The development of the embryo and ruminate endosperm in an early-divergent angiosperm, Asimina triloba (Annonaceae).

Background and aims: Embryo and seed development are essential for the reproductive success of flowering plants. However, these processes remain underexplored in the Annonaceae family that belongs to the early-divergent angiosperm clade Magnoliid, and are characterized by the distinctive feature of ruminations in the seeds. To fill this knowledge gap, we conducted a study to characterize the embryogeny and seed development of Asimina triloba ("pawpaw"), the northernmost species of the mainly tropical family Annonaceae.

Methods: We performed a comprehensive histological examination of embryogeny in A. triloba, from fertilization to the emergence of the embryo from the seed, paying special attention to the formation of the ruminations in the endosperm.

Key results: After a rapid fertilization process, the embryo develops slowly, which may support initial embryo development. Concomitant with this early embryogenesis, a ruminate nucellus develops as the main and primary storage tissue, which is later gradually replaced by the endosperm while still maintaining the ruminations. Finally, in the mature seed, the ruminate endosperm is consumed by the small and relatively underdeveloped embryo, which requires additional growth and development prior to germination.

Conclusions: Our study provides a comprehensive overview of the stages from fertilization and early embryogenesis to seed germination of A. triloba. The results reveal both ancestral features, such as a slow embryogenesis and an underdeveloped embryo in the mature seed, and derived features, such as the presence of a ruminate endosperm, which is commonly found in the Annonaceae family. This combination of traits is also observed in other angiosperm families, suggesting a convergent evolutionary solution with adaptive significance, where ruminate endosperm may evolve in response to specific environmental conditions. These findings contribute to a better understanding of both the diversity of embryological characters and their evolutionary significance across early-divergent and more derived angiosperm lineages.