Control of corolla monosymmetry in the Brassicaceae Iberis amara

Abstract

Establishment of morphological novelties has contributed to the enormous diversification of floral architecture. One such novelty, flower monosymmetry, is assumed to have evolved several times independently during angiosperm evolution. To date, analysis of monosymmetry regulation has focused on species from taxa where monosymmetry prevails, such as the Lamiales and Fabaceae. In Antirrhinum majus, formation of a monosymmetric corolla is specified by the activity of the TCP transcription factors CYCLOIDEA (CYC) and DICHOTOMA (DICH). It was shown that establishment of monosymmetry likely requires an early asymmetric floral expression of CYC homologs that needs to be maintained until late floral stages. To understand how CYC homologs might have been recruited during evolution to establish monosymmetry, we characterized the likely CYC ortholog IaTCP1 from Iberis amara (Brassicaceae). Species of the genus Iberis form a monosymmetric corolla, whereas the Brassicaceae are otherwise dominated by genera developing a polysymmetric corolla. Instead of four equally sized petals, I. amara produces two small adaxial and two large abaxial petals. The timing of IaTCP1 expression differs from that of its Arabidopsis homolog TCP1 and other CYC homologs. IaTCP1 lacks an asymmetric early expression but displays a very strong differential expression in the corolla at later floral stages, when the strongest unequal petal growth occurs. Analysis of occasionally occurring peloric Iberis flower variants and comparative functional studies of TCP homologs in Arabidopsis demonstrate the importance of an altered temporal IaTCP1 expression within the Brassicaceae to govern the formation of a monosymmetric corolla.floral symmetry ͉ IaTCP1

Evolution of flower shape in Plantago lanceolata

“…In the zygomorphic Brassicaceae species Iberis amara, relative differences in dorsal and ventral petal growth start to become apparent at the onset of stamen differentiation. However, in situ hybridization shows no obvious difference in the level of IaTCP1 expression in dorsal or ventral petal primordia at this stage (Busch and Zachgo 2007). Again, this lack of difference may be a reflection of the limitations of in situ hybridization to detect, or discriminate between, very low levels of gene expression in plant tissues.…”

“…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.…”

“…Constitutive expression of TB1 in wheat has the generalized effect of reducing internode length in transgenic plants, and affects inflorescence architecture by reducing internode length on mature spikes, giving rise to more compact inflorescences than in wild-type plants (Lewis et al 2008). In addition, constitutive expression of IaTCP1 in Arabidopsis resulted in some transgenic plants that were dwarfed in all aspects of their growth (Busch and Zachgo 2007). Thus, the extremely compact architecture of the Plantago inflorescence may be determined by PlCYC activity inhibiting internode and pedicel elongation in the inflorescence.…”

“…These results suggest that expression of CYC-like genes early in stamen development leads to stamen developmental arrest mediated by the inhibition of cell cycle genes. Iberis amara flowers are zygomorphic, and have two small adaxial and two large abaxial petals (Busch and Zachgo 2007). Expression of IaTCP1 is stronger in developing adaxial petals than in abaxial petals, and IaTCP1 expression inhibits adaxial petal growth by negatively regulating cell proliferation (Busch and Zachgo 2007).…”

“…Iberis amara flowers are zygomorphic, and have two small adaxial and two large abaxial petals (Busch and Zachgo 2007). Expression of IaTCP1 is stronger in developing adaxial petals than in abaxial petals, and IaTCP1 expression inhibits adaxial petal growth by negatively regulating cell proliferation (Busch and Zachgo 2007). In Plantago, PlCYC is expressed relatively late in stamen development, after anthers and filaments have formed but before filament elongation, and expression is localised to the connective tissue of anthers and the upper parts of the filaments in all four stamens.…”