Functional diversification of duplicated CYC2 clade genes in regulation of inflorescence development in Gerbera hybrida (Asteraceae)

Abstract

SUMMARYThe complex inflorescences (capitula) of Asteraceae consist of different types of flowers. In Gerbera hybrida (gerbera), the peripheral ray flowers are bilaterally symmetrical and lack functional stamens while the central disc flowers are more radially symmetrical and hermaphroditic. Proteins of the CYC2 subclade of the CYC/TB1-like TCP domain transcription factors have been recruited several times independently for parallel evolution of bilaterally symmetrical flowers in various angiosperm plant lineages, and have also been shown to regulate flower-type identity in Asteraceae. The CYC2 subclade genes in gerbera show largely overlapping gene expression patterns. At the level of single flowers, their expression domain in petals shows a spatial shift from the dorsal pattern known so far in species with bilaterally symmetrical flowers, suggesting that this change in expression may have evolved after the origin of Asteraceae. Functional analysis indicates that GhCYC2, GhCYC3 and GhCYC4 mediate positional information at the proximal-distal axis of the inflorescence, leading to differentiation of ray flowers, but that they also regulate ray flower petal growth by affecting cell proliferation until the final size and shape of the petals is reached. Moreover, our data show functional diversification for the GhCYC5 gene. Ectopic activation of GhCYC5 increases flower density in the inflorescence, suggesting that GhCYC5 may promote the flower initiation rate during expansion of the capitulum. Our data thus indicate that modification of the ancestral network of TCP factors has, through gene duplications, led to the establishment of new expression domains and to functional diversification.

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

“…In addition to ray and disc florets, the G. hybrida capitulum has zygomorphic trans florets that have intermediate features of both ray and disc florets. Among the G. hybrida CYC2 clade members, GhCYC2, GhCYC3, GhCYC4, GhCYC5, and GhCYC9 also showed ray/trans floret-specific expression (Broholm et al, 2008;Juntheikki-Palovaara et al, 2014) and overexpression of GhCYC2 generated disc florets with ray floret features (Broholm et al, 2008;Preston and Hileman, 2009;Juntheikki-Palovaara et al, 2014). In agreement with the other species, two CYC2 genes in S. vulgaris, RAY1 and RAY2, were expressed only in the ray florets and were also shown to control ray versus disc floret identity (Kim et al, 2008).…”

“…Functional analyses in S. vulgaris revealed that overexpression of RAY1 reduced ventral petal growth in ray florets, while overexpression of RAY2 promoted dorsal ray petal outgrowth to produce tubular ray florets (Kim et al, 2008). Further work in gerbera suggests that localized expression of GhCYC2 to the ventral petals explains this zygomorphic phenotype (Broholm et al, 2008;Juntheikki-Palovaara et al, 2014); however, differential expression of CYC2 clade genes in ventral and dorsal petals in other Asteraceae species has not yet been seen.…”

A CYCLOIDEA-like gene mutation in sunflower determines an unusual floret type able to produce filled achenes at the periphery of the pseudanthium

“…We hypothesize that other CYC/TB1-like genes are important to determine the specific characteristics of tubular-like ray florets. In fact, 10 genes of the CYC/TB1-like gene family have been identified in gerbera as well in sunflower, and duplicated CYC2 clade genes are associated with pseudanthium architecture and differentiation of floral reproductive organs (Broholm et al 2008;Chapman et al 2008;Tähtiharju et al 2012;Juntheikki-Palovaara et al 2014). CYC2 clade genes show highly overlapping expression patterns, and functional gene specificity could be obtained through context-specific protein complexes that activate different downstream targets.…”

“…In the last few years, the molecular aspects of pseudanthium development have been studied in Asteraceae, Dipsacaceae, and Myrtaceae, implicating CYC2 clade genes in the regulation of floret type identity (Broholm et al 2008;Chapman et al 2008;Kim et al 2008;Carlson et al 2011;Tähtiharju et al 2012;Claßen-Bockhoff et al 2013;Juntheikki-Palovaara et al 2014).…”

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

“…Different combinations of these florets and variation of the petal types give rise to a variety of flower head types. Moreover, the presence of the showy ray florets in the capitulum has been shown to be associated with pollinator-mediated speciation, outcrossing rage and genetic diversity, and may lead to the evolutionary success of the Asteraceae (Marshall and Abbott, 1984; Sun and Ganders, 1990; Endress, 1999; Sargent, 2004; Juntheikki-Palovaara et al, 2014). Both classical and modern molecular genetic studies have indicated that the presence or absence of ray florets is mainly under the control of one or two major genes and some other modifier genes (Gillies et al, 2002; Andersson, 2008).…”