Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome

Abstract

Angiosperms exhibit staggering diversity in floral form, and evolution of floral morphology is often correlated with changes in pollination syndrome. The showy, bilaterally symmetrical flowers of the model species Antirrhinum majus (Plantaginaceae) are highly specialized for bee pollination. In A. majus, CYCLOIDEA (CYC), DICHOTOMA (DICH), RADIALIS (RAD), and DIVARICATA (DIV) specify the development of floral bilateral symmetry. However, it is unclear to what extent evolution of these genes has resulted in flower morphological divergence among closely related members of Plantaginaceae differing in pollination syndrome. We compared floral symmetry genes from insect-pollinated Digitalis purpurea, which has bilaterally symmetrical flowers, with those from closely related Aragoa abietina and wind-pollinated Plantago major, both of which have radially symmetrical flowers. We demonstrate that Plantago, but not Aragoa, species have lost a dorsally expressed CYC-like gene and downstream targets RAD and DIV. Furthermore, the single P. major CYC-like gene is expressed across all regions of the flower, similar to expression of its ortholog in closely related Veronica serpyllifolia. We propose that changes in the expression of duplicated CYC-like genes led to the evolution of radial flower symmetry in Aragoa/Plantago, and that further disintegration of the symmetry gene pathway resulted in the wind-pollination syndrome of Plantago. This model underscores the potential importance of gene loss in the evolution of ecologically important traits.

Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances

“…In Plantago, Tengia, Cadia and Microsteria, one CYC-like paralogue (or set of closely related paralogues in the case of Tengia) is expressed across the dorsoventral flower axis, owing to regulatory evolution either at or upstream of that paralogue. The other CYC-like paralogue has been lost (Plantago and Microsteria), or is no longer expressed in flowers (Cadia and Tengia) [80][81][82][83]. Alternatively, both CYC-like paralogues are expressed across the dorsoventral flower axis (Psychopterys), or neither is expressed in flowers (Sphedamnocarpus) [82].…”

“…Examples of derived radial symmetry (from CYC-dependent bilateral symmetry) for which the expression of CYC homologues has been studied include Plantago (Plantaginaceae, Lamiales), Cadia (Fabaceae, Fabales), two independent transitions to radial from bilateral symmetry in Gesneriaceae (Lamiales)-Bournea and Tengia, and four independent transitions to radial from bilateral symmetry in Malpighiaceae (Malpighiales)-Psychopterys, Sphedamnocarpus, Microsteria and Lasiiocarpus (figure 4) [62,[80][81][82][83]. For each of these, two or more paralogous CYC-like genes are dorsally expressed in close relatives.…”

Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors

“…Conversely, a different actinomorphic Gesneriaceae, Bournea leiophylla , exhibits rapid down-regulation of CYC2 expression at later developmental stages (Zhou et al, 2008), suggesting loss-of-function. Similarly, the actinomorphic flowers of Plantago , a member of the Plantaginaceae, are associated with degeneration of both the CYC -based dorsal identity and MYB-based ventral identity programs, although one CYC2 homolog is still broadly expressed (Preston et al, 2011). …”

Function of theCYC-Like Genes During Floral Development in Soybean

“…Flower symmetry is of special interest in understanding angiosperm evolution (16). As flower bilateral symmetry is drawing more and more attention in different species, CYClike genes have been shown to be involved in the development of zygomorphy in different species (22,27,28). in legumes, numerous CYC-like genes have been isolated and found to have undergone repeated duplication events, implying that they might have divergent functions (1,11,12).…”