Evolution and Diversification of the CYC/TB1 Gene Family in Asteraceae--A Comparative Study in Gerbera (Mutisieae) and Sunflower (Heliantheae)

Abstract

Plant-specific TCP domain transcription factors have been shown to regulate morphological novelties during plant evolution, including the complex architecture of the Asteraceae inflorescence that involves different types of flowers. We conducted comparative analysis of the CYCLOIDEA/TEOSINTE BRANCHED1 (CYC/TB1) gene family in Gerbera hybrida (gerbera) and Helianthus annuus (sunflower), two species that represent distant tribes within Asteraceae. Our data confirm that the CYC/TB1 gene family has expanded in Asteraceae, a condition that appears to be connected with the increased developmental complexity and evolutionary success of this large plant family. Phylogenetic analysis of the CYC/TB1 gene family revealed both shared and lineage-specific duplications in gerbera and sunflower, corresponding to the three gene lineages previously identified as specific to core eudicots: CYC1, CYC2, and CYC3. Expression analyses of early stages of flower primordia development indicated that especially within the CYC2 clade, with the greatest number of secondary gene duplications, gene expression patterns are conserved between the species and associated with flower and inflorescence development. All sunflower and gerbera CYC2 clade genes showed differential expression between developing flower types, being upregulated in marginal ray (and trans) flowers. One gene in gerbera (GhCYC3) and two in sunflower (HaCYC2d and HaCYC2c) were indicated to be strong candidates as regulators of ray flower identity, a function that is specific for Asteraceae. Our data further showed that other CYC2 clade genes are likely to have more specialized functions at the level of single flowers, including the late functions in floral reproductive organs that may be more conserved across plant families. The expression patterns of CYC1 and CYC3 clade genes showed more differences between the two species but still pointed to possible conserved functions during vegetative plant development. Pairwise protein-protein interaction assays gave the first molecular evidence that CYC/TB1-like proteins function in complexes. Compared with sunflower, the gerbera proteins showed higher capacity for dimerization, between as well as within CYC clades. Our data from two distant species within the Asteraceae suggest that the expansion and the apparent conservation of especially the CYC2 clade CYC/TB1-like genes are associated with the evolution of the increased complexity of the Asteraceae inflorescence architecture.

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

“…In particular, the RAY3 gene fragment was shown to be a homolog of the sunflower HaCYC2b gene and gerbera GhCYC4 and GhCYC9. While RAY3 expression was consistent with GhCYC4 and GhCYC9 (Tähtiharju et al, 2012), its expression differed from that of HaCYC2b (Tähtiharju et al, 2012;Chapman et al, 2008). Our in situ hybridization and qRT-PCR data showed that RAY3 was expressed mainly in ray florets throughout all stages (Figs.…”

“…2 and 3A). The RAY3 sunflower homolog HaCYC2b was initially expressed in ray florets as seen here in Senecio; however, later, HaCYC2b was expressed across multiple floral and vegetative tissues including disc florets (Tähtiharju et al, 2012;Chapman et al, 2008). Instead, RAY3 expression was more similar to the sunflower paralogs, HaCYC2c and HaCYC2d, which were expressed mainly in ray florets throughout all stages.…”

“…Of these CYC2 clade genes, some members are expressed exclusively in ray florets and also cause altered ray floret morphology when disrupted. For example, in H. annuus, HaCYC2c and HaCYC2d showed ray floret-specific expression Tähtiharju et al, 2012). Furthermore, overexpression of HaCYC2c due to an insertion in the promoter generated capitula with only ray florets, providing functional evidence for its role in ray formation (Chapman et al, 2012).…”

“…Of the three CYC clades of the CYCLOIDEA/TEOSINTE BRANCHED1-LIKE (CYC/TB1) subfamily, the CYC2 clade has highly diversified and duplicated within the Asteraceae lineage; six CYC2 clade genes have been identified in both G. hybrida and S. vulgaris, and five in H. annuus (Tähtiharju et al, 2012;Broholm et al, 2008;Kim et al, 2008). Of these CYC2 clade genes, some members are expressed exclusively in ray florets and also cause altered ray floret morphology when disrupted.…”

The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution

“…In evolutionary biology, the Helianthus genus is a long-time model for hybrid speciation and adaptive introgression 10 . In plant science, the sunflower is a model for understanding solar tracking 11 and inflorescence development 12 .…”