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

Abstract

Evolution of floral monosymmetry is thought to be a major driving force of angiosperm radiation, making angiosperms the most successful land plant group in terms of species richness. Monosymmetry evolved from a polysymmetric ancestor repeatedly in different angiosperm lineages, where it likely facilitated diversification through the interaction with insects. Most monosymmetric taxa are thus dominated by monosymmetric members. However, in the Brassicaceae, only few members develop a monosymmetric corolla with two petal pairs of unequal size, making them an ideal system to study the evolution of molecular mechanisms enhancing flower complexity. 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.

Evolution of Double Positive Autoregulatory Feedback Loops in CYCLOIDEA2 Clade Genes Is Associated with the Origin of Floral Zygomorphy

“…A dosage effect of CYC2 gene function is also demonstrated in the difference between the dorsal and lateral stamens in both morphology and CYC1 expression in P. heterotricha, which has also been shown in previous studies (Song et al, 2009;Busch et al, 2012).…”

“…Therefore, this neofunctionalization (i.e., the double positive autoregulatory feedback loops underlain by a key regulatory change in CYC2 clade genes) might have been subsequent to the second WGD event in angiosperms that provided novel opportunities for the evolutionary success of the core eudicots. With a possible exception in the family Brassicaceae, it is likely that a single CYC2 gene can function to establish a perfect floral zygomorphy, such as TCP1 in I. amara flowers (Busch and Zachgo, 2007;Busch et al, 2012). It would be interesting to know whether the CYC2 genes in Brassicaceae have employed a single positive autoregulatory loop to maintain their expression with different regulatory and evolutionary mechanisms underlying the diverse forms of floral symmetry, such as dorsal/ventral dosage effect of TCP1-like genes as suggested by Busch et al (2012).…”

“…Therefore, it is important to understand how the maintenance of expression of CYC2 clade genes has been achieved, as co-option of its dorsal-specific location could be functionally sufficient to generate morphological zygomorphy. Furthermore, transient or weak expression of CYC2 clade genes in young floral or floral organ meristems in the ancestral actinomorphic lineages usually has no or very weak morphological effects (Cubas et al, 2001;Zhang et al, 2010;Busch et al, 2012). Therefore, the regulatory changes required to maintain and strengthen CYC2 expression, co-opted along with the regulatory mechanisms that produce dorsal-specific CYC2 expression, may represent a major step in the evolutionary origin of floral zygomorphy.…”

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

“…Flower symmetry is generally assessed via the face-on view of a flower at the time of anthesis, and is usually expressed most strongly in the petal and stamen whorls of the flower. Radially symmetrical flowers (figure 1a) display several planes of symmetry that bisect the flower into mirror images, and bilaterally symmetrical flowers ( figure 1d) [38][39][40][41]. Bilateral flower symmetry itself can range from elaborate to subtle patterns of low complexity (reviewed in [6]).…”

“…In Iberis, the two ventral petals are expanded relative to the two dorsal petals (figure 4). This difference is established late during Iberis flower development, and is associated with relatively late expression of IaTCP1, a CYC homologue, in the smaller dorsal petals (figure 4) [38,39]. Because Iberis is closely related to Arabidopsis, heterologous functional studies of IaTCP1 in Arabidopsis provided meaningful assessment of IaTCP1 function.…”