Gene duplication and relaxation from selective constraints of GCYC genes correlated with various floral symmetry patterns in Asiatic Gesneriaceae tribe Trichosporeae

Abstract

Floral bilateral symmetry is one of the most important acquisitions in flower shape evolution in angiosperms. Members of Gesneriaceae possess predominantly zygomorphic flowers yet natural reversal to actinomorphy have independently evolved multiple times. The development of floral bilateral symmetry relies greatly on the gene CYCLOIDEA (CYC). Our reconstructed GCYC phylogeny indicated at least five GCYC duplication events occurred over the evolutionary history of Gesneriaceae. However, the patterns of GCYC expression following the duplications and the role of natural selection on GCYC copies in relation to floral symmetry remained largely unstudied. The Asiatic tribe Trichosporeae contains most reversals to actinomorphy. We thus investigated shifts in GCYC gene expression among selected zygomorphic species (Hemiboea bicornuta and Lysionotus pauciflorus) and species with reversals to actinomorphy (Conandron ramondioides) by RT-PCR. In the actinomorphic C. ramondioides, none of the three copies of GCYC was found expressed in petals implying that the reversal was a loss-of-function event. On the other hand, both zygomorphic species retained one GCYC1 copy that was expressed in the dorsal petals but each species utilized a different copy (GCYC1C for H. bicornuta and GCYC1D for L. pauciflorus). Together with previously published data, it appeared that GCYC1C and GCYC1D copies diversified their expression in a distinct species-specific pattern. To detect whether the selection signal (ω) changed before and after the duplication of GCYC1 in Asiatic Trichosporeae, we reconstructed a GCYC phylogeny using maximum likelihood and Bayesian inference algorithms and examined selection signals using PAML. The PAML analysis detected relaxation from selection right after the GCYC1 duplication (ωpre-duplication = 0.2819, ωpost-duplication = 0.3985) among Asiatic Trichosporeae species. We propose that the selection relaxation after the GCYC1 duplication created an "evolutionary window of flexibility" in which multiple copies were retained with randomly diverged roles for dorsal-specific expressions in association with floral symmetry changes.

Gene Duplication and Differential Expression of Flower Symmetry Genes in Rhododendron (Ericaceae)

“…This differential expression pattern likely contributed to the dorsal petal being the longest in R. beyerinckianum (Figure 5). Besides Antirrhinum, similar patterns have been observed in other bilaterally symmetric species in asterids, where one CYC ortholog is more dorsally restricted than the other(s) [31,[60][61][62][63][64][65]. Therefore, in Rhododendron, we see conserved patterns of differential expression of CYC orthologs in dorsal versus ventral regions of the flower that are associated with bilateral symmetry.…”

Advances in Research on the Regulation of Floral Development by CYC-like Genes

“…CYC -like gene duplication events have occurred at least five times in the evolutionary history of Gesneriaceae [ 51 ]. Three copies of CYC -like genes in the actinomorphic Conandron ramondioides were not expressed in the corolla, whereas the zygomorphic species Hemiboea bicornuta and Lysionotus pauciflorus retained a CYC1 copy (i.e., GCYC1C and GCYC1D , respectively) expressed in dorsal corolla lobes [ 51 ].…”

“…CYC -like gene duplication events have occurred at least five times in the evolutionary history of Gesneriaceae [ 51 ]. Three copies of CYC -like genes in the actinomorphic Conandron ramondioides were not expressed in the corolla, whereas the zygomorphic species Hemiboea bicornuta and Lysionotus pauciflorus retained a CYC1 copy (i.e., GCYC1C and GCYC1D , respectively) expressed in dorsal corolla lobes [ 51 ]. Selective relaxation after the duplication of CYC1 created evolutionary diversification, in which multiple copies retained the effect of random differentiation affecting the dorsal-specific expression of genes associated with floral symmetry changes [ 51 ].…”

“…The functionally redundant CYC and DICH genes belong to the CYC2 clade and originated from gene duplication events associated with angiosperm evolution [ 48 , 49 , 50 ]. These genes are essential for the development of zygomorphic flowers in angiosperms, especially the CYC genes [ 45 , 51 , 52 ]. The results of studies on snapdragon compelled researchers to investigate the mechanism by which CYC genes regulate floral symmetry.…”

Transcriptomic Analysis Suggests Auxin Regulation in Dorsal-Ventral Petal Asymmetry of Wild Progenitor Sinningia speciosa

“…Therefore, the ventralizing effect of DIV is restricted to the ventral petals, while CYC activates RAD in the dorsal petals, thus creating the dorsal-ventral polarity. In Gesneriaceae species, diversified CYC expression patterns have been found to correlate with floral symmetry transition and flower shape diversity [12][13][14]. However, little is known about which gene regulatory network (GRN) is necessary in addition to CYC-RAD and DIV in generating the size and shape differences between dorsal and ventral petals.…”