Floral development begins with the conversion of vegetative meristems to flowering meristems in angiosperms (flowering plants). Meristems are regions of tissue consisting of plant stem cells. These undifferentiated cells divide to give rise to specialised cells like leaf cells.
The switch to flowering occurs through the induction of floral developmental genes in response to environmental signals. Different plants respond to either a short photoperiod or a long photoperiod to initiate flowering. Specifically, leaves detect photoperiod and flowering is induced by a transmissible signalling molecule called florigen. This hormone-like molecule is produced in the leaves and is transported to the apical vegetative meristem via the phloem. Some plants require a vernalisation stage where exposure to cold temperatures before the correct photoperiod is required to trigger flowering. Hormones and the stage of maturity of the plant also play a part in flower initiation. These requirements ensure flowers are developed at the right point in the season to maximise the plants success.
The flower of a plant consists of four floral organs arranged in concentric whorls (Figure 1):
1. Sepal (Green)
2. Petal (Red)
3. Stamen (Purple)
4. Carpel (Blue)
Arabidopsis thaliana is a small angiosperm weed with a short lifecycle lasting 6-8 weeks. They are easy to transform genetically because their genome is small and sequenced. This means genetically mutanted plants are readily available. Arabidopsis can self-pollinate and cross pollinate which simplifies reproduction and allows increasing seed production. These features make Arabidopsis a convenient model organism for plant research.
Genes involved in flower development were studied in Arabidopsis. Three classes of genes specify floral organ identity in the developing flower:
The proteins encoded by the ABC genes are MADS box transcription factors. These transcription factors include a MADS box sequence that binds DNA and a K-box sequence for dimerization. Therefore, these proteins form dimers on DNA. ABC genes activate the expression of other genes that cause cells of the meristem to form different parts of the flower.
Activity of each class of genes is required in the cells of two adjacent floral whorls. Each floral organ type originates from a specific region in the floral meristem due to the expression of ABC genes in developmental fields. Each class of gene is expressed in specific parts of the meristem. However, there is areas of overlap in gene expression (Figure 2).
The ABC model for floral organ development
Losing class A or C genes makes the remaining gene extend it's activity into the absent genes’ developmental field. Thus class A and C genes are mutually antagonistic; the functional proteins produced inhibit expression of the opposing gene. Additionally, the class C genes terminate stem cell maintenance which allows cells to differentiate into floral organ cells.
Mutations that occur in hox (or homeotic) genes are called homeotic mutations. These genes encode transcription factors that control development by regulating the identity of body parts to eventually give rise to the body plan. Homeotic mutants are displayed as transformation of one body part into another. These mutations were used in the model plant Arabidosis thaliana to determine the model for floral development. Plants with mutated ABC genes produce homeotic mutant flowers.
Class A mutant: sepals (Figure 1, green) and petals (Figure 1, red) transformed into stamens (purple) and carpels (blue). Class C gene activity was not inhibited by class A genes, therefore it's activity spread into the other whorls.
Class B mutant: petals (Figure 1, red) and stamens (Figure 1, purple) transformed into sepals (green) and carpels (blue). In the absence of class B genes, ABC genes cannot work together to activate petal and stamen development.
Class C mutant: stamens (Figure 1, purple) and carpels (Figure 1, blue) transformed into petals (red) and sepals (green). Activity of class A genes was not inhibited by class C genes, therefore their activity spread into the other whorls.
Double mutant plants helped to determine the inhibitory characteristics of the class A and C genes.
The ABC model gets a bit more complicated…
A triple ABC mutant plant does not form flowers at all however ectopic expression of the ABC genes does not form a flower either. Something else was needed for flower development. Using multiple gene mutants, it was found that four SEPALLATA genes (E genes), which are also MADS box transcription factors, act redundantly together with ABC genes to specify floral organ identity. Moreover, E genes are necessary for ovule development along with D genes. Thus, the general ABC model expanded to an ABCDE model (Figure 3), although other variations exist.
Thus, as shown in Figure 4, the respective ABC transcription factors work in combination with SEPALLATA transcription factors by forming combinations of tetrameric complexes. These four protein complexes act together to regulate genes involved in development of parts of the flower. For instance, the development of carpels requires class C genes, so the class C transcription factor AGAMOUS forms a complex with three other proteins (in this case two SEPALLATAs and another AGAMOUS) to promote transcription of genes for carpel development.
When leaves produce the chemical signal florigen, it is transmitted to apical vegetative meristems to initiate the conversion process by turning on the Flowering Locus T gene which then switches on the expression of LEAFY.
LEAFY is a transcription factor that binds as a dimer to the promoters of ABC genes to turn on the floral organ identity genes to then cause undifferentiated cells in the meristem to change fate and develop as flowers rather than shoots. A LEAFY mutant makes a leafy plant because the developmental ground state of a floral organ is a leaf since vegetative meristems first need to convert to floral meristems. The vegetative meristem carries on making leaves as there are no ABC transcription factors to switch on floral genes and so there is no transition from vegetative growth to flowering.
Overexpressing LEAFY in Arabidopsis thaliana, results in a short terminal flower. LEAFY activity is regulated by Terminal Flower 1 (TFL1) which represses LEAFY activity. In a TFL1 mutant, LEAFY is no longer repressed and a single terminal flower is developed. Conversely, when TFL1 is constitutively expressed, flowering is delayed.
Snapdragon flowers (Antirrhinum majus) are not radially symmetrical but bilaterally symmetrical. If floral developmental genes function in designated regions of the floral meristem, how does asymmetry develop? There are two genes involved in the asymmetrical growth of Antirrhinum flowers; CYCLOIDEA and DICHOTOMA. Double mutants for these two genes result in radially symmetrical flowers.
Evidence suggests that the ABC model is an ancient regulatory system and may apply to most angiosperms. Homologues of ABC genes are found across many model plant species including Petunia hybrida (petunia), Oryza saliva (Asian rice) and Zea Mays (maize) to name a few. Separate genes may be involved in specifying diverse flowers such as the bilaterally symmetrical flowers of Antirrhinum but the ABC model can be applied to nearly all flowering plants.
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Pelaz, S., Ditta, G. S. & Baumann, E. et al. (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 405 (6783): 200-203
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