Positive Selection and Expression Divergence Following Gene Duplication in the Sunflower CYCLOIDEA Gene Family

Abstract

Members of the CYCLOIDEA (CYC)/TEOSINTE-BRANCHED1 (TB1) group of transcription factors have been implicated in the evolution of zygomorphic (i.e., bilaterally symmetric) flowers in Antirrhinum and Lotus and the loss of branching phenotype during the domestication of maize. The composite inflorescences of sunflower (Helianthus annuus L. Asteraceae) contain both zygomorphic and actinomorphic (i.e., radially symmetric) florets (rays and disks, respectively), and the cultivated sunflower has evolved an unbranched phenotype in response to domestication from its highly branched wild progenitor; hence, genes related to CYC/TB1 are of great interest in this study system. We identified 10 members of the CYC/TB1 gene family in sunflower, which is more than found in any other species investigated to date. Phylogenetic analysis indicates that these genes occur in 3 distinct clades, consistent with previous research in other eudicot species. A combination of dating the duplication events and linkage mapping indicates that only some of the duplications were associated with polyploidization. Cosegregation between CYC-like genes and branching-related quantitative trait loci suggest a minor, if any, role for these genes in conferring differences in branching. However, the expression patterns of one gene suggest a possible role in the development of ray versus disk florets. Molecular evolutionary analyses reveal that residues in the conserved domains were the targets of positive selection following gene duplication. Taken together, these results indicate that gene duplication and functional divergence have played a major role in diversification of the sunflower CYC gene family.

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.…”

“…In addition to controlling zygomorphy in solitary flowers such as Antirrhinum, the floral symmetry regulator CYC has acquired a novel role in determining floret identity (disc versus ray) within the capitulum (Kim et al, 2008;Broholm et al, 2008;Chapman et al, 2008). Much of this work has focused on the three model Asteraceae species: Senecio vulgaris (common groundsel), Helianthus annuus (sunflower), and Gerbera hybrida (gerbera; Kim et al, 2008;Broholm et al, 2008;Chapman et al, 2008).…”

A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus

“…The putative TURF-HaCYC2c peptide was 381 amino acids long with a calculated molecular mass of 43,570 Da. No nucleotide polymorphisms were detected between the CDS sequences of TURF-HaCYC2c and the HaCYC2c previously isolated in sunflower (GenBank accession number EU088370; Chapman et al 2008). However, in the HaCYC2c gene isolated from the USDA inbred line Ames 3963 , the intron is positioned before the stop codon (see Fig.…”

Flower symmetry evolution: towards understanding the abominable mystery of angiosperm radiation

“…Expression analysis suggests that gene duplication was followed by divergence in gene regulation and that the specific expression of HaCYC2c only in ray petals indicates a possible role in floral symmetry regulation. (39) In other members of the Asteraceae, however, fewer copy numbers, such as three for Gerbera hybrida and two for Senecio vulgaris, are reported (Fig. 3B).…”