Members of the CYCLOIDEA2 (CYC2) clade of the TEOSINTE BRANCHED1, CYCLOIDEA, and PCF transcription factor genes are widely involved in controlling floral zygomorphy, a key innovation in angiosperm evolution, depending on their persistently asymmetric expression in the corresponding floral domains. However, it is unclear how this asymmetric expression is maintained throughout floral development. Selecting Primulina heterotricha as a model, we examined the expression and function of two CYC2 genes, CYC1C and CYC1D. We analyzed the role of their promoters in protein-DNA interactions and transcription activation using electrophoresis mobility shift assays, chromatin immunoprecipitation, and transient gene expression assays. We find that CYC1C and CYC1D positively autoregulate themselves and cross-regulate each other. Our results reveal a double positive autoregulatory feedback loop, evolved for a pair of CYC2 genes to maintain their expression in developing flowers. Further comparative genome analyses, together with the available expression and function data of CYC2 genes in the core eudicots, suggest that this mechanism might have led to the independent origins of floral zygomorphy, which are associated with plant-insect coevolution and the adaptive radiation of angiosperms.
In Asterids, specific expression of CYC‐like genes in the corresponding regions promotes or reduces dorsal petal growth and aborts stamen development. In Rosids, however, the reduced or enlarged dorsal petals are not accompanied by the abortion of stamens, which implies that the function of CYC‐like genes in regulating petal growth and stamen development might be independently recruited. To address this, we investigated the function of the PhCYC1C gene in Primulina heterotricha Y. Dong & Y. Z. Wang on petal growth and stamen development by overexpressing it in two different transformation systems, that is, Arabidopsis belonging to Rosids and tobacco located in Asterids. The results showed that overexpression of PhCYC1C reduced petal sizes in both tobacco and Arabidopsis transgenic plants mainly by repressing cell expansion, indicating its conserved function in determining petal growth between Asterids and Rosids. However, the fertility of both tobacco and Arabidopsis stamens was not affected at all. Given that strong expression signals of PhCYC1C are detected in both tobacco and Arabidopsis stamens and CYC‐like genes actually function to repress stamen development in Lamiales, we suggest that the CYC‐like gene‐associated regulatory network for controlling stamen development might have not established in Rosids as well as in early evolution of Asterids, but evolved as Asterids proceeded further. Our results provide valuable information on the conservation of CYC‐like genes' function in controlling corolla asymmetry and the divergence of their function in determining stamen abortion in angiosperms.
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