Divergent Evolution of Genes and Gene Expression Programs during Reproductive Transition Drives Inflorescence Architecture Diversity in Solanaceae

Phenotypic diversity is the ultimate result of divergent gene evolution. Genome-wide analyses across deep animal phylogeny have matched developmental phylotypic point with a molecular phylotypic point characterized by expression of ancient genes, revealing genome-wide divergent molecular evolution underlying phenotypic divergence. In Solanaceae, species produce inflorescences of diverse forms from a single flower to highly branched cymes. Our previous study in Solanum species has shown that slower meristem maturation causes increased meristem initiation, leading to more branched inflorescence. However, it is unknown whether the rate of meristem maturation determines inflorescence branching pattern beyond Solanum. Here we analyzed transcriptomes captured during meristem maturation by deep sequencing from Solanaceae species showing diverse inflorescence architecture, including tomato, pepper and Nicotiana benthamiana. We show that genes under divergent evolution express at higher levels when the meristems transition from vegetative to reproductive phase. In contrast, conserved genes are highly expressed in both vegetative and floral meristems, suggesting an older development program for vegetative growth and flower production. Tracing gene origins with phylostraigraphy-based Transcriptome Age Index (TAI), we show that the transition meristem stage is also characterized by expression of phylogenetically younger genes. Comparing the Transcriptome Maturaion Index (TMI) defined by dynamically expressed orthologous groups, we show that precocious meristem maturation, an early activation of the development program leading to reproductive transition, underlies the single flower inflorescence in pepper and N. benthamiana. Together, we propose a ‘spindle’ meristem maturation model: at transition stage divergent evolution in both genes and their expression programs drives Solanaceae inflorescence architecture evolution.