'Organ'ising Floral Organ Development

Abstract

Flowers are plant structures characteristic of the phylum Angiosperms composed of organs thought to have emerged from homologous structures to leaves in order to specialize in a distinctive function: reproduction. Symmetric shapes, colours, and scents all play important functional roles in flower biology. The evolution of flower symmetry and the morphology of individual flower parts (sepals, petals, stamens, and carpels) has significantly contributed to the diversity of reproductive strategies across flowering plant species. This diversity facilitates attractiveness for pollination, protection of gametes, efficient fertilization, and seed production. Symmetry, the establishment of body axes, and fate determination are tightly linked. The complex genetic networks underlying the establishment of organ, tissue, and cellular identity, as well as the growth regulators acting across the body axes, are steadily being elucidated in the field. In this review, we summarise the wealth of research already at our fingertips to begin weaving together how separate processes involved in specifying organ identity within the flower may interact, providing a functional perspective on how identity determination and axial regulation may be coordinated to inform symmetrical floral organ structures.

Keywords: axiality; flower organs; flowers; gynoecium; homeobox; hormones; identity; symmetry.

Figure 1

The development of the complex shape of a flower is reliant on the combined participation of developmental processes specifying axis growth, identity specification, and symmetry organisation. (A) The transition from a spherical inflorescence meristem (IM) to a floral meristem (FM) and a developed flower requires coordinated growth across adaxial (ad), abaxial (ab), apical (A), basal (B), and medial (M), and lateral (L) axes. (B) Scanning electronic micrograph showing the phyllotactic arrangement of floral buds (differently false-coloured) and primordia at roughly 137° of an Arabidopsis thaliana inflorescence. (C) Scanning electronic micrograph of a mature Arabidopsis flower at stage 12 of its development, showing sepals (s), petals (p), stamens (st), and the central gynoecium (g) (note, some sepals and petals have been removed to show organs located in the central whorls). Schematic transverse sections (dashed lines) at the style and ovary regions of the gynoecium displaying radial and bilateral symmetry, respectively.

Figure 2

The initiation of floral organs is coordinated through inhibitory genetic mechanisms, spatial coordination, and the activity of plant hormones. (A) Inhibition of ventral identity in petals by CYC (Antirrhinum) and PAN/BOP (Arabidopsis). The dorsal petals (red) are a distinct shape to the lateral (yellow) and ventral (blue) petals in Antirrhinum, whereas in Arabidopsis, all petals are the same (brown). (B) Auxin and cytokinin signalling output (yellow and purple, respectively) pattern sites of sepal organ initiation in Arabidopsis floral primordia (black outline).

Figure 3

The development of the female reproductive organ, the gynoecium, in Arabidopsis, requires step-wise recruitment of axis and auxin distribution. (A) The expression patterns of HAT3 (cyan), ATHB4 (red), and SPT (orange), coordinators of axial development, in stage 9 and stage 12 gynoecium. (B) The stepwise development of the style from stage 5 to 10, in terms of auxin localisation (yellow) as regulated be the activity of the transcription factors shown in the figure.

Figure 4

The ABCDE model describes the arrangement of floral organs by classes of genes acting as master regulators of organ identity. (A) The concentric whorls of an Arabidopsis thaliana flower, enclosing the organs they define: the gynoecium, stamen, petals, and sepals from the innermost whorl extending outwards. (B) The ABCDE model as described in the dicotyledonous Arabidopsis flowers. (C) The ABCDE model in the monocotyledonous rice model flower; DL stands for the DROOPING LEAF, the homeotic equivalent to the C-class gene in defining carpel identity. Sepals in whorl 1 are specified by A class genes (red), petals in whorl 2, are specified by A and B class genes (yellow), stamen in whorl 3 are specified by B and C class genes (green) and the gynoecium in whorl 4 is specified by the C class genes (blue).

Figure 5

The role of axiality at the tissue and organ level to direct the symmetry and function of organs. (A) Schematic representation of a petal organised across axes with scanning electron micrographs of abaxial and adaxial cell characteristics. (B) Schematic representation of a bilateral (left) and radial (right) leaf. Loss of adaxial identity in a leaf system results in radialisation of the leaf. (C) Schematic representation of a bilateral petal where loss of abaxiality through imposed adaxiality has the same effect: radialisation of the petal structure. (D) Schematic representation of how coordinated growth rates across the adaxial–abaxial axes form differing symmetries in the establishment of the floral and leaf primordia.