Chapter 9. Flowering
9.2 Flower morphogenesis
The flower meristem of Arabidopsis produces four different organs in the four whorls of the flower:
sepals, petals, anthers and carpel. It indicates that different morphogenetic pathways and gene expression programs are operating in the different whorls. How the flower meristem can govern this variety of programs?
9.2.1. The ABC model of flower morphogenesis
The scientists searching an answer for this question were looking for Arabidopsis mutants where flowering was not affected only flower organ formation. Three classes of mutants could be identified (22): in the “A” class, the mutants had neither sepals nor petals but all four whorls had anthers or carpels (the two mutants were named apetala1 and apetala2; note: the corresponding genes APETALA 1 and APETALA 2 has other functions as well as it was already discussed); in the “B” class, the mutant
100 flowers had neither petals nor anthers, only sepals and carpels in all whorls (two mutants falling into this category were named as apetala3 and pistillata); in the “C” class there was only one mutant that had flowers having only sepals and petals in all whorls (no anthers, no carpels, therefore, it got the name agamous). In these mutants, the formation of given flower organs was not prevented, but a given type of organ was converted into another. This type of mutation is called “homeotic”.
The above findings indicate that only three classes of mutations exist for four flower organs. This contradiction could be resolved by establishing the so called “ABC model” of flower development (22,23). The model is based on the assumption that the genes responsible for the “A”, “B” and “C”
functions corresponding to the “A”, “B”, and “C” mutations, are expressed in partially overlapping fashion in the four whorls (Fig. 9.9). In the first whorl, only genes of the “A” function (APETALA 1 and 2; AP1 and AP2) are expressed and govern sepal development; in the second one, in addition to the
“A” function genes, those of the “B” function (APETALA 3 and PISTILLATA; AP3 and PI) are also expressed and there petals develop; in the third one, the genes of function “B” and that of function
“C” (AGAMOUS; AG) are transcribed leading to anther initiation; and finally, in the fourth whorl, only the gene of the function “C” (AG) is active leading to the formation of carpel (Figure 10).
Figure 9.9. The ABC model of flower organ formation of wild type and the five homeotic flower development mutant Arabidopsis plants forming three classes A, B and C. The ABC mutant classes indicate “functions” required for flower organ development. These
“functions” are carried out by organ identity transcription factors. Combinations (overlapping expression) of these factors define organ identity: A = APETALA1 and 2 = sepals and petals; B = APETALA3 and PISTILLATA = petals and anthers; C = AGAMOUS
= anthers and carpels. “A” and “C” functions restrict each other’s expression. If one is removed the other occupies the whole meristem changing organ identity in the two other whorls. (Figure of A. Fehér)
This model fully explains the phenotypes of the ABC mutants, if one further condition is met (Fig. 9.9):
the “A” and “C” function genes must be antagonistic restricting each other’s expression. If one of them is removed by mutation, the other function extends to the whole meristem.
One may ask the question, how the same meristem identity factors can regulate the various developmental pathways in the four whorls. The answer is that they have different co-factors in each four whorls modifying their target gene set.
9.2.2. The extended ABC model and the quartet model of flower development
If all five genes involved into the ABC model are mutated in a single plant, instead of real flowers only green pseudo-flowers will develop with leaf-like organs in each whorl. This confirms that the flower organs are modified leaves and the flowers are modified shoots. The flower organ identity homeotic
101 transcription factors convert leaf development into flower organ development. One can assume that overexpressing these factors in vegetative leaf primordia according to the rules of the ABC model, the primordia will develop into flower organs. However, experiments showed that it is not the case. Other factors are also required for flower organ morphogenesis. These factors were also identified via the characterization of Arabidopsis flower morphogenesis mutants. Arabidopsis has four SEPALATA (SEP1,2,3 and 4) transcription factors with overlapping functions. If all four SEP gene is mutated in one plant pseudo-flowers develop instead of real ones: the ABC factors without the SEP factors are not enough to drive the morphogenesis of the flower (24). This finding is explained by the “quartet model of flower development” (25). This model states that in whorl a quartet of transcription factors forms a complex that regulates the development of the given organ (Fig. 9.10). The SEP factors are and must be present in each quartet since they keep together the functional complexes. This hypothesis was validated by experiments where the flower organ identity transcription factors were overexpressed in vegetative leaf primordia together with a SEP factor and instead of leaves these primordia developed to flower organs (e.g. petals) (26). The SEP factors were included into the extended ABC model as responsible for the “E” function (the “D” function was earlier used for transcription factors determining ovule identity).
Figure 9.10. The quartet model of flower organ development. In each whorl a quartet of transcription factors determine organ identity. SEPALLATA (SEP) transcription factors are required in each quartet besides the transcription factors of the ABC model (see Fig. 9.9). (Figure of A. Fehér)
9.2.3. The validity of the ABC model
Further studies confirmed that the basic mechanisms of the extended ABC model of Arabidopsis are operating in all investigated flower types (27) (Fig 12). The great variability of the morphology of flowers is due to alterations in the temporal and spatial gene expression pattern, the number and novel functions of the homeotic transcription factors and their target genes. One simple example is tulip.
The tulip flower has no sepals only petals. In its flower meristem, the “B” function genes are expressed in the first three whorls and therefore in the first whorl instead of sepals also petals will develop (Fig.
9. 12). The complex flower structure of orchids is due to the amplification of the “B” function gene AP3. The new AP3 copies have different regional expression patterns in the flower meristem and activate specific target genes regionally defining different sepal and petal types in the two outmost whorls and the fusion of anthers and carpels in the two innermost whorls (Fig. 9.11). In modern roses, the extension of the expression domain of the “A” function in expense of the expression domain pf the
“C” function resulted in more petals instead of anthers. The very different flower type of cereals and grasses can also be explained by a variant of the ABC model.
102 Figure 9.11. Examples for the variations of the ABC model of flower development. Details are discussed in the text. (Figure of A. Fehér)
The AGAMOUS (AG) transcription factor is expressed in the middle of the flower meristem. Beside of its function to regulate anther and carpel development in this region, this factor is responsible for the determinate development of the flower. The WUSCHEL (WUS) homeotic transcription factor
regulates the indeterminate growth of the vegetative shoot meristem maintaining the stem cell pool.
AG switches off WUS expression in the middle of the meristem after the completion of the development of the carpel-producing fourth whorl of the flower.