Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum

Abstract

To understand how genes control floral asymmetry, we have isolated and analyzed the role of the RADIALIS (RAD) gene in Antirrhinum. We show that the RAD gene encodes a small MYB-like protein that is specifically expressed in the dorsal region of developing flowers. RAD has a single MYB-like domain that is closely related to one of the two MYB-like domains of DIV, a protein that has an antagonistic effect to RAD on floral development. Interactions between RAD and other genes indicate that floral asymmetry depends on the interplay between two pairs of transcription factors. First, a pair of TCP proteins is expressed in dorsal regions of the floral meristem, leading to the activation of RAD in the dorsal domain. The RAD MYB-like protein then antagonizes the related DIV MYB-like protein, preventing DIV activity in dorsal regions. In addition to its role in dorsal regions, RAD acts nonautonomously on lateral regions either directly, through RAD protein movement, or indirectly, through a signaling molecule.F loral asymmetry is thought to have evolved many times independently as a specialized mechanism for pollinator interaction (1-3). In a few cases, most notably in Antirrhinum majus, the molecular genetic basis of floral asymmetry has begun to be understood. Four key genes have been shown to control dorsoventral asymmetry in Antirrhinum: CYCLOIDEA (CYC), DICHOTOMA (DICH), RADIALIS (RAD), and DIVARICATA (DIV) (4-8). Two of these genes, CYC and DICH, promote dorsal identity and encode proteins belonging to the TCP family of transcription factors. DIV promotes ventral identity and encodes a protein belonging to the MYB family of transcription factors, carrying two MYB-like domains. However, the mechanism by which CYC, DICH, and DIV interact remains unclear. To address this question, we have isolated and characterized RAD, the fourth member of this group of genes, and explored how it acts in combination with the other genes to establish floral asymmetry.Flowers of wild-type Antirrhinum are zygomorphic, having a single plane of symmetry (bilateral symmetry), in contrast to actinomorphic flowers, which have multiple planes of symmetry (radial symmetry) (3). The zygomorphy of Antirrhinum flowers reflects morphological distinctions between the upper (dorsal) and lower (lateral and ventral) organs of whorls two and three. In whorl two, each flower has two dorsal petals, two lateral petals, and one ventral petal, whereas whorl three comprises a single arrested dorsal stamen (staminode), two lateral stamens, and two ventral stamens (Fig. 1 a and b).The CYC and DICH genes are required for dorsoventral asymmetry in Antirrhinum and are expressed from an early stage in the dorsal domain of the floral meristem (5, 7, 9). At later stages, CYC expression persists throughout most of the dorsal domain, whereas DICH becomes restricted to the most dorsal half of the dorsal domain. Inactivation of both CYC and DICH results in peloric (radially symmetrical) flowers, in which all petals have ventral identity (Fig. 1h). In cyc or dich single ...

Evolution of flower shape in Plantago lanceolata

“…We found no evidence for positive Darwinian selection in the PlCYC protein-coding region, as might be expected if the protein had acquired a novel function. Thus, the TCP transcription factor encoded by PlCYC most likely functions like other related CYC-like transcription factors to regulate plant cell proliferation and growth (Gaudin et al 2000;Corley et al 2005;Busch and Zachgo 2007). In Plantago, it is equally plausible that CYC-like gene function was lost in dorsal floral regions because of a gene loss event or a gene regulatory event.…”

“…Flowers can be classified as zygomorphic (having only one plane of reflectional symmetry or bilaterally symmetric), actinomorphic (having multiple planes of symmetry or radially symmetric) or asymmetric (having no plane of symmetry) (Endress 2001). The gene regulatory network that determines zygomorphy is best understood in the model plant Antirrhinum majus (Corley et al 2005). In Antirrhinum zygomorphy is evident primarily in the distinct shape of the dorsal, lateral and ventral petals of the flower (Fig.…”

“…In Antirrhinum zygomorphy is evident primarily in the distinct shape of the dorsal, lateral and ventral petals of the flower (Fig. 1a, Corley et al 2005). Two genes, CYCLOIDEA (CYC) and DICHOTOMA (DICH), play a key role in promoting dorsal identity in Antirrhinum (Luo et al 1996(Luo et al , 1999.…”

Control of corolla monosymmetry in the Brassicaceae Iberis amara

“…The MYB-like transcription factors RADIALIS (RAD; ref. 16) and DIVARICATA (DIV; refs. 17 and 18) participate in symmetry regulation.…”

“…RAD is a target gene of CYC (19), and rad mutants, similar to cyc mutants, form partially abaxialized flowers (10). RAD acts antagonistically to DIV (16), a factor promoting abaxial petal identity.…”