Dehiscent fruits in Brassicaceae and Papaveraceae: convergent morpho-anatomical features with divergent underlying genetic mechanisms.

Background and aims: Dry dehiscent fruits have independently evolved multiple times during angiosperm diversification. A striking example is the convergent evolution of Brassicaceae siliques and Papaveraceae pods, both formed by two fused carpels forming valves, that meet at a replum or replum-like structure. In both cases, valve separation occurs through a dehiscence zone at the valve margins in contact with the replum. In Arabidopsis, fruit development is regulated by transcription factors: FRUITFULL (FUL) ensures proper valve cell division, REPLUMLESS (RPL) specifies replum identity, and SHATTERPROOF (SHP1/2) genes pattern the dehiscence zone. SHP1/2 also regulate INDEHISCENT (IND) for lignified layer formation and ALCATRAZ (ALC) and SPATULA (SPT) for the non-lignified layer, with the network antagonized by APETALA2 (AP2), which influences replum formation and valve margin growth.

Methods: Using previously published and new In situ RNA hybridization expression data, we evaluated how this network applies to basal eudicots.

Key results: In Bocconia frutescens, homolog expression suggests conserved roles for FUL and AP2 in fruit wall proliferation, acting antagonistically to ALC and RPL homologs localized to the dehiscence zone. A role for STK homologs in dehiscence zone formation cannot be excluded, while the role of AG-like genes, the closest homologs of SHP during fruit development is unlikely.

Conclusions: Our findings indicate significant rewiring of the fruit developmental network between basal and core eudicots, underscoring the need for functional studies in non-eudicot species to validate this framework.