Evolutionary Origin of Flowers: A Genome-Wide Study of Floral Development Genes in Seed Plants

Darwin famously characterized the origin and rapid diversification of the angiosperms as an abominable mystery. In recent years, new advances in the fields of molecular phylogenetics and evolutionary developmental biology have not only corrected the mistakes in previous theories and models, but also proposed new and testable hypotheses, revealed possible processes through which the flower first originated, and discussed the contributions of the duplication   and diversification of floral developmental genes to the origin of flowers. However, previous studies are insufficient for a complete understanding the contributions of genomic changes to those biological innovations. Here, we examined the origin and duplication history of orthogroups containing 424 genes known to play roles in Arabidopsis floral timing and development, and found that upstream genes in the floral developmental regulatory network had higher frequencies of old orthogroups that originated with tracheophytes, and downstream genes were overrepresented by those in new orthogroups originated within derived angiosperms. Furthermore, the similar pattern was found when using 1312 core-floral genes, which conserved expressed in flower tissues of water lily, rice, California poppy, and Arabidopsis. These results suggest that although much of the floral development genetic toolkit is ancient, gene recruitment has been an ongoing process in floral evolution, and that different components of the floral regulatory network have recruited genes at different rates through history, with a larger proportion of new orthogroups being represented by genes functioning in organ identity, development and maturation than by genes functioning in the environment sensing and floral timing.