22.3 Genes Control the Development of Flowers in Plants

We have now examined in detail pattern formation in Drosophila, which serves as a model system of development. Another model system that has provided important insight into how genes influence patterns of growth and development is the formation of flower parts in angiosperms.

One of the most important developmental events in the life of a plant is the switch from vegetative growth to flowering. The precise timing of this switch is affected by season, day length, plant size, and a number of other factors and is under the control of a large number of different genes. The development of the flower itself also is under genetic control, and homeotic genes play a crucial role in the determination of the floral structures.

Flower Anatomy

A flower is made up of four concentric rings of modified leaves, called whorls. The outermost whorl (whorl 1) consists of the green leaflike sepals. The next whorl (whorl 2) consists of the petals, which typically lack chlorophyll. Whorl 3 consists of the stamens, which bear pollen, and whorl 4 consists of carpels that are often fused to form the stigma bearing the ovules. In wild-type Arabidopsis, a model genetic plant (see the Reference Guide to Model Genetic Organisms and Figure 22.14), there are four sepals, four white petals, six stamens (four long and two short), and two carpels (Figure 22.15a).

Figure 22.14: The flower produced by Arabidopsis thaliana has four sepals, four white petals, six stamens, and two carpels.
[Darwin Dale/Photo Researchers,Inc.]
Figure 22.15: Analysis of homeotic mutants in Arabidopsis thaliana led to an understanding of the genes that determine floral structures in plants.

Genetic Control of Flower Development

Elliot Meyerowitz and his colleagues conducted a series of experiments to examine the genetic basis of flower development in Arabidopsis. They began by isolating and analyzing homeotic mutations in Arabidopsis. Homeotic mutations were actually first identified in plants, in 1894, when William Bateson noticed that the floral parts of plants occasionally appeared in the wrong place: he found, for example, flowers in which stamens grew in the place where petals normally grow.

Meyerowitz and his coworkers used these types of mutants to reveal the genes that control flower development. They were able to place the homeotic mutations that they isolated into three groups on the basis of their effect on floral structure. Class A mutants had carpels instead of sepals in the first whorl and stamens instead of petals in the second whorl (Figure 22.15b). The third whorl consisted of stamens, and the fourth whorl consisted of carpels, the normal pattern. Class B mutants had sepals in the first and second whorls and carpels in the third and fourth whorls (Figure 22.15c). The final group, class C mutants, had sepals and petals in the first and second whorls, respectively, as is normal, but had petals in the third whorl and sepals in the fourth whorl (Figure 22.15d)

Meyerowitz and his colleagues concluded that each class of mutants was missing the product of a gene or the products of a set of genes that are critical to proper flower development: class A mutants were missing gene A activity, class B mutants were missing gene B activity, and class C mutants were missing gene C activity. They hypothesized that the class A genes are active in the first and second whorls. Class A gene products alone cause the first whorl to differentiate into sepals, and together with class B gene products they cause the second whorl to develop into petals. Class C gene products together with Class B gene products induce the third whorl to develop into stamens. Class C genes alone cause the fourth whorl to become carpels. The products of the different gene classes and their effects are summarized in the conclusion of Figure 22.15.

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To explain the results, they also proposed that the genes of some classes affect the activities of others. Where class A is active, class C is repressed, and where class C is active, class A is repressed. Additionally, if a mutation inactivates A, then C becomes active and vice versa. Class A genes are normally expressed in whorls 1 and 2, class B genes are expressed in whorls 2 and 3, and class C genes are expressed in whorls 3 and 4 (Figure 22.16).

Figure 22.16: Expression of class A, B, and C genes varies among the structures of a flower.

The interaction of these three classes of genes explains the different classes of mutants in Figure 22.15. For example, class A mutants are lacking class A gene products, and therefore class C genes are active in all tissues because when A is inactivated C becomes active. Therefore whorl 1, with only class C gene products, will consist of carpels; whorl 2, with class C and class B gene products, will produce stamens; whorl 3, with class B and class C gene products, will produce stamens; and whorl 4, with only class C gene activity, will produce carpels (see Figure 22.15b):

Class C (in the absence of class A) gene products → carpels (1st whorl)
Class B + class C (in the absence of class A) gene products → stamens (2nd whorl)
Class B + class C gene products → stamens (3rd whorl)
Class C gene products → carpels (4th whorl)

To confirm this explanation, Meyerowitz and his colleagues bred double and triple mutants and predicted the outcome. The resulting flower structures fit their predictions. In subsequent studies, they isolated the genes of each class. There are two class A genes, termed APETALA1 (AP1) and APETALA2 (AP2); two class B genes, termed APETALA3 (AP3) and PISTILLATA (PI); and one class C gene termed AGAMOUS (AG). The cloning and sequencing of these genes revealed that all are MADS-box genes—genes that function as transcription factors and affect the expression of other genes. MADS-box genes in plants play a similar role to that of homeobox genes in animals, although MADS-box genes and homeobox genes are not homologous.

The results of other studies have demonstrated the presence of an additional group of genes called SEPALLATA (SEP) that are expressed in whorls 2, 3, and 4, and they, too, are required for normal floral development. If the SEP genes are defective, the flower consists entirely of sepals. Findings from studies of other species have demonstrated that this system of flower development exists not only in Arabidopsis but also in other flowering plants. It is important to note that these genes are necessary but not sufficient for proper flower development; other genes also take part in the identity of the different parts of flowers. TRY PROBLEM 25

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CONCEPTS

Plant homeotic genes control the development of floral structures in plants. The products of three classes of homeotic genes interact to determine the formation of the four whorls that constitute a complete flower.

CONCEPT CHECK 5

What types of flower structures would you expect to see in whorls 1 through 4 of a mutant plant that failed to produce both class A and class B gene products?

  1. Carpels, stamens, stamens, carpels.
  2. Sepals, sepals, carpels, carpels.
  3. Sepals, sepals, sepals, sepals.
  4. Carpels, carpels, carpels, carpels.

CONNECTING CONCEPTS: Comparison of Development in [em]Drosophila[/em] and Flowers

We have now considered two very different model systems of development: the formation of body form and pattern in fruit flies and the development of flower structures in angiosperms. In spite of their differences, these two systems exhibit similarities in how genes control development.

First, both pattern formation in Drosophila and flower development in plants are controlled by numerous genes that interact in complex ways. For example, we saw in Drosophila how a large complex of genes successively defines smaller and smaller regions of the fruit fly embryo and how genes at one level stimulate and inhibit genes at other levels. Similarly, flower development is controlled by class A, class B, and class C genes. The action of each class depends on which products of other classes are present, and the individual genes of each class interact in complex ways to control the differentiation of each whorl of a flower.

Another common feature of development in fruit flies and flowers is that many of the genes involved in these processes function by influencing the expression of other genes. In both fruit flies and flowers there is a cascade of development, in which gene products stimulate other genes, which in turn stimulate yet other genes. Many of the gene products are regulatory proteins that bind to DNA and affect the transcription of other genes. For example, Hox genes in Drosophila and MADS-box genes in flowers encode transcription factors that play an important role in development.

A final similarity is that each system contains homeotic genes, which define the identity of particular structures or segments. Mutation of these homeotic genes produces structures that are in the wrong place, such as legs where antennas are normally found in fruit flies or carpels where sepals usually occur in flowers.