Abstract
The Dasymaschalon alliance within the early divergent angiosperm family Annonaceae comprises c. 180 species in four genera (Dasymaschalon, Desmos, Friesodielsia, and Monanthotaxis). The alliance offers an excellent opportunity for investigating perianth evolution and functional adaptations because of the presence of different numbers of petal whorls and contrasting floral chamber morphologies. The absence of the inner petal whorl in Dasymaschalon renders it distinctive in the family: previous studies have suggested that its three outermost stamens might be homologous with the inner petals of the sister genus, Friesodielsia, reflecting a homeotic shift of floral organ identify from inner petals to stamens. To investigate this hypothesis and general perianth evolution in the alliance, we (i) compared the floral vascularization of selected Dasymaschalon and Friesodielsia species using paraffin serial sectioning, and (ii) mapped selected perianth characters of inferred functional significance onto a molecular phylogenetic framework of the Dasymaschalon alliance (46 accessions; five cpDNA, and two nrDNA markers). The results indicate that the vasculature of the outermost stamen whorl of Dasymaschalon does not fuse with the perianth cortical vascular system, but instead splits from the basal traces of the free stamen bundles, contradicting previous inferences of homology with the inner corolla whorl of other Annonaceae. The loss of the inner petal whorl in Dasymaschalon is less likely to be due to a homeotic mutation, and instead possibly involved either the loss of genes that are responsible for determining inner petals or else the expression failure of these genes. Optimizations of perianth characters indicate that the absence of the inner petal whorl and the connivence of outer petals during anthesis are synapomorphic for Dasymaschalon. Circadian trapping of pollinators is inferred either to be derived in the stem lineage of the Dasymaschalon–Friesodielsia clade, or else to have evolved in parallel in the Dasymaschalon and Friesodielsia lineages. Subsequent changes in the remaining petals of Dasymaschalon flowers (which do not fully separate during anthesis) are likely to have enabled perpetuation of the circadian trapping mechanism, lessening the adverse impacts of inner petal loss.
Highlights
Friesodielsia desmoides possesses a vascular anatomy that is typical of the Annonaceae, comprising a perianth cortical vascular system (CVS, sensu Deroin, 1989, 1999) with three whorls of vascular traces
The floral vascular anatomy of D. trichophorum is similar to that of F. desmoides: the cortical stele in the pedicel (Figure 3A) diverges to form six clusters of vascular bundles (b1–6 in Figure 3B); the vasculature of the first perianth whorl consists of three clusters of vascular bundles, each leading to one median and two lateral traces (Figures 3D–G)
The vascular traces leading to various perianth organs are intimately connected, collectively forming a perianth cortical vascular system (CVS) that correspond to the outer and middle whorls widely reported in most other Annonaceae flowers (Deroin, 1989, 1999; Deroin and Le Thomas, 1989; Xue and Saunders, 2013)
Summary
F. & Thomson) Dalla Torre & Harms, Desmos Lour., Friesodielsia Steenis and Monanthotaxis Baill. The genera Desmos, Friesodielsia and Monanthotaxis are largely uniform in their underlying floral ‘Bauplan’ and are similar to most other Annonaceae species: the flowers are trimerous with a whorl of sepals and two morphologically distinct whorls of petals. Unlike most species of the alliance and the family as a whole, the flowers of Dasymaschalon only have one whorl of three petals (Figure 1D), which are regarded as homologous with outer petals of the other three genera in the alliance due to their alternating position relative to the sepals (Saunders, 2010; Wang et al, 2012). Obvious differences that can distinguish Dasymaschalon from its close relatives Desmos and Friesodielsia are observed in the number of stamens in the outermost whorl: Desmos and Friesodielsia flowers have six outer stamens located directly in front of the inner or outer petals (Figure 1E), whereas Dasymaschalon flowers only have three outer stamens located at the corners of the triangular floral meristem (Figure 1F)
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