Duplication and expression patterns of CYCLOIDEA-like genes in Campanulaceae

Abstract

AbstractBackgroundCYCLOIDEA (CYC)-like transcription factors pattern floral symmetry in most angiosperms. In core eudicots, two duplications led to three clades ofCYC-like genes:CYC1,CYC2,andCYC3, with orthologs of theCYC2clade restricting expression dorsally in bilaterally symmetrical flowers. Limited data fromCYC3suggest that they also play a role in flower symmetry in some asterids. We examine the evolution of these genes in Campanulaceae, a group that contains broad transitions between radial and bilateral floral symmetry and 180° resupination (turning upside-down by twisting pedicle).ResultsWe identify here all three paralogousCYC-likeclades across Campanulaceae. Similar to other core eudicots, we show thatCamCYC2duplicated near the time of the divergence of the bilaterally symmetrical and resupinate Lobelioideae. However, in non-resupinate, bilaterally symmetrical Cyphioideae,CamCYC2appears to have been lost andCamCYC3duplicated, suggesting a novel genetic basis for bilateral symmetry in Cyphioideae. We additionally, utilized qRT-PCR to examine the correlation betweenCYC-like gene expression and shifts in flower morphology in four species of Lobelioideae. As expected,CamCYC2gene expression was dorsoventrally restricted in bilateral symmetrical flowers. However, because Lobelioideae have resupinate flowers, bothCamCYC2AandCamCYC2Bare highly expressed in the finally positioned ventral petal lobes, corresponding to the adaxial side of the flower relative to meristem orientation.ConclusionsOur sequences across Campanulaceae of all three of these paralogous groups suggests that radially symmetrical Campanuloideae duplicatedCYC1, Lobelioideae duplicatedCYC2and lostCYC3early in their divergence, and that Cyphioideae lostCYC2and duplicatedCYC3. This suggests a dynamic pattern of duplication and loss of major floral patterning genes in this group and highlights the first case of a loss ofCYC2in a bilaterally symmetrical group. We illustrate here thatCYCexpression is conserved along the dorsoventral axis of the flower even as it turns upside-down, suggesting that at least lateCYCexpression is not regulated by extrinsic factors such as gravity. We additionally show that while the pattern of dorsoventral expression of each paralog remains the same,CamCYC2Ais more dominant in species with shorter relative finally positioned dorsal lobes, andCamCYC2Bis more dominant in species with long dorsal lobes.