Late-acting self-incompatibility in Asimina triloba: implications for the evolution of self-incompatibility in angiosperms

Abstract Background Self-incompatibility (SI) has been reported in many angiosperm species; however, numerous SI systems remain poorly understood, particularly in early-divergent angiosperms where the molecular and genetic regulation of late-acting self-incompatibility (LSI) remains largely unknown. Asimina triloba, a member of the Annonaceae (order Magnoliales), provides a valuable model for investigating LSI in early-divergent flowering plants. Results This study provides the first comprehensive investigation of LSI in A. triloba using macroscopic, histochemical, and transcriptomic approaches. We demonstrate that under auto-incompatible (AI) pollination, fertilization occurs but embryo development is arrested at the first zygotic division, while endosperm develops briefly, resulting in a uniseriate endosperm by 14 days after pollination (DAP). This contrasts with normal embryo development under cross-compatible (CC) pollination, where the embryo resumes division at 18–19 DAP. These postzygotic events ultimately lead to massive fruitlet abscission at 20 DAP following AI pollination. Transcriptomic analyses reveal the first differences in gene expression between early developing seeds from CC and AI pollination as early as 8 DAP, suggesting the initiation of the self-incompatibility response. Conclusion These findings not only support the presence of a functional LSI system in A. triloba but also suggest the conservation of key molecular pathways across distantly related taxa. This work advances our understanding of the evolution and diversification of self-incompatibility mechanisms in early-diverging angiosperms and highlights the adaptive significance of LSI in promoting outcrossing and reproductive success.