Phylogenomics Resolves the Phylogeny of Theaceae by Using Low-Copy and Multi-Copy Nuclear Gene Makers and Uncovers a Fast Radiation Event Contributing to Tea Plants Diversity

SIMPLE SUMMARY: The Theaceae includes more than 300 species of great morphological diversity and has immense economic, cultural, and ornamental values. However, the evolutionary history of this family remains elusive. We integrated 91 genomes and transcriptome datasets of Theaceae and successfully resolved the phylogeny of Theaceae including relatives of cultivated tea plants from both extensive low-copy and multi-copy nuclear gene markers. Bayes-based molecular dating revealed that the ancestor of the tea family originated slightly earlier than the K-Pg boundary (Mass extinction events including the extinction of dinosaurs) with early diversification of three tribes associated with the Early Eocene Climatic Optimum. Further speciation analysis suggested a sole significant diversification shift rate in the common ancestor of Camellia associated with the Mid-Miocene Climatic Optimum. Collectively, polyploidy events, and key morphological innovation characters, such as pericarp with seed coat hardening, could possibly contribute to the Theaceae species diversity. ABSTRACT: Tea is one of the three most popular nonalcoholic beverages globally and has extremely high economic and cultural value. Currently, the classification, taxonomy, and evolutionary history of the tea family are largely elusive, including phylogeny, divergence, speciation, and diversity. For understanding the evolutionary history and dynamics of species diversity in Theaceae, a robust phylogenetic framework based on 1785 low-copy and 79,103 multi-copy nuclear genes from 91 tea plant genomes and transcriptome datasets had been reconstructed. Our results maximumly supported that the tribes Stewartieae and Gordonieae are successive sister groups to the tribe Theeae from both coalescent and super matrix ML tree analyses. Moreover, in the most evolved tribe, Theeae, the monophyletic genera Pyrenaria, Apterosperma, and Polyspora are the successive sister groups of Camellia. We also yield a well-resolved relationship of Camellia, which contains the vast majority of Theaceae species richness. Molecular dating suggests that Theaceae originated in the late L-Cretaceous, with subsequent early radiation under the Early Eocene Climatic Optimal (EECO) for the three tribes. A diversification rate shift was detected in the common ancestors of Camellia with subsequent acceleration in speciation rate under the climate optimum in the early Miocene. These results provide a phylogenetic framework and new insights into factors that likely have contributed to the survival of Theaceae, especially a successful radiation event of genus Camellia members to subtropic/tropic regions. These novel findings will facilitate the efficient conservation and utilization of germplasm resources for breeding cultivated tea and oil-tea. Collectively, these results provide a foundation for further morphological and functional evolutionary analyses across Theaceae.