Integrated transcriptomic and phytohormonal insights across developmental time points to decipher floral sex determination in Zanthoxylum armatum

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• Male flower development in Z. armatum is promoted by auxins and gibberellins, while female flower development is associated with cytokinins and jasmonates inactivation, revealing a hormone-based regulatory switch. • Key transcription factor families—including MADS-box, AP2/ERF, WRKY, and NAC—are differentially expressed between male and female flowers, with MADS-box genes particularly enriched in males and AP2/ERF and WRKY TFs prominent in females, indicating their roles in organ identity. • Alternative splicing events are widespread during floral development, with three genes consistently differentially spliced across all stages—implicated in meiosis, pollen function, and cell cycle regulation—highlighting the role of post-transcriptional regulation in sex differentiation. Floral sex differentiation is a pivotal biological process with implications for species evolution and biodiversity. Zanthoxylum armatum , a economically important pseudo-dioecious species, exhibits remarkable sexual plasticity, including a rare female-to-male sex transition, yet the underlying regulatory mechanisms remain poorly understood. To decipher the mechanisms underlying this phenomenon, we conducted a high-resolution temporal analysis integrating transcriptomics and phytohormone profiling across seven critical floral developmental stages. Our results revealed that sexual fate is governed by a dynamic hormonal antagonism: male flower development is promoted by a surge of bioactive cytokinins (e.g., tZR, cZR) and gibberellins (e.g., GA1, GA9), while female fate is associated with auxin conjugation (e.g., IAA-Asp) and cytokinin inactivation. Concurrent transcriptomic analyses identified key transcription factors—including MADS-box, AP2/ERF, WRKY, and GRF families—that are differentially expressed between sexes and orchestrate organ identity and development. Furthermore, weighted gene co-expression network analysis (WGCNA) linked specific hormonal signatures to distinct genetic modules, and alternative splicing analysis uncovered post-transcriptional regulation of genes critical for meiosis and pollen function. Additionally, alternative splicing analysis uncovered a complex network of splicing events that contribute to the regulation of gene expression during flower development. This study provides a comprehensive regulatory framework for floral sex determination in Z. armatum, highlighting the intricate interplay between phytohormones and transcriptional networks. Our findings offer foundational insights into the mechanisms of sex determination in plants and pave the way for manipulating sexual expression to enhance yield stability in horticultural crops.

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