Diversity and Evolution of CYCLOIDEA-Like TCP Genes in Relation to Flower Development in Papaveraceae

Abstract

Monosymmetry evolved several times independently during flower evolution. In snapdragon (Antirrhinum majus), a key gene for monosymmetry is CYCLOIDEA (CYC), which belongs to the class II TCP gene family encoding transcriptional activators. We address the questions of the evolutionary history of this gene family and of possible recruitment of genes homologous to CYC in floral development and symmetry in the Papaveraceae. Two to three members of the class II TCP family were found in each species analyzed, two of which were CYC-like genes, on the basis of the presence of both the TCP and R conserved domains. The duplication that gave rise to these two paralogous lineages (named PAPACYL1 and PAPACYL2) probably predates the divergence of the two main clades within the Papaveraceae. Phylogenetic relationships among angiosperm class II TCP genes indicated that (1) PAPACYL genes were closest to Arabidopsis (Arabidopsis thaliana) AtTCP18, and a duplication at the base of the core eudicot would have given rise to two supplementary CYC-like lineages; and (2) at least three class II TCP genes were present in the ancestor of monocots and eudicots. Semiquantitative reverse transcription-polymerase chain reaction and in situ hybridization approaches in three species with different floral symmetry indicated that both PAPACYL paralogs were expressed during floral development. A pattern common to all three species was observed at organ junctions in inflorescences and flowers. Expression in the outer petals was specifically observed in the two species with nonactinomorphic flowers. Hypotheses concerning the ancestral pattern of expression and function of CYC-like genes and their possible role in floral development of Papaveraceae species leading to bisymmetric buds are discussed.

Expression differentiation of CYC-like floral symmetry genes correlated with their protein sequence divergence in Chirita heterotricha (Gesneriaceae)

“…A recent study in legumes, distantly related to A. majus, shows that a CYC homologue LjCYC2 also establishes adaxial identity in the legume flowers (Feng et al 2006). In the basal eudicot family Papaveraceae sensu lato, the duplication and diversification of CYC-like TCP genes are accompanied by their divergence in expression patterns, in which one type of them may play a role in flower symmetry (Kölsch and Gleissberg 2006;Damerval et al 2007). These facts indicate that the basic function of CYC and its homologues seems to be conserved in eudicots, i.e., controlling the development of floral asymmetry.…”

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

“…The plane of bilateral symmetry in Fumariodeae flowers is transverse (figure 4), although partial resupination ultimately brings the transverse plane into dorsoventral orientation. In Capnoides, expression of two CYC-lineage paralogues [40,41] is asymmetric, with slightly stronger expression at the base of the outer petal that forms a nectary [76].…”

“…And again, we find evidence supporting a role for CYC-like genes in the development of bilaterally symmetrical flowers from early diverging eudicot and monocot lineages. Bilaterally symmetrical flowers of Capnoides in the Fumariodeae lineage of Papaveraceae (Ranunculales) are derived from disymmetric flowers [40,41]. The plane of bilateral symmetry in Fumariodeae flowers is transverse (figure 4), although partial resupination ultimately brings the transverse plane into dorsoventral orientation.…”

“…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]).…”

The Cotton Transcription Factor TCP14 Functions in Auxin-Mediated Epidermal Cell Differentiation and Elongation

“…In particular, great progress has been made in functional characterization of the class II TCPs in Arabidopsis. These transcription factors play important roles in leaf, flower, shoot morphogenesis, and hormone biosynthesis (Damerval et al, 2007;Koyama et al, 2007;Schommer et al, 2008;Nag et al, 2009;Guo et al, 2010). The cellular functions of class I TCPs are less well explored, but several previous studies indicated that they are involved in a number of cellular or developmental processes.…”