Genetic Analysis of Floral Symmetry Transition in African Violet Suggests the Involvement of Trans-acting Factor for CYCLOIDEA Expression Shifts

Abstract

With the growing demand for its ornamental uses, the African violet (Saintpaulia ionantha) has been popular owing to its variations in color, shape and its rapid responses to artificial selection. Wild type African violet (WT) is characterized by flowers with bilateral symmetry yet reversals showing radially symmetrical flowers such as dorsalized actinomorphic (DA) and ventralized actinomorphic (VA) peloria are common. Genetic crosses among WT, DA, and VA revealed that these floral symmetry transitions are likely to be controlled by three alleles at a single locus in which the levels of dominance are in a hierarchical fashion. To investigate whether the floral symmetry gene was responsible for these reversals, orthologs of CYCLOIDEA (CYC) were isolated and their expressions correlated to floral symmetry transitions. Quantitative RT-PCR and in situ results indicated that dorsal-specific SiCYC1s expression in WT S. ionantha (SCYC1A and SiCYC1B) shifted in DA with a heterotopically extended expression to all petals, but in VA, SiCYC1s' dorsally specific expressions were greatly reduced. Selection signature analysis revealed that the major high-expressed copy of SCYC1A had been constrained under purifying selection, whereas the low-expressed helper SiCYC1B appeared to be relaxed under purifying selection after the duplication into SCYC1A and SiCYC1B. Heterologous expression of SCYC1A in Arabdiopsis showed petal growth retardation which was attributed to limited cell proliferation. While expression shifts of SCYC1A and SiCYC1B correlate perfectly to the resulting symmetry phenotype transitions in F1s of WT and DA, there is no certain allelic combination of inherited SiCYC1s associated with specific symmetry phenotypes. This floral transition indicates that although the expression shifts of SCYC1A/1B are responsible for the two contrasting actinomorphic reversals in African violet, they are likely to be controlled by upstream trans-acting factors or epigenetic regulations.

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

“…While in Oreocharis dinghushanensis , GCYC1C ( OpdCYC1C ) expression further extended to all petals but GCYC1D ( OpdCYC1D ) remained expressed in the dorsal petals only (Fig 6) [27]. In Saintpaulia ionanthus (now Streptocarpus ionanthus , see [29]), one additional duplication of GCYC1C resulted in one major copy, GCYC1A , strongly expressed in dorsal petals, and the other copy, GCYC1B , weakly expressed there [32] (Fig 6). Similar to the case for CYC and DICH , this GCYC1A / GCYC1B duplication indicated a functionally redundant duplication in which perhaps one major and one helper function evolved.…”

“…Within tribe Trichosporeae, perhaps two additional independent GCYC1 duplication events were identified. One duplication was detected across the tribe except for European species, forming two subclades, namely GCYC1C and GCYC1D , the other occurred solely for the African genus Streptocarpus [29] generating GCYC1A and GCYC1B [23, 27, 28, 30, 31, 32]. Together with the fact that Trichosporeae species have the highest number of reversals to actinomorphy, the high number of GCYC1 duplications may imply that GCYC duplication correlates with the frequent floral symmetry transitions.…”

Expression shifts of floral symmetry genes correlate to flower actinomorphy in East Asia endemic Conandron ramondioides (Gesneriaceae)

“…In Gesneriaceae, reversal to actinomorphy through both ventralization or dorsalization were reported (e.g. Bournea leiophylla , Tengia scopulorum and Saintpaulia ionantha ) (Zhou et al 2008 ; Pang et al 2010 ; Hsu et al 2018 ). In B. leiophylla , the BlCYC1 and BlRAD genes were transiently expressed in floral meristem initiation stage and then quickly vanished at latter developmental stages.…”

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.…”

“…Transgenic plants of Arabidopsis thaliana over-expressing the CYC gene from A. majus show increased petal size as a consequence of an increase in cell expansion in petals, whereas CYC reduces both cell proliferation (by promoting the early arrest of cell division) and cell expansion in leaves [16,17]. Among Gesneriaceae species, over-expressing the SiCYC1A gene from the African violet (Streptocarpus ionanthus) in A. thaliana results in a reduction in petal size due to decreased cell proliferation [14]. The constitutive expression of CYC1C homologous genes from Primulina heterotricha and SsCYC from S. speciosa in A. thaliana, however, reduce petal size via the regulation of decreased cell growth [18,19].…”