TheABC model of flower development is ascientific model of the process by whichflowering plants produce a pattern ofgene expression inmeristems that leads to the appearance of an organ oriented towardssexual reproduction, a flower. There are threephysiological 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 theapical meristem's function from a vegetative meristem into a floral meristem orinflorescence; and finally the growth of the flower's individual organs. The latter phase has been modelled using theABC model, which aims to describe the biological basis of the process from the perspective ofmolecular anddevelopmental genetics.
An externalstimulus is required in order to trigger thedifferentiation of the meristem into a flower meristem. This stimulus will activatemitotic cell division in the apical meristem, particularly on its sides where newprimordia are formed. This same stimulus will also cause the meristem to follow adevelopmental 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 ofstem elongation among the successivewhorls or verticils of the primordium. These verticils follow an acropetal development, giving rise tosepals,petals,stamens andcarpels. Another difference from vegetative axillary meristems is that the floral meristem is "determined", which means that, once differentiated, its cells will no longerdivide.[1]
The identity of the organs present in the four floral verticils is a consequence of the interaction of at least three types ofgene 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 theperianth 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'sfoliar 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 erklären").[2] where Goethe wrote:
"...we may equally well say that a stamen is a contracted petal, as that a petal is a stamen in a state of expansion; or that a sepal is a contracted stem leaf approaching a certain stage of refinement, as that a stem leaf is a sepal expanded by the influx of cruder saps".[3]
Thetransition from thevegetative phase to areproductive 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 producesdescendants. 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. Thismorphogenetic change contains both endogenous and exogenous elements: For example, in order for the change to be initiated the plant must have a certain number ofleaves and contain a certain level of totalbiomass. Certain environmental conditions are also required such as a characteristicphotoperiod.Plant hormones play an important part in the process, with thegibberellins having a particularly important role.[4]
There are manysignals that regulate themolecular biology of the process. The following three genes inArabidopsis thaliana possess both common and independent functions in floral transition:FLOWERING LOCUS T (FT),LEAFY (LFY),SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1, also calledAGAMOUS-LIKE20).[5]SOC1 is aMADS-box-type gene, which integrates responses to photoperiod,vernalization and gibberellins.[4]
Themeristem can be defined as the tissue or group of plant tissues that contain undifferentiatedstem cells, which are capable of producing any type of cell tissue. Their maintenance and development, both in the vegetative meristem or the meristem of the inflorescence is controlled by geneticcell fate determination mechanisms. This means that a number of genes will directly regulate, for example, the maintenance of the stem cell's characteristics (geneWUSCHEL orWUS), and others will act vianegative feedback mechanisms in order to inhibit a characteristic (geneCLAVATA orCLV). In this way both mechanisms give rise to afeedback loop, which along with other elements lend a great deal of robustness to the system.[6] Along with theWUS gene theSHOOTMERISTEMLESS (STM) gene also represses the differentiation of the meristematic dome. This gene acts by inhibiting the possibledifferentiation of the stem cells but still allowscell division in the daughter cells, which, had they been allowed to differentiate, would have given rise to distinct organs.[7]
A flower's anatomy, as defined by the presence of a series of organs (sepals, petals, stamens and carpels) positioned according to a given pattern, facilitatesexual reproduction inflowering plants. The flower arises from the activity of three classes of genes, which regulate floral development:[8]
The ABC model of flower development was first formulated by George Haughn and Chris Somerville in 1988.[9] It was first used as a model to describe the collection of genetic mechanisms that establish floral organ identity in theRosids, as exemplified byArabidopsis thaliana, and theAsterids, as demonstrated byAntirrhinum majus. Both species have four verticils (sepals, petals, stamens and carpels), which are defined by the differential expression of a number ofhomeotic genes present in each verticil. This means that the sepals are solely characterized by the expression of A genes, while the petals are characterized by the co-expression of A and B genes. The B and C genes establish the identity of the stamens and the carpels only require C genes to be active. Type A and C genes are reciprocally antagonistic.[10]
The fact that these homeotic genes determine an organ's identity becomes evident when a gene that represents a particular function, for example the A gene, is not expressed. InArabidopsis this loss results in a flower which is composed of one verticil of carpels, another containing stamens and another of carpels.[10] This method for studying gene function usesreverse genetics techniques to produce transgenic plants that contain a mechanism forgene silencing throughRNA interference. In other studies, usingforward genetics techniques such asgenetic mapping, it is the analysis of thephenotypes of flowers with structural anomalies that leads to thecloning of the gene of interest. The flowers may possess a non-functional orover expressedallele for the gene being studied.[11]
The existence of two supplementary functions, D and E, have also been proposed in addition to the A, B and C functions already discussed. Function D specifies the identity of theovule, as a separate reproductive function from the development of the carpels, which occurs after their determination.[12] Function E relates to a physiological requirement that is a characteristic of all floral verticils, although, it was initially described as necessary for the development of the three innermost verticils (Function Esensu stricto).[13] However, its broader definition (sensu lato) suggests that it is required in the four verticils.[14] Therefore, when Function D is lost the structure of the ovules becomes similar to that of leaves and when Function E is lostsensu stricto, the floral organs of the three outer most verticils are transformed into sepals,[13] while on losing Function Esensu lato, all the verticils are similar to leaves.[14] Thegene products of genes with D and E functions are also MADS-box genes.[15]
The methodology for studying flower development involves two steps. Firstly, the identification of the exact genes required for determining the identity of the floral meristem. InA. thaliana these include APETALA1 (AP1) and LEAFY (LFY). Secondly, genetic analysis is carried out on the aberrantphenotypes for the relative characteristics of the flowers, which allows the characterization of thehomeotic genes implicated in the process.[citation needed]
There are a great manymutations that affect floralmorphology, although the analysis of these mutants is a recent development. Supporting evidence for the existence of these mutations comes from the fact that a large number affect the identity of floral organs. For example, some organs develop in a location where others should develop. This is calledhomeotic mutation, which is analogous toHOX gene mutations found inDrosophila. InArabidopsis andAntirrhinum, the two taxa on which models are based, these mutations always affect adjacent verticils.[citation needed]
This allows the characterization of three classes of mutation, according to which verticils are affected:
Cloning studies have been carried out onDNA in the genes associated with the affected homeotic functions in the mutants discussed above. These studies usedserial analysis of gene expression throughout floral development to show patterns of tissue expression, which, in general, correspond with the predictions of the ABC model.[citation needed]
The nature of these genes corresponds to that oftranscription factors, which, as expected, have analogous structures to a group of factors contained inyeasts andanimal cells. This group is called MADS, which is an acronym for the different factors contained in the group. These MADS factors have been detected in all the vegetable species studied, although the involvement of other elements involved in theregulation of gene expression cannot be discounted.[8]
InA. thaliana, function A is mainly represented by two genesAPETALA1 (AP1) andAPETALA2 (AP2)[16]AP1 is a MADS-box type gene, whileAP2 belongs to the family of genes that contains AP2, which it gives its name to and which consists oftranscription factors that are only found in plants.[17] AP2 has also been shown to complex with the co-repressor TOPLESS (TPL) in developing floral buds to repress the C-class geneAGAMOUS (AG).[18] However,AP2 is not expressed in the shoot apical meristem (SAM), which contains the latent stem cell population throughout the adult life ofArabidopsis, and so it is speculated that TPL works with some other A-class gene in the SAM to repressAG.[18]AP1 functions as a type A gene, both in controlling the identity of sepals and petals, and it also acts in thefloral meristem.AP2 not only functions in the first two verticils, but also in the remaining two, in developing ovules and even in leaves. It is also likely thatpost-transcriptional regulation exists, which controls its A function, or even that it has other purposes in the determination of organ identity independent of that mentioned here.[17]
InAntirrhinum, theorthologous gene toAP1 isSQUAMOSA (SQUA), which also has a particular impact on the floral meristem. The homologs forAP2 areLIPLESS1 (LIP1) andLIPLESS2 (LIP2), which have a redundant function and are of special interest in the development of sepals, petals and ovules.[19]
A total of three genes have been isolated fromPetunia hybrida that are similar toAP2:P. hybrida APETALA2A (PhAP2A),PhAP2B andPhAP2C.PhAP2A is, to a large degree, homologous with theAP2 gene ofArabidopsis, both in its sequence and in its expression pattern, which suggests that the two genes are orthologs. The proteinsPhAP2B andPhAP2C, on the other hand, are slightly different, even though they belong to the family of transcription factors that are similar toAP2. In addition they are expressed in different ways, although they are very similar in comparison withPhAP2A. In fact, the mutants for these genes do not show the usual phenotype, that of thenull alleles of A genes.[20] A true A-function gene has not been found in Petunia; though a part of the A-function (the inhibition of the C in the outer two whorls) has been largely attributed to miRNA169 (colloquially called BLIND)[citation needed]
InA. thaliana the type-B function mainly arises from two genes,APETALA3 (AP3) andPISTILLATA (PI), both of which are MADS-box genes. A mutation of either of these genes causes the homeotic conversion of petals into sepals and of stamens into carpels.[21] This also occurs in its orthologs inA. majus, which areDEFICIENS (DEF) andGLOBOSA (GLO) respectively.[22] For both species the active form of binding with DNA is that derived from the heterodimer: AP3 and PI, or DEF and GLO,dimerize. This is the form in which they are able to function.[23]
TheGLO/PI lines that have been duplicated inPetunia containP. hybrida GLOBOSA1 (PhGLO1, also calledFBP1) and alsoPhGLO2 (also calledPMADS2 orFBP3). For the functional elements equivalent toAP3/DEF inPetunia there is both a gene that possesses a relatively similar sequence, calledPhDEF and there is also an atypical B function gene called PhTM6.Phylogenetic studies have placed the first three within the «euAP3» lineage, while PhTM6 belongs to that of «paleoAP3».[24] It is worth pointing out that, in terms of evolutionary history, the appearance of the euAP3 line seems to be related with the emergence ofdicotyledons, as representatives of euAP3-type B function genes are present in dicotyledons while paleoAP3 genes are present in monocotyledons and basal angiosperms, among others.[25]
As discussed above, the floral organs of eudicotyledonous angiosperms are arranged in 4 different verticils, containing the sepals, petals, stamen and carpels. The ABC model states that the identity of these organs is determined by the homeotic genes A, A+B, B+C and C, respectively. In contrast with the sepal and petal verticils of the eudicots, the perigone of many plants of the familyLiliaceae have two nearly identical external petaloid verticils (thetepals). In order to explain the floral morphology of the Liliaceae, van Tunenet al. proposed a modified ABC model in 1993. This model suggests that class B genes are not only expressed in verticils 2 and 3, but also in 1. It therefore follows that the organs of verticils 1 and 2 express class A and B genes and this is how they have a petaloid structure. This theoretical model has been experimentally proven through the cloning and characterization of homologs of theAntirrhinum genesGLOBOSA andDEFICIENS in a Liliaceae, thetulipTulipa gesneriana. These genes are expressed in verticils 1,2 and 3.[26]The homologsGLOBOSA andDEFICIENS have also been isolated and characterized inAgapanthus praecox ssp.orientalis (Agapanthaceae), which is phylogenetically distant from the model organisms. In this study the genes were calledApGLO andApDEF, respectively. Both containopen reading frames that code for proteins with 210 to 214amino acids. Phylogenetic analysis of these sequences indicated that they belong to B gene family of themonocotyledons.In situ hybridization studies revealed that both sequences are expressed in verticil 1 as well as in 2 and 3. When taken together, these observations show that the floral development mechanism ofAgapanthus also follows the modified ABC model.[27]
InA. thaliana, the C function is derived from one MADS-box type gene calledAGAMOUS (AG), which intervenes both in the establishment of stamen and carpel identity as well as in the determination of the floral meristem.[16] Therefore, theAG mutants are devoid ofandroecium andgynoecium and they have petals and sepals in their place. In addition, the growth in the centre of the flower is undifferentiated, therefore the petals and sepals grow in repetitive verticils.[citation needed]
ThePLENA (PLE) gene is present inA. majus, in place of theAG gene, although it is not an ortholog. However, theFARINELLI (FAR) gene is an ortholog, which is specific to the development of theanthers and the maturation ofpollen.[28]
InPetunia,Antirrhinum and inmaize the C function is controlled by a number of genes that act in the same manner. The genes that are closer homologs ofAG inPetunia arepMADS3 andfloral-binding protein 6 (FBP6).[28]
The D function genes were discovered in 1995. These genes are MADS-box proteins and they have a function that is distinct from those previously described, although they have a certain homology with C function genes. These genes are calledFLORAL BINDING PROTEIN7 (FBP7) andFLORAL BINDING PROTEIN1L (FBP1l).[12] It was found that, inPetunia, they are involved in the development of the ovule. Equivalent genes were later found inArabidopsis,[29] where they are also involved in controlling the development of carpels and the ovule and even with structures related toseed dispersal.
The appearance of interesting phenotypes inRNA interference studies inPetunia andtomato led, in 1994, to the definition of a new type of function in the floral development model. The E function was initially thought to be only involved in the development of the three innermost verticils, however, subsequent work found that its expression was required in all the floral verticils.[13]
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