The Evolution of Inflorescence Diversity in the Nightshades and Heterochrony during Meristem Maturation

One of the most remarkable manifestations of plant evolution is the diversity of floral branching systems. These inflorescences arise from stem cell populations in shoot meristems that gradually mature to a reproductive state. Genetic analyses in model and crop species have revealed several pathways controlling meristem maturation and their significance for inflorescence development. However, the basis for the continuum of inflorescence complexity observed in nature is poorly understood. In the nightshade (Solanaceae) family, which includes pepper and tomato, inflorescences range from solitary flowers to highly elaborate branched structures that can bear dozens or hundreds of flowers. Here we compare transcriptome profiles of meristem maturation stages from five domesticated and wild Solanaceae species reflecting the evolutionary range of inflorescence complexity. We find these species share hundreds of dynamically expressed genes enriched for transcription factors. Principal component analysis shows meristem stages have distinct molecular identities, and points to modified maturation schedules underlying architectural variation. These modified schedules are reflected in a peak of transcriptome divergence during reproductive transition, driven by heterochronic shifts of a small subset of dynamic genes including transcriptional regulators with known roles in flowering. Thus, quantitative variation in Solanaceae inflorescence complexity is determined within a critical transitional window of meristem maturation, which we propose is the foundation for similar examples of inflorescence diversity in the plant kingdom. More broadly, our findings resemble a recently proposed transcriptome “inverse hourglass” model for animal embryogenesis, suggesting both plant and animal development morphological variation is driven by a transitional period of transcriptome divergence.