Tissue-resolved comparative developmental transcriptomics reveals auxin-associated regulatory shifts underlying divergent fruit tissue origins in pomes and drupes.

Fruit type divergence in closely related species offers a powerful lens into the evolution of plant developmental programs. Within the Rosaceae family, pomes (e.g., apple) and drupes (e.g., peach) share a common ancestry but exhibit a fundamental difference: pomes recruit the hypanthium to form fleshy tissue, while drupes develop flesh solely from the ovary wall. To uncover the regulatory basis of this divergence, we conduct a comparative tissue-resolved developmental transcriptomic analysis across these fruit types. We identify distinct patterns of auxin-related networks, with pomes showing preferential activation of auxin signaling, transport, and biosynthetic pathways within the hypanthium, accompanied by differences in gibberellin responses. Through integrated network analysis, we identify a set of candidate regulators, including MADS-box, YABBY, and AP2 family genes, that interface with auxin signaling in a tissue-specific manner. Furthermore, we delineate a putative regulatory axis in which upstream transcription factors (FIL, ANT, and AP1), potentially modulated by DOF3.2, are differentially associated with the auxin biosynthesis framework (e.g., YUC6) between pomes and drupes. Our findings suggest that fruit type divergence is associated with the spatial redeployment of auxin-related regulatory modules across tissues, providing a molecular framework for understanding fleshy fruit diversification and a basis for future evolutionary-developmental studies.