The transcriptome analysis reveals the regulatory mechanisms of female sterility in Lagerstroemia speciosa 'Zichan'.

Background: Ovule abortion presents a major biological obstacle to hybrid breeding in the genus Lagerstroemia, but its molecular regulatory mechanisms remain inadequately understood. This study investigates the female sterility cultivar Lagerstroemia speciosa 'Zichan', providing a comprehensive analysis of the cytological features and molecular regulatory networks underlying female sterility in L. speciosa 'Zichan' for the first time through paraffin section microscopy and transcriptome profiling.

Results: Morphological analyses indicate that female sterility in L. speciosa 'Zichan' results from abnormal embryo sac development. Post the eight-nucleate stage, the embryo sac exhibits disordered fibrous structures, ultimately shrinking and dissolving. During the tetranuclear embryo sac stage, the ovules display irregular fibrous arrangements within the embryo sac and undergo programmed degeneration of the female gametophyte. Transcriptome analysis revealed significant downregulation of the AGL15 gene at the binucleate embryo sac stage, which may affect embryo sac development through the gibberellin metabolic pathway, while abnormal overexpression of the AG1 gene triggers a reproductive inhibition signal. In the auxin signaling pathway, accumulation of AUX/IAA suppresses ARF6 activity, and compensatory activation of ARF7/ARF9 fails to reverse the sterility process. Additionally, retention of DELLA proteins (GAI1) interferes with embryo sac maturation by inhibiting gibberellin-responsive genes. Abnormal overexpression of SPL family genes at the eight-nucleate stage may indirectly affect development by regulating the spatial distribution of auxin.

Conclusions: This study demonstrates that ovule abortion in Lagerstroemia speciosa 'Zichan' results from the combined disruption of cytokinin, gibberellin, and auxin signaling pathways, leading to impaired embryo sac development at the eight-nucleate stage. Significant downregulation of cytokinin signaling components, abnormal accumulation of DELLA proteins due to GID1B dysfunction, and suppressed ARF6 activity collectively interfere with embryo sac maturation. Additionally, misregulation of SPL family and floral organ development genes contributes to sterility. These findings provide new molecular insights into the regulatory network of female sterility in woody plants and establish a foundation for fertility restoration through targeted gene editing or hormone treatments.