In 1991, we published a paper in Development that proposed the ABC model of flower development, an early contribution to the genetic analysis of development in plants. In this, we used a series of homeotic mutants, and double and triple mutants, to establish a predictive model of organ specification in developing flowers. This model has served as the basis for much subsequent work, especially towards understanding seed plant evolution. Here, we discuss several aspects of this story, that could be a much longer one. One surprising conclusion is that materials and methods that might have led to similar work, and to the same model, were available 100 years before our experiments, belying the belief that progress in biology necessarily comes from improvements in methods, rather than in concepts.

The cover of the issue of Development in which the ABC paper appeared. The photograph depicts eight different genotypes of Arabidopsis flowers. Wild-type flowers are shown with three different single floral homeotic mutants (ap3-1, ap2-1 and ag-1), and the three double mutant and the triple mutant combinations of these alleles.


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The ABC model was popularized in a review in Nature published later in 1991 by the senior author and Enrico Coen, whose group had been making parallel new findings of similar homeotic mutants in snapdragon (Antirrhinum majus) (Coen and Meyerowitz, 1991). In this review, functions were distinguished from regions (or fields) by using a, b and c for functions and A, B and C for regions, although it is now customary to capitalize the functions. The importance of comparative findings in Antirrhinum was highlighted by the earlier contribution of Zsuszanna Schwarz-Sommer and colleagues, who independently generated a floral organ identity model that proposed the equivalent of B and C functions, but lacked A function and was not tested using multiple mutants (Schwarz-Sommer et al., 1990).

The ABC model is still widely used as a framework for understanding floral development today (Krizek and Fletcher, 2005; Causier et al., 2010). The impact of the Development paper is reflected in its continued high citation rate (it still gathers over 30 citations a year according to the Web of Knowledge, ). Significant advances since 1991 include findings that: (1) all genes, except AP2, encode MADS transcription factors (e.g. Weigel and Meyerowitz, 1994); (2) another A function gene, APETALA1, exists in Arabidopsis (Bowman et al., 1993; Gustafson-Brown et al., 1994); (3) four other MADS genes (SEPALLATAs) are involved in establishing the floral nature of flower organs in Arabidopsis (Pelaz et al., 2000) (often called E function, although using our terminology these would be meristem identity, not organ identity, genes); (4) SEP proteins likely act in multimeric combination with A, B and C function MADS proteins (the quartet model) (e.g. Melzer and Theissen 2009); (5) AP2 transcripts are regulated post-transcriptionally by microRNAs (Aukerman and Sakai, 2003; Chen, 2004); and (6) AP2 is a direct negative regulator of AG expression, a very recent finding (Dinh et al., 2012).

Perhaps owing to its relative simplicity, and to the ubiquity of the appreciation of flowers in human society, the ABC model was rapidly introduced into university textbooks, not only those focused on developmental biology (e.g. Wolpert and Tickle, 2011), but also to first year general biology textbooks (e.g. Campbell et al., 1999; Freeman, 2008), cell biology texts (e.g. Alberts et al., 1994) and those focused on genetics (e.g. Griffiths et al., 1993; Sanders and Bowman, 2012). The ABC model is even being taught to high school students in some locales (Fig. 3).

Cartoon of the ABC model drawn by Ryoko Hirano and which Hiroyuki Hirano used to teach summer school for secondary school students in Japan. Note the colorful inclusion of the critical A-C mutual inhibition. Image courtesy of Hiroyuki and Ryoko Hirano (University of Tokyo).

While an insect eats, some pollen from the flower sticks to it. When the insect lands on another flower, that pollen is collected on the stigma. A pollen tube then grows down through the style to the ovary, which the pollen travels down.

To use the models, close one eye and hold the models at eye level. Rotate the models and observe how the perceived proportions of length and width change. Also notice how the angles of the tip of the leaf, veins, and negative spaces between petals change. To take the leaf model to another level, turn it over and trace the vein lines with a pencil on the back side. Then curl the leaf model gently. Observe the shapes and angles when you can see both the top and the bottom of the leaf. Once you understand how the widths and lengths of the petals change as you rotate the flower model, you are ready to study cone-shaped flowers. Turn the flower model over and trace the petal shapes on the back of the paper. Then overlap two of the petals to form a cone. Now observe how the proportions of the petals change as you rotate the cone (again with one eye closed and the model at eye level). If you study this model, you will develop an intuitive understanding of how to foreshorten flowers.

Using paper models to teach and understand leaf and flower foreshortening is a very effective way to learn and teach. I have developed and refined this system through teaching classes and experimentation. I give my permission to use these materials to any teacher who would like to use them. Please give an acknowledgment where appropriate and let your students know about other learning resources on this site.

The ABC model of flower development is a scientific model of the process by which flowering plants produce a pattern of gene expression in meristems that leads to the appearance of an organ oriented towards sexual reproduction, a flower. There are three physiological developments that must occur in order for this to take place: firstly, the plant must pass from sexual immaturity into a sexually mature state (i.e. a transition towards flowering); secondly, the transformation of the apical meristem's function from a vegetative meristem into a floral meristem or inflorescence; and finally the growth of the flower's individual organs. The latter phase has been modelled using the ABC model, which aims to describe the biological basis of the process from the perspective of molecular and developmental genetics.

An external stimulus is required in order to trigger the differentiation of the meristem into a flower meristem. This stimulus will activate mitotic cell division in the apical meristem, particularly on its sides where new primordia are formed. This same stimulus will also cause the meristem to follow a developmental pattern that will lead to the growth of floral meristems as opposed to vegetative meristems. The main difference between these two types of meristem, apart from the obvious disparity between the objective organ, is the verticillate (or whorled) phyllotaxis, that is, the absence of stem elongation among the successive whorls or verticils of the primordium. These verticils follow an acropetal development, giving rise to sepals, petals, stamens and carpels. Another difference from vegetative axillary meristems is that the floral meristem is "determined", which means that, once differentiated, its cells will no longer divide.[1]

The identity of the organs present in the four floral verticils is a consequence of the interaction of at least three types of gene products, each with distinct functions. According to the ABC model, functions A and C are required in order to determine the identity of the verticils of the perianth and the reproductive verticils, respectively. These functions are exclusive and the absence of one of them means that the other will determine the identity of all the floral verticils. The B function allows the differentiation of petals from sepals in the secondary verticil, as well as the differentiation of the stamen from the carpel on the tertiary verticil.

Goethe's foliar theory was formulated in the 18th century and it suggests that the constituent parts of a flower are structurally modified leaves, which are functionally specialized for reproduction or protection. The theory was first published in 1790 in the essay "Metamorphosis of Plants" ("Versuch die Metamorphose der Pflanzen zu erklren").[2] where Goethe wrote:

The transition from the vegetative phase to a reproductive phase involves a dramatic change in the plant's vital cycle, perhaps the most important one, as the process must be carried out correctly in order to guarantee that the plant produces descendants. This transition is characterised by the induction and development of the meristem of the inflorescence, which will produce a collection of flowers or one flower. This morphogenetic change contains both endogenous and exogenous elements: For example, in order for the change to be initiated the plant must have a certain number of leaves and contain a certain level of total biomass. Certain environmental conditions are also required such as a characteristic photoperiod. Plant hormones play an important part in the process, with the gibberellins having a particularly important role.[4] 006ab0faaa

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