Is a Ring-arranged Vascular Pattern Unique to Stems? A Three Dimensional Reconstruction ofAnaxagorea(Annonaceae) Carpel Vasculature and its Evolutionary Implications

Abstract

<jats:title>Abstract</jats:title><jats:p>The 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 <jats:italic>Anaxagorea</jats:italic> 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 <jats:italic>Anaxagorea</jats:italic> emerges at the early stage of carpel development. Vascular bundles at the base of <jats:italic>Anaxagorea</jats:italic> 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.</jats:p>

Molecular Control of Carpel Development in the Grass Family

“… Baum and Hileman (2007) proposed a central role of gene LEAFY ( LFY ) in the origin of the flower, which regulates C-function MADS-box genes in the flowering plants ancestor; these C-class genes then would have specified apical female reproductive structure, which later became carpels ( Vialette-Guiraud and Scutt, 2009 ; Ferrándiz et al, 2010 ). Recently, the carpel of Anaxagorea , the most basal genus of primitive angiosperms Annonaceae (Magnoliales), is studied ( Li et al, 2020 ). Supports are provided in this study for another carpel origin theory called the stachyosporous theory, which suggests that carpel originated from a compound shoot of the ovular axis and foliar appendage ( Hickey and Taylor, 1996 ; Li et al, 2020 ).…”

“…Recently, the carpel of Anaxagorea , the most basal genus of primitive angiosperms Annonaceae (Magnoliales), is studied ( Li et al, 2020 ). Supports are provided in this study for another carpel origin theory called the stachyosporous theory, which suggests that carpel originated from a compound shoot of the ovular axis and foliar appendage ( Hickey and Taylor, 1996 ; Li et al, 2020 ). Besides these theories, a basic ancestral angiosperm carpel developmental networks has been proposed ( Becker, 2020 ), involving STYLISH ( STY )-, SPATULA ( SPT )-, ETTIN ( ETT )-, and CRABS CLAW ( CRC )-like genes in basal/apical and adaxial/abaxial polarity specification and growth, and HECATE ( HEC ) homologs regulating only longitudinal growth.…”