Elucidating the origin of flowers has been a challenge in botany for a long time. One of the central questions surrounding the origin of flowers is how to interpret the carpel, especially the relationship between the phyllome part (carpel wall) and the ovule. Recently, consensus favors the carpel originating from the fusion of an ovule-bearing part and the phyllome part that subtends it. Considering the carpel is a complex organ, the accurate presentation of the anatomical structure of the carpel is necessary for resolving this question. Anaxagorea is the most basal genus in a primitive angiosperm family, Annonaceae. The conspicuous stipe at the base of each carpel makes it an ideal material for exploring the histological relationships among the receptacle, the carpel, and the ovule. In the present study, floral organogenesis and vasculature were delineated in Anaxagorea luzonensis and Anaxagorea javanica, and a three-dimensional model of the carpel vasculature was reconstructed based on serial sections. The results show that in Anaxagorea, the vasculature in the carpel branches in the form of shoots. The radiosymmetrical vasculature pattern is repeatedly presented in the receptacle, the carpel, and the funiculus of the ovule. This provides anatomical evidence of the composite origin of the carpel.

AbstractThe carpel is the definitive structure of angiosperms and the origin of the carpel is of great significance to the phylogenetic origin of angiosperms. The traditional view has been that angiosperm carpels emerged from structures similar to macrosporophylls of pteridosperms or Bennettitales, which bear ovules on the surface of foliar organs. Conversely, according to other perspectives, carpels originated from foliar appendages enclosing the ovule-bearing axis. One of the key distinctions between the two conflicting views lies in whether the ovular axis is involved in the evolution of the carpel. The aim of the present study was to investigate whether the axial homologs remain in the carpel of extant angiosperms, and, in turn, reveal the integrated axial-foliar nature of carpel. Two Anaxagorea species were used for organogenesis and comparative anatomical studies owing to their outstanding and unusually long carpel stipes. The continuous change of vascular bundles at the carpel stipe at different developmental stages is described here in detail. Organogenesis revealed that the carpel stipe of Anaxagorea emerges at the early stage of carpel development. Vascular bundles at the base of Anaxagorea carpel are a set of discrete ring-arranged collateral bundles that branch out at the upper portion into two sets of ring-arranged collateral bundles below each ovule. The ring-arranged collateral bundles are clear morphological evidence of the existence of axial homologs in the carpel, and, therefore, support the perspective that carpels originated from the integration of the ovular axis and foliar parts. This finding could prompt the reconsideration of how the bract-bracteole-terminal ovule system in gymnosperms evolved into an angiosperm carpel.