Structure and evolution of the Forsythieae genome elucidated by chromosome-level genome comparison of Abeliophyllum distichum and Forsythia ovata (Oleaceae)

Abeliophyllum distichum and Forsythia ovata are two closely related ornamental species of the tribe Forsythieae (Oleaceae) native to Korea. Here we report their genomic characteristics, highlighting genetic differences contributing to variations in corolla coloration, genomic variations associated with heterostyly, and the reconstruction of their ancestral karyotypes. Genome comparison revealed that A. distichum had a more compact organization of gene space than F. ovata. Centromeres of both species were enriched in Forsythieae-specific satellite repeats, hAT-Ac and MuLE-MuDR DNA transposons, and OTA-Athila Ty3/Gypsy retrotransposons. Transcriptome analysis revealed spatially differential expression of carotenoid biosynthesis-related genes in A. distichum, with downregulation in the white lobe and upregulation in the yellow base. Genome-wide analysis of structural variation in A. distichum identified retrotransposon insertions in the promoter region of an AGAMOUS homolog in the thrum plant, which showed significant downregulation of the gene compared to the pin plant. Evolutionary analyses suggested that the Oleaceae genomes evolved from 13 ancestral karyotypes via lineage-specific genomic events, including chromosome recombination, rearrangement, and whole-genome duplication followed by diploidization. The divergence of A. distichum and F. ovata was estimated to have occurred 13.87 million years ago during the Miocene epoch.