Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots

Abstract

Background: The aim of this paper is to discuss the controversial origins of petals from tepals or stamens and the links between the morphological expression of petals and floral organ identity genes in the core eudicots.

Scope: I challenge the widely held classical view that petals are morphologically derived from stamens in the core eudicots, and sepals from tepals or bracts. Morphological data suggest that tepal-derived petals have evolved independently in the major lineages of the core eudicots (i.e. asterids, Santalales and rosids) from Berberidopsis-like prototypes, and that staminodial petals have arisen only in few isolated cases where petals had been previously lost (Caryophyllales, Rosales). The clear correlation between continuous changes in petal morphology, and a scenario that indicates numerous duplications to have taken place in genes controlling floral organ development, can only be fully understood within a phylogenetic context. B-gene expression plays a fundamental role in the evolution of the petals by controlling petaloidy, but it does not clarify petal homology.

Conclusions: An increased synorganization of the flower in the core eudicots linked with the establishment of floral whorls restricts the petaloid gene expression to the second whorl, reducing the similarities of petals with tepals from which they were originally derived. An increased flower size linked with secondary polyandry or polycarpelly may lead to a breakdown of the restricted gene expression and a reversal to ancestral characteristics of perianth development. An altered 'sliding boundary' hypothesis is proposed for the core eudicots to explain shifts in petaloidy of the perianth and the event of staminodial petals. The repetitive changes of function in the perianth of the core eudicots are linked with shifts in petaloidy to the outer perianth whorl, or losses of petal or sepal whorls that can be secondarily compensated for by the inclusion of bracts in the flower. The origin and evolution of petals appears to be as complex on a molecular basis as it is from a morphological point of view.

Fig. 1.

Illustration of the phylogenetic relationship of the major clades of eudicots, based on APG (2003). (A) Reconstruction of perianth differentiation in the basal eudicot grade and Gunnerales, in contrast to the supposedly staminodial petals of the core eudicots. (B) Reconstruction of petal homologies in the eudicots. The distribution of characters has been mapped for the major lineages of the core eudicots, indicating cases where petals have a staminodial or a bract-derived origin.

Fig. 2.

(A,B) Stages of the floral development of Berberidopsis corallina (Berberidopsidaceae). (A) Early stage of perianth initiation showing two pentamerous whorls of tepals arising in a spiral sequence. The arrow points to the sixth tepal initiating a second ‘whorl’. (B) Later stage of development of the flower at gynoecium development. The outer tepals have been removed. Numbers show the sequence of the 12 tepals; c, carpel; st, stamen. (C,D) Stages of the floral development of Cochlospermum vitifolium (Bixaceae – rosids). (C) Young inflorescence with three flowers at different stages of development. Numbers show the sequence of initiation of the sepals on individual flowers and first petal (arrow in front flower); br, bracteole. (D) Older bud at the initiation of the carpels (sepals removed); c, carpel primordium. (E) Section through young flower of Potentilla sp. (Rosaceae). Initiation of three primordia on a common primordium; the uppermost primordium develops as a petal and the lower as stamens. S, sepal. (F) Young flower primordium of Corbichonia decumbens (Lophiocarpaceae). The outer members of a centrifugal androecium develop into petaloid staminodes (arrow). St, stamen; c, carpel. Scale bars = 100 µm.

Fig. 3.

Floral diagrams demonstrating the putative sequence for the origin of petals in the core eudicots. (A) Prototype such as Berberidopsis with a spiral perianth of 12 tepals. (B) Core eudicot flower with a bipartite perianth of five broad sepals and five petals arising in a spiral sequence. (C) Core eudicot flower with five sequentially arising sepals and five petals arising simultaneously (in grey).

Fig. 4.

Altered ‘sliding-boundary’ hypothesis for the core eudicots. (A) ABC model for flowers with well-differentiated sepals and petals; (B) flowers with petaloid calyx next to a corolla; (C) flowers with staminodial petals, either by an ectopic expression of C genes linked with different B-genes, or by a restriction of the C-gene activity.

Fig. 5.

Floral models showing different levels of perianth evolution in the core eudicots; phyllomes from bottom to top represent bracts, sepals and petals; black colour represents absence of petaloidy; white colour represents petaloidy; broken curves represent lost whorls. For each model the putative ABC-model is shown. (A) Flower with well-differentiated biseriate perianth; (B) reduction or loss of petals and petaloidy of the sepal whorl; (C) secondary insertion of bracts in an apetalous flower; (D) reduction or loss of sepals; (E) secondary insertion of bracts in an asepalous flower; (F) development of staminodial petals after the initial loss of petals.