Within papilionoid legumes, characterized by flowers with strong bilateral symmetry, a derived condition within angiosperms, Cadia (Cadia purpurea) has reverted to radially symmetrical flowers. Here, we investigate the genetic basis of this morphological reversal. Two orthologues of the floral symmetry gene CYCLOIDEA (CYC) demarcate the adaxial (dorsal) region of the flower in typical papilionoid legumes. In the model legume Lotus japonicus, one of these LegCYC genes has been shown, like CYC, to be required for the establishment of floral bilateral symmetry. This study shows that these genes are expressed in the adaxial region of the typical papilionoid flower of Lupinus, which belongs to the same papilionoid subclade as Cadia. In Cadia, these genes also are expressed, but the expression pattern of one of these has expanded from the adaxial to the lateral and abaxial regions of the corolla. This result suggests that the radial flowers of Cadia are dorsalized and, therefore, are not a true evolutionary reversal but an innovative homeotic transformation, where, in this case, all petals have acquired dorsal identity. This study raises a question over other putative reversals in animals and plants, which also may be cryptic innovations.M ost members of the plant family Leguminosae (Fabaceae) have flowers that are characterized by a single axis of symmetry (bilateral symmetry or zygomorphy). The majority of legume species, from the subfamily Papilionoideae and accounting for Ϸ5% of all flowering plant species, are characterized by having typical ''pea'' (papilionoid) flowers with pronounced bilateral symmetry particularly in the corolla (illustrated here by Lupinus nanus; Fig. 1a). The typical papilionoid flower has three distinctive petal types: a single upper (adaxial or dorsal) petal (the ''standard''), two lateral petals (''wings''), and two lower (abaxial or ventral) petals (''keel'' petals). The androecium of typical papilionoids also is bilaterally symmetrical, with stamens of different lengths along the dorsoventral axis, the adaxial stamens being shorter (Fig. 1a). However, within the Papilionoideae, a number of unrelated genera have radially or nearly radially symmetrical flowers. The flowers of these atypical species frequently have been considered primitive (reviewed in ref. 1), but more recent phylogenetic studies suggest that they are derived from a zygomorphic ancestral state (2, 3). An example is Cadia Forsk., a genus of seven species of small shrubs from Arabia, Madagascar, and eastern Africa. Cadia has actinomorphic pendent f lowers in solitary or few-f lowered axillary racemes ( ref. 4; Fig. 1b). These flowers produce abundant nectar but no scent, suggesting these may be pollinated by birds (1). The early development of Cadia (Cadia purpurea) flowers is similar to that of most papilionoid species with zygomorphic flowers where sepals, petals, and stamens are initiated unidirectionally, starting on the abaxial side (6). In typical papilionoid legumes, although organogenesis is asymmetric, a phase of...
No abstract
Numerous TCP genes (transcription factors with a TCP domain) occur in legumes. Genes of this class in Arabidopsis (TCP1) and snapdragon (Antirrhinum majus; CYCLOIDEA) have been shown to be asymmetrically expressed in developing floral primordia, and in snapdragon, they are required for floral zygomorphy (bilaterally symmetrical flowers). These genes are therefore particularly interesting in Leguminosae, a family that is thought to have evolved zygomorphy independently from other zygomorphic angiosperm lineages. Using a phylogenomic approach, we show that homologs of TCP1/CYCLOIDEA occur in legumes and may be divided into two main classes (LEGCYC group I and II), apparently the result of an early duplication, and each class is characterized by a typical amino acid signature in the TCP domain. Furthermore, group I genes in legumes may be divided into two subclasses (LEGCYC IA and IB), apparently the result of a duplication near the base of the papilionoid legumes or below. Most papilionoid legumes investigated have all three genes present (LEGCYC IA, IB, and II), inviting further work to investigate possible functional difference between the three types. However, within these three major gene groups, the precise relationships of the paralogs between species are difficult to determine probably because of a complex history of duplication and loss with lineage sorting or heterotachy (within-site rate variation) due to functional differentiation. The results illustrate both the potential and the difficulties of orthology determination in variable gene families, on which the phylogenomic approach to formulating hypotheses of function depends.
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