Anatomical and genetic bases underlying convergent evolution of fleshy and dry dehiscent fruits in Cestrum and Brugmansia (Solanaceae)

Background: The mechanisms controlling evolutionary shifts between dry and fleshy fruits in angiosperms are poorly understood. In Solanaceae, Cestrum and Brugmansia represent cases of convergent evolution of fleshy and dry fruits, respectively. Here we study the anatomical and genetic bases of the independent origin of fleshy fruits in Cestrum and the reversion to dry dehiscent fruits in Brugmansia. We also characterize the expression of candidate fruit development genes, including ALCATRAZ/SPATULA, FRUITFULL, HECATE1/2/3, REPLUMLESS and SHATTERPROOF.

Methods: We identify anatomical changes to establish developmental stages in the ovary-to-fruit transition in Cestrum nocturnum and Brugmansia suaveolens. We generate reference transcriptomes for both species, isolate homologs for all genes in the fruit genetic regulatory network (GRN) and perform gene expression analyses for ALC/SPT, FUL, HEC1/2/3, RPL and SHP throughout fruit development. Finally, we compare our results to expression patterns found in typical capsules of Nicotiana tabacum and berries of Solanum lycopersicum available in public repositories.

Results: We have identified homologous, homoplasious and unique anatomical features in C.nocturnum and B. suaveolens fruits, resulting in their final appearance. Expression patterns suggest that FUL, SHP and SPT might control homologous characteristics, while ALC and RPL likely contribute to homoplasious anatomical features.

Conclusions: The convergent anatomical features in Cestrum and Brugmansia fruits are likely the result of changes in ALC and RPL expression patterns. The fruit GRN changes considerably in these genera when compared to typical capsules and berries of Solanaceae, particularly in B. suaveolens, where expression of FUL2 and RPL1 is lacking.