TCP transcription factors in action: shaping floral traits and inflorescence architectures

Xuan Hu; Yuyang Wang; Yafei Zhao; Xuan Hu; Yuyang Wang; Yafei Zhao

doi:10.48130/opr-0025-0015

Figure 1.

Floral symmetry and inflorescence patterns in ornamental plants. Actinomorphic (radially symmetrical) flowers: (a) Rosa hybrida; (b) Eschscholzia californica; (c) Michelia figo; (d) Aquilegia viridiflora. Zygomorphic (bilaterally symmetrical) flowers: (e) Cysticapnos vesicaria; (f) Primulina 'Flying Wings' (P. fimbrisepala × P. linearifolia); (g) Antirrhinum majus; (h) Phalaenopsis aphrodite. Pseudanthia (false flowers): (i) Helianthus annuus; (j) Scabiosa comosa; (k) Allium giganteum; (l) Gomphrena globose. Schematic diagrams of (m) actinomorphic flower, (n) zygomorphic flower, and (o) pseudanthia.

Figure 2.

Classification and structural domains of TCP transcription factors. (a) Phylogenetic classification of TCP transcription factors into two major classes: Class I (TCP-P), represented by the PCF subfamily, and Class II (TCP-C), which is further divided into CIN-like and CYC/TB1 subclades. The CYC/TB1 subclade is angiosperm-specific and further differentiates into distinct lineages in core and non-core eudicots. In core eudicots, three paralogous groups (CYC1, CYC2, and CYC3) are typically present, while in non-core eudicots, homologs are referred to as CYC-like (CYL) or TB1-like (TBL). (b) Schematic representation of the conserved domains in Class II TCP proteins: the TCP domain (green), the ECE motif (pink), the R domain (blue) and the miR319 target site (yellow). They contribute to the specification of different TCP subclades.

Figure 3.

Phylogenetic distribution and floral expression patterns of CYC/TB1 homologs across angiosperms. The left panel depicts a simplified phylogeny of angiosperm lineages, including core eudicots (pink), basal eudicots (green), monocots (blue), and magnoliids (yellow). Representative species from different clades are shown. The right panel illustrates the spatial and temporal expression patterns of CYC/TB1 homologs in floral primordia and floral organs at different development stages. Genes with documented roles in floral symmetry regulation are displayed, with expression domains highlighted in green and undetected expression in white. Expression is mapped onto floral diagrams, with petals, sepals, stamens, and carpels indicated according to the key at the bottom. Legend symbols indicate meristem and floral stages: IM, inflorescence meristem; FM, floral meristem; iB, involucral bract; RF, ray flower; DF, disc flower. * denote species with ray flower-specific expression (Gerbera hybrida). The black dot represents the stem indicating dorsal position. Dashed lines separate different angiosperm groups for comparative analysis.

Figure 4.

Expression levels and spatial patterns of CYC genes in various pseudanthia structures across four plant families. (a) In Asteraceae, the expression of CYC2c (analogous to CYC2g) is associated with floral zygomorphy in Chrysanthemum morifolium, with stronger expression in ray flowers, while absent expression in disc flowers and the flowers of Ajania pacifica; meanwhile, tubular and flat ray flowers show different expression pattern of CYC2c in ventral petal primordia. (b) In Apiaceae, CYC expression contributes to floral asymmetry in Daucus carota and Echinophora trichophylla*, where marginal flowers show higher expression levels at their elongated petals. (c) In Dipsacaceae, multiple CYC homologs regulate zygomorphy in Knautia macedonica, and their expression gradient level contributes to floral symmetry variation, while Bassecoia bretschneideri exhibits actinomorphic flowers with low CYC copies and absent CYC expression. (d) In Myrtaceae, the CYC1 genes show a gradient expression from outer ray-like branches to inner flowers and are likely to control branch suppression in Actinodium cunninghamii. Expression intensity is in a gradient from low (white) to high (orange). * Indicates insufficient data and hypothetical interpretations.

Figure 5.

Regulatory network of TCP transcription factors in flower and inflorescence development. (a) Co-option of petal morphology with pigmentation and floral orientation. The CYC/TB1 clade regulates petal pigmentation, asymmetric patterning, and floral orientation through TCP transcription factor binding sites (TFBS). Downstream targets include MYB1, F3'5'H, CCD4a, and chlorophyll biosynthesis genes, which modulate floral symmetry and pigmentation patterning, as well as additional unknown factors that contribute to floral orientation. (b) Auto- and cross-regulation among TCP and MADS-box genes. TCP transcription factors regulate each other through auto- and cross-regulatory feedback loops to establish and maintain floral zygomorphy. TCPs regulate and interact with MADS-box genes contribute to floral organ identity establishment and development. (c) BOP-CYC interaction module. MlBOP self-ubiquitinates and suppresses MlCYC2A self-activation, while MlCYC2A impedes MlBOP ubiquitination, creating a molecular tug-of-war that fine-tunes flower symmetry. This module ensures precise spatial and temporal control of CYC expression in floral symmetry patterning.