Beyond dry and fleshy: Hidden developmental and anatomical transitions in Solanaceae fruit evolution

Classifying fruits based solely on mature morphology can obscure underlying developmental and anatomical diversity. Current fruit types described in Solanaceae inadequately capture the complexity of fruit evolution within the family.

We compared the anatomy of different fruit developmental stages across representative Solanaceae lineages encompassing dry, fleshy, and intermediate fruit types. We also optimized fruit types, cell division patterns, endocarp lignification, and mesocarp expansion in a recent Solanaceae phylogenetic framework to reconstruct evolutionary changes.

Early pericarp organization and tissue patterning were found to be largely conserved across lineages of Solanaceae, regardless of the mature fruit type. Divergence among fruit types arose primarily from lineage-specific modifications in endocarp lignification, mesocarp expansion, and lacunae formation, which together determine fruit patterning. We identified fruits with intermediate anatomical features in Lycianthes, Lycium, and Nolana, that are characterized by discontinuous endocarp lignification or sclerosomes and mesocarp expansion. We identified contrasting anatomical bases for fruit dehiscence: Lineages outside Solanoideae rely on a continuously lignified endocarp, whereas members of Solanoideae have independent dehiscence mechanisms based on tissue tensions without endocarp lignification.

Solanaceae fruit diversity emerged through modifications of conserved developmental programs and independent evolution of novel anatomical mechanisms. The anatomical patterns and character optimizations support our interpretation that sclerosomes represent remnants of a formerly continuous lignified endocarp, indicating that fleshy fruit in the family may have evolved through developmental programs repressing lignification. Our findings highlight the importance of integrating anatomical and ontogenetic perspectives to better understand fruit evolution in the family.