Dysfunction of CYC2g is responsible for the evolutionary shift from radiate to disciform flowerheads in the Chrysanthemum group (Asteraceae: Anthemideae)

• Published in: The Plant journal : for cell and molecular biology 2021-05, Vol.106 (4), p.1024-1038
• Main Authors: Shen, Chu‐Ze, Chen, Jie, Zhang, Chu‐Jie, Rao, Guang‐Yuan, Guo, Yan‐Ping
• Format: Article
• Language: English
• Subjects: Ajania; Asteraceae; capitulum; Chrysanthemum; CYCLOIDEA; Divergence; dysfunction; Evolution; evolutionary alteration; Evolutionary genetics; Gene deletion; Gene expression; Morphogenesis; Morphology; Phylogeny; Pollination; ray floret; TATA‐box
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15216

Summary Evolutionary shifts among radiate, disciform and discoid flowerheads have occurred repeatedly in a number of major lineages across the Asteraceae phylogeny; such transitions may also appear within evolutionarily young groups. Although several studies have demonstrated that CYC2 genes partake in regulating floral morphogenesis in Asteraceae, the evolution of capitulum forms within a recently diverging lineage has remained poorly understood. Here, we study the molecular regulation of the shift from a radiate to a disciform capitulum within the Chrysanthemum group. This is a recently radiating group mainly comprising two genera, Chrysanthemum and Ajania, that are phylogenetically intermingled but distinct in flowerhead morphology: Chrysanthemum spp. with radiate capitula and Ajania spp. with disciform capitula. We found that the morphogenesis of zygomorphy in the marginal floret in Ajania was disrupted soon after floral primordium emergence; CYC2g, one of the CYC2 copies that was expressed prominently in the ray floret of Chrysanthemum was not expressed in flowerheads of Ajania. Weakening the expression of ClCYC2g in Chrysanthemum lavandulifolium led to the gradual transition of a ray flower toward the disc‐like form. Molecular evolutionary analyses indicated that the disciform capitulum might have evolved only once, approximately 8 Mya, arising from dysfunction of the CYC2g orthologs. A 20‐nt deletion, including a putative TATA‐box of the Ajania‐type CYC2g promoter, appeared to inhibit the expression of the gene. Considering the divergent habitats of Chrysanthemum and Ajania, we propose that the shift from radiate to disciform capitulum must have been related to changes in pollination strategies under selective pressure. Significance Statement Innovation or alteration of floral organ morphology is usually associated with speciation events in flowering plants. This study demonstrates that the dysfunction of the CYC2g gene arising from the loss of the TATA‐box in its promoter leads to the shift from radiate to disciform capitulum in the Chrysanthemum group. Considering the ecological differentiation of this species group, our results widen the knowledge about the mechanisms and evolutionary significance of changes in the architecture of the capitulum in Asteraceae.