Gene co-option behind the shape-color association of radiate capitula is evolutionarily conserved in the tribe Anthemideae (Asteraceae)

Abstract

The Asteraceae capitulum, particularly a radiate capitulum with differing colors of ray and disc florets, resembles a solitary flower probably through adaption to animal pollination. A previous study found that the shape-color association in Chrysanthemum was due to co-option of the carotenoid-cleavage-dioxygenase gene CCD4a under regulation of the ray-floret identity CYC2g, a member of floral symmetry regulators CYCLOIDEA. Then questions arise: Is such a gene co-option specific to Chrysanthemum? Or did it originate earlier in the evolution of Chrysanthemum and allies? To answer these questions, we examined 11 species representing four color patterns of radiate capitula in the tribe Anthemideae, to which Chrysanthemum belongs. Comparative examinations of carotenoid content, expression patterns of CYC2-like and CCD-like genes along floret developments, and dual-luciferase assays showed that capitular color patterns were strongly correlated with patterns of carotenoid accumulation/degeneration. In the white-ray/yellow-disc species, both CYC2g and CCD4a were ray-specifically expressed and CYC2g can activate CCD4a; in the yellow-ray/yellow-disc species, CCD4a genes were either lost or repressed by CYC2g. The white discs of Achillea alpina must be due to other regulators activating CCD4a expression. The bicolor rays of Glebionis coronaria seemed to have complex color regulation probably due to redundant function of two CCD4a paralogs. In sum, the shape-color association of a radiate capitulum is evolutionarily conserved in the tribe Anthemideae, and the underpinning gene co-option of CCD4a into the floral symmetry regulation network probably arose before divergence of the tribes Anthemideae and Astereae as the divergence of CCD4 into CCD4a and CCD4b occurred at approximately that time.

Keywords

Anthemideae / Asteraceae / color pattern evolution / gene co-option / radiate capitulum / shape-color association

RIGHTS & PERMISSIONS

2025 Institute of Botany, Chinese Academy of Sciences.