sexual system. Comparative genomic analyses demonstrated extensive chromosome fusion/fissions and structural variations between the two genomes, which might have played a role in rapid establishment of post‐zygotic reproductive isolation, facilitating the initial rapid radiation of Rhodiola. Possible gene families responsible for high‐altitude adaptation and the salidroside biosynthesis pathway were identified, and the salidroside biosynthesis pathway might evolve in a stepwise manner in Rhodiola.