Allopolyploidization events and immense paleogenome reshuffling underlying the diversification of plants and secondary metabolites in Oleaceae

Abstract

Oleaceae, a eudicot family with great species diversity, has attracted much attention from botanists because it contains many plants with important economic, medicinal, and ornamental values. However, the history of polyploidization and ancestral genome reshuffling of Oleaceae remains unclear. Here, we clarified an Oleaceae‐common hexaploidization (OCH) event occurring at ~53–61 million years ago (Ma) common in all Oleaceae plants and an Oleaceae‐recent tetraploidization (ORT) event occurring at ~18–21 Ma shared by the lineages of Syringa, Olea, Osmanthus, and Fraxinus. We found that high‐frequency polyploidization events drove the frequency of gene loss in Oleaceae genomes and extended the size of regions containing adjacent gene loss, thereby promoting the degree of genome fragmentation. We revealed that biased fractionation between the OCH‐ and ORT‐produced subgenomes is likely attributed to the origin of allopolyploidization in the OCH and ORT events. Significantly, through paleochromosome rearrangement comparisons, we proposed a "two‐step" genome duplication model for OCH and determined the duplicated orders of OCH tripled genome. We reconstructed 11 protochromosomes of the most recent ancestral Oleaceae karyotype (AOK) and elucidated the trajectories of immense paleochromosome reorganization of Oleaceae species from ancestral eudicot karyotype. Notably, we tracked the diversification history of secondary metabolite synthesis genes in the Oleaceae and explored the effects of paleogenome evolution on specialized metabolite synthesis. Our findings provide new insights into the polyploidization and paleogenomic evolution of Oleaceae and have important scientific significance for understanding the genetic basis of species and secondary metabolic diversity in Oleaceae.