Co‐option of a carotenoid cleavage dioxygenase gene (CCD4a) into the floral symmetry gene regulatory network contributes to the polymorphic floral shape–color combinations in Chrysanthemum sensu lato

Abstract

Morphological novelties, including formation of trait combinations, may result from de novo gene origination and/or co-option of existing genes into other developmental contexts. A variety of shape-color combinations of capitular florets occur in Chrysanthemum and its allies. We hypothesized that co-option of a carotenoid cleavage dioxygenase gene into the floral symmetry gene network would generate a white zygomorphic ray floret.We tested this hypothesis in an evolutionary context using species in Chrysanthemum sensu lato, a monophyletic group with diverse floral shape-color combinations, based on morphological investigation, interspecific crossing, molecular interaction and transgenic experiments.Our results showed that white color was significantly associated with floret zygomorphy. Specific expression of the carotenoid cleavage dioxygenase gene CCD4a in marginal florets resulted in white color. Crossing experiments between Chrysanthemum lavandulifolium and Ajania pacifica indicated that expression of CCD4a is trans-regulated. The floral symmetry regulator CYC2g can activate expression of CCD4a with a dependence on TEOSINTE BRANCHED1/ CYCLOIDEA/PROLIFERATING (TCP) binding element 8 on the CCD4a promoter.Based on all experimental findings, we propose that gene co-option of carotenoid degradation into floral symmetry regulation, and the subsequent dysfunction or loss of either CYC2g or CCD4a, may have led to evolution of capitular shape-color patterning in Chrysanthemum sensu lato.

Symmetry vs coloration in flowers: a tight genetic link through evolutionary co‐option

“…In this issue of New Phytologist , Zhang et al . (2022; pp. 1197–1211) investigated the genetic cause of the intriguing combination of white, zygomorphic ray florets and yellow, actinomorphic disc florets in species of Chrysanthemum sensu lato (s.l.).…”

“…Together with the findings from Zhang et al . (2022), it indicates that co‐option of pigmentation regulators, even from diverse pigmentation pathways, into the same floral symmetry regulatory network has occurred independently in distinct plant lineages. Future research on more examples would help to clarify whether a similar strategy is widespread during the evolution of flowering plants.…”

“…Flower symmetry and colour are often considered as two separate traits controlled by independent genetic regulatory networks, however, their interconnection is less understood. In this issue of New Phytologist, Zhang et al (2022; pp. 1197-1211 investigated the genetic cause of the intriguing combination of white, zygomorphic ray florets and yellow, actinomorphic disc florets in species of Chrysanthemum sensu lato (s.l.).…”

“…For coloration, it was shown that white colour in ray floret petals of Chrysanthemum morifolium is regulated by the carotenoid cleavage dioxygenase CCD4a, and that the presence or absence of CCD4a in the genome of different wild Chrysanthemum species resulted in white or yellow colours in their ray florets, respectively (Ohmiya et al, 2006). In their study, Zhang et al (2022) isolated and analysed the CCD4 sequences from 27 Chrysanthemum and 21 Ajania species. Interestingly, the authors found that there were three Ajania species with all yellow flowers showing intact genomic sequences of CCD4 in their genome.…”

“…1a,b) (Ren & Guo, 2015;Shen et al, 2021b). To systematically analyse how colour and symmetry of capitular florets have evolved in this group, Zhang et al (2022) first collected morphological data from 89 species that belong to Chrysanthemum s.l. and related species.…”