Control of Floret Symmetry by RAY3, SvDIV1B, and SvRAD in the Capitulum of Senecio vulgaris

Abstract

ORCID IDs: 0000-0002-3703-7531 (H.M.P.G.); 0000-0002-9930-1377 (V.M.R.S.); 0000-0002-8470-793X (M.K.).All members of Asteraceae, the largest flowering family, have a unique compressed inflorescence known as a capitulum, which resembles a solitary flower. The capitulum often consists of bilateral (zygomorphic) ray florets and radial (actinomorphic) disc florets. In Antirrhinum majus, floral zygomorphy is established by the interplay between dorsal petal identity genes, CYCLOIDEA (CYC) and RADIALIS (RAD), and a ventral gene DIVARICATA (DIV). To investigate the role of CYC, RAD, and DIV in the development of ray and disc florets within a capitulum, we isolated homologs of these genes from an Asteraceae species, Senecio vulgaris (common groundsel). After initial uniform expression of RAY3 (CYC), SvRAD, and SvDIV1B in ray florets only, RAY3 and SvRAD were exclusively expressed in the ventral petals of the ray florets. Our functional analysis further showed that RAY3 promotes and SvDIV1B represses petal growth, confirming their roles in floral zygomorphy. Our results highlight that while floral symmetry genes such as RAY3 and SvDIV1B appear to have a conserved role in petal growth in both Senecio and Antirrhinum, the regulatory relationships and expression domains are divergent, allowing ventral petal elongation in Senecio versus dorsal petal elongation in Antirrhinum. In S. vulgaris, diversification of CYC genes has led to novel interactions; SvDIV1B inhibits RAY3 and SvRAD, and may activate RAY2. This highlights how recruitment of floral symmetry regulators into dynamic networks was crucial for creating a complex and elaborate structure such as the capitulum.

Identification and Characterization of CYC-Like Genes in Regulation of Ray Floret Development in Chrysanthemum morifolium

“…In some inflorescences, the growth of ray florets was severally inhibited and resulted in malformation (data not shown). Interestingly, no phenotypic difference was observed in DF among different lines, in accordance with the results in Senecio (Kim et al, 2008; Garcês et al, 2016). …”

“…Furthermore, it is possible that the context-specific protein complex involving GhCYC2 proteins and their co-regulators may target different downstream genes (Juntheikki-Palovaara et al, 2014). Unlike in Gerbera, RAY1, RAY2 , and RAY3 in Senecio are only involved in promoting ventral identity in ray florets, whereas no change is found in DF (Kim et al, 2008; Chapman and Abbott, 2010; Garcês et al, 2016). Therefore, although a great amount of data have shown that these CYC -like genes in Asteraceae are key regulators in regulating flower development, a much more complex regulatory system seems to stay behind the complex flower head (Fambrini et al, 2014b; Juntheikki-Palovaara et al, 2014).…”

“…Much of the work has focused on the three model species: S. vulgaris (Kim et al, 2008; Garcês et al, 2016), H. annuus (Chapman et al, 2008, 2012) and G. hybrid (Broholm et al, 2008; Juntheikki-Palovaara et al, 2014). Surprisingly, few reports have been published on the function of these genes in the chrysanthemum, which is characterized by the extreme diversity of floral morphology.…”

“…In Asteraceae, however, the expression of CYC -like genes is excluded from the dorsal petals and has shifted to the ventral part of ray florets (Chapman et al, 2008; Kim et al, 2008; Tahtiharju et al, 2012; Juntheikki-Palovaara et al, 2014). For example, RAY1, RAY2 , and RAY3 in Senecio , proved to control ray versus disc floret identity, are expressed only in ray florets (Kim et al, 2008; Garcês et al, 2016). Here in chrysanthemum, the CmCYC2 genes were also predominantly expressed in petals of ray florets, consistent with what has been reported previously in Asteraceae (Chapman et al, 2008; Tahtiharju et al, 2012).…”

“…Similarly, in Mohavea confertiflora , the expression of McCYC and McDICH in both dorsal and lateral regions is correlated with the abortion of both dorsal and lateral stamens and the increase of dorsal petal sizes (Hileman and Baum, 2003). In addition to controlling symmetry in a single flower, the TCP domain regulatory proteins in Asteraceae have developed a novel role in regulation of floral identity within the capitulum (Broholm et al, 2008; Fambrini et al, 2014b; Juntheikki-Palovaara et al, 2014; Garcês et al, 2016). Abundant expression data have shown that these members of CYC2 subclade in Asteraceae play a pivotal role in promoting or repressing the growth of ventral petal ligule, and sometimes affecting stamen development, hence change the symmetry of corresponding flowers (Broholm et al, 2008; Fambrini et al, 2014b; Juntheikki-Palovaara et al, 2014; Garcês et al, 2016).…”