Corolla Monosymmetry: Evolution of a Morphological Novelty in the Brassicaceae Family

Abstract

Monosymmetry is controlled by the TCP transcription factors that belong to the CYC2 clade in distantly related taxa. In Iberis amara, the first crucifer analyzed in terms of monosymmetry development, unequal corolla formation is due to a stronger CYC2 clade gene expression in the smaller adaxial petals compared with the larger abaxial ones. Phylogenetic reconstruction of the crucifer family reveals that the monosymmetric genera Iberis, Calepina, and Teesdalia belong to one major crucifer lineage. Monosymmetry is most pronounced in Iberis and less so in Calepina and Teesdalia, with a positive dosage-dependent correlation between the strength of a CYC2 expression difference and the extent of monosymmetry formation. An early adaxial CYC2 expression in floral meristems, observed in many distantly related taxa, might have facilitated the repeated evolution of CYC2-controlled monosymmetry. Comparison of early and late CYC2 expression in monosymmetric and polysymmetric crucifers representative for the four major crucifer lineages reveals that an adaxial CYC2 expression in floral meristems is likely ancestral for the Brassicaceae. However, it got lost in all analyzed monosymmetric members and is, as such, not a prerequisite for the establishment of corolla monosymmetry in crucifers. Here, monosymmetry evolved via a heterochronic CYC2 expression shift from an ancestral early adaxial expression in floral meristems to an adaxial CYC2 transcript accumulation later in petal development. This study emphasizes the potential of regulatory changes in the evolution of morphological novelties, like corolla monosymmetry in the Brassicaceae. In combination with a corymboid inflorescence, monosymmetry might have served as a key invention driving diversification in the genus Iberis comprising more than 20 monosymmetric species.