Ray flower initiation in the Helianthus radula inflorescence is influenced by a functional allele of the HrCYC2c gene

Abstract

The radiate pseudanthium, with actinomorphic disk flowers surrounded by showy marginal zygomorphic ray flowers, is the most common inflorescence in the Helianthus genus. In Helianthus radula, ray flower primordia are normally absent at the dorsal domain of the inner phyllaries (discoid heads) while the occurrence of radiate inflorescences is uncommon. In Helianthus spp., flower symmetry and inflorescence architecture are mainly controlled by CYCLOIDEA (CYC)-like genes but the putative role of these genes in the development of discoid inflorescences has not been investigate. Three CYC genes of H. radula with a role in ray flower identity (HrCYC2c, HrCYC2d, and HrCYC2e) were isolated. The phylogenetic analysis placed these genes within the CYC2 subclade. We identified two different alleles for the HrCYC2c gene. A mutant allele, designed HrCYC2c-m, shows a thymine to adenine transversion, which generates a TGA stop codon after a translation of 14 amino acids. We established homozygous dominant (HrCYC2c/HrCYC2c) and recessive (HrCYC2c-m/HrCYC2c-m) plants for this nonsense mutation. Inflorescences of both HrCYC2c/HrCYC2c and HrCYC2c/HrCYC2c-m plants initiated ray flowers, despite at low frequency. By contrast, plants homozygous for the mutant allele (HrCYC2c-m/ HrCYC2c-m) failed at all to develop ray flowers. The results support, for the first time, a role of the HrCYC2c gene on the initiation of ray flower primordia. However, also in the two dominant phenotypes, discoid heads are the prevalent architecture suggesting that this gene is required but not sufficient to initiate ray flowers in pseudanthia. Other unknown major genes are most likely required in the shift from discoid to radiate inflorescence.

Development and evolution of the Asteraceae capitulum

“…However, Fambrini et al (2014) discovered that the insertion of the TE in HaCYC2c promoter does not always lead to ectopic expression and shift toward zygomorphic florets, suggesting that the regulation of flower type identity is much more complexand genotype-specific. In sunflower, discoid capitula are found in Helianthus radula, a species widespread in the southeast of the United States (Mason et al, 2015;Fambrini et al, 2020). Although H. radula occasionally forms ray florets, they are few and tiny, and not comparable to any other Helianthus species (Heiser et al, 1969;Fambrini et al, 2020).…”

“…In sunflower, discoid capitula are found in Helianthus radula, a species widespread in the southeast of the United States (Mason et al, 2015;Fambrini et al, 2020). Although H. radula occasionally forms ray florets, they are few and tiny, and not comparable to any other Helianthus species (Heiser et al, 1969;Fambrini et al, 2020). Fambrini et al (2020) showed that a functional allele of HrCYC2c gene is necessary, but not sufficient, for ray initiation.…”

Advances in Research on the Regulation of Floral Development by CYC-like Genes

“…Fambrini et al isolated three CYC2 subclade genes ( HrCYC2c , HrCYC2d , and HrCYC2e ) associated with the identity of the Helianthus ray–floret (Hr), among which HrCYC2c played an important role in the initiation of the ray floret primordium [ 38 ]. The capitula of HrCYC2c -mutant homozygous dominant plants ( HrCYC2c / HrCYC2c ) and heterozygous dominant plants ( HrCYC2c / HrCYC2c-m ) initiated ray florets, whereas the recessive homozygous plants ( HrCYC2c-m / HrCYC2c-m ) did not develop ray florets [ 38 ].…”

“…In different evolutionary lineages, gene duplication events occurred in each branch at different time points during evolution [ 29 , 30 , 31 , 32 , 33 , 34 , 35 ], as shown in Figure 1 . A more thorough analysis of the CYC2 subgroup confirmed that they are key regulatory genes for the bilateral symmetry of flowers [ 36 , 37 , 38 ].…”

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

“…It has central (usually bisexual) disc florets and peripheral conspicuous (usually female) ray florets. Other types, such as the discoid head (with only bisexual disc florets) and the disciform head (discoid-like, but with a few female asymmetric marginal florets) are scattered across the phylogeny of the family (Bello et al, 2013;Chen et al, 2018;Fambrini et al, 2020;Funk et al, 2009;Harris, 1995Harris, , 1999Jeffrey, 2009;Leppik, 1970).…”