As long as a shoot apical meristem has a vegetative identity, it continues to produce new leaf primordia that emerge in a particular pattern from the apical dome. When the repression of the floral meristem identity factors AP1 and LFY is released by the induction of flowering, the meristem switches to a program of producing the floral organs: sepals, petals, stamens, and carpels. These organs form in distinct bands, or whorls, that encircle the meristem, which leads to the radial symmetry found in most flowers. Even in flowers showing bilateral symmetry, the same organs are formed in roughly the same whorls, but the organs are often fused in distinctive ways that lead to novel flower shapes. The central question, then, is how does a meristem control the placement of the proper organ in the proper location — how are the floral organs specified?
ABC Model of Floral Organ Formation
Using a genetic approach to answer the question of floral organ identity, researchers have isolated mutants in floral organ formation that show specific defects in the formation of one or more organ. Intriguingly, when an organ went missing, it was often “replaced” by a different organ. For example, in one flowering mutant, the plant failed to form stamens and carpels, and instead replaced them with petals and sepals, respectively. This kind of mutation, where an organ is replaced with another, is known as a homeotic mutation: the replacement of one organ with a different one.
Screening for flower organ mutants eventually uncovered many genes involved in the specification of organ identity, and the genes were often named based on the phenotype of the mutant. The APETALA mutants, AP1, AP2, and AP3, all lacked petals. The PISTILATA (PI) mutant produced excess pistils in place of stamens. Finally, the AGAMOUS (AG) mutant lacked both stamens and carpels, the gamete-bearing organs. As more and more of these mutants were isolated and characterized, a pattern began to emerge that would become known as the ABC model.
The ABC model predicts that each floral organ is specified by the activity of one or two of the organ identity genes, all of which can be placed into only 3 classes. The ‘A’ class includes AP1 and AP2 activity and specifies the formation of sepals. The ‘B’ class includes AP3 and PI, and specifies the middle two organs (petals and stamens), which we’ll return to in a moment. The ‘C’ class is encoded by AG, and specifies carpel identity.
To explain the homeotic effects, it was postulated that class ‘A’ genes and class ‘C’ genes mutually exclude each other. In cells where the ‘A’ genes are expressed, there can be no ‘C’ gene expression. This phenomenon is common in development, with ‘A’ and ‘C’ known as cadastral genes, setting up a firm boundary between them. Returning to the ‘B’ class, these genes are expressed in an overlapping fashion atop both ‘A’ and ‘C’ regions such that, when ‘B’ mixes with ‘A’, the result is a petal and when ‘B’ mixes with ‘C’, the result is a stamen.
If we return for a moment to the mutant phenotypes, we see that this model explains the main observations of each mutant. For example, the loss of AP1 by mutation results in the pattern carpel-stamen-stamen-carpel. The domain of ‘C’ expression expands into ‘A’ territory, just as would be predicted by loss of ‘A’ activity, resulting in the specification of organs associated with C alone (carpel) or B plus C (stamen). Likewise, agamous mutants show the pattern sepal-petal-petal-sepal, just as predicted by the loss of ‘C’ activity and explained by the encroachment of A activity to take its place. The organs specified are those of A alone (sepal) or A plus B (petal). Finally, in the case of the pistilata mutant, the pattern observed was sepal-sepal-carpel-carpel, just as predicted by the loss of ‘B’ activity.
Since its initial proposal, the ABC model has been enhanced and refined. A fourth class, known as ‘E’, has been added to recognize the contribution of the SEPALLATA genes 1-4. These act as co-regulators in all whorls of the floral meristem, and the loss of all SEP genes results in the formation of only sepals in all organs, thus returning the flower to a collection of leaf-like organs.
The cloning and molecular characterization of the ABC genes revealed them to mostly encode transcription factors. The common thread that ties them together is the nature of the DNA element to which they bind, known as the MADS box. The MADS box is a DNA regulatory region characterized by the sequence CC[A/T]6 GG, and is present in the targets of ABC gene activity. Since their initial discovery in the model plant Arabidopsis, homologs of these MADS-box transcription factors have been identified not only in the flowering plants, but across all eukaryotes.