Goethe was right when he proposed that flowers are modified leaves. It seems that four genes involved in plant development must be expressed together to turn leaves into floral organs.
What controls the difference between a plant's floral organs and its leaves? Over 200 years ago Johann Wolfgang von Goethe proposed that the different parts of a plant result from 'metamorphosis' (meaning transformation) of a basic organ, the 'ideal leaf'. But if floral organs are just modified leaves, what are the modifiers? On page 525 of this issue1 Honma and Goto provide the answer in molecular terms.
A typical flower consists of four different types of organ arranged in four whorls (Fig. 1). There are leaf-like sepals in the outermost whorl; showy petals in the second whorl; stamens (male reproductive organs) in the third whorl; and carpels (female reproductive organs) in the fourth, innermost whorl. But not all flowers develop properly. In certain mutants the identity of some floral organs is changed, a phenomenon known as homeosis. In the model plants thale cress (Arabidopsis thaliana ) and snapdragon (Antirrhinum majus), for example, such homeotic mutants come in three classes, A, B and C. Class A mutants have carpels in the first and stamens in the second whorl; class B mutants have sepals in the second and carpels in the third whorl; and class C mutants have petals in the third and sepals in the fourth whorl2,3. Organ identity in the other whorls is unchanged.
Following genetic analyses of these mutants, simple models were developed to explain how the different floral organs adopt their unique identities during development2,3. The most widely known is the ABC model, in which combinatorial interactions between three classes of floral homeotic genes are affected in the respective mutants. So these genes are termed class A, class B and class C genes, with A specifying sepals, A + B petals, B + C stamens and C carpels3. (Class D genes, specifying ovules, were later added to the ABC model, but they are not considered further here.) The Arabidopsis class A genes are APETALA1 (AP1) and APETALA2 (AP2); the class B genes are APETALA3 (AP3) and PISTILLATA (PI); and the only class C gene is AGAMOUS (AG). Apart from AP2, these genes are all members of the MADS- box family2,3,4 which encode transcription factors — proteins that recognize specific DNA motifs of other genes and influence their transcription.
Combined loss-of-function of class A, B and C genes results in a transformation of all floral organs into leaves, corroborating Goethe's view that leaves are a developmental 'ground state'. But expression of the ABC genes throughout a plant does not transform leaves into floral organs, showing that the ABC genes, though necessary, are not sufficient to superimpose floral organ identity on a leaf developmental programme1,5. So, what other mysterious factors are required to specify floral organ identity?
A telling clue came just a few months ago with the report5 that all flower organs resembled sepals in mutants where three other MADS-box genes — SEPALLATA1 (SEP1), SEP2 and SEP3 — had lost their function. Together with gene expression data, this finding suggested that the SEP genes represent another class of floral homeotic genes, termed class E genes6, which, together with the class B and C genes, is required for the specification of organ identity in the petal (A + B + E), stamen (B + C + E) and carpel (C + E)5,6.
But by what mechanism do these different genes interact? MADS-box proteins bind DNA as dimers, but attempts to explain the interaction between class A, B and C genes by MADS-box protein heterodimerization have failed7. However, there was a twist to the tale with the demonstration8 that some homeotic MADS-box proteins from Antirrhinum form multimeric DNA-binding complexes. Honma and Goto1 now report that Arabidopsis proteins also bind to DNA as multimeric complexes containing the class B proteins AP3 and PI, the class E protein SEP3, and either AP1 (a class A protein) or AG (a class C protein). These are the exact combinations of proteins required to specify petal (A + B + E) or stamen (B + C + E) identity, respectively. The ability of MADS-box proteins to form multimeric complexes may therefore provide the molecular basis for the combinatorial interaction of the floral homeotic genes.
So are the SEP proteins the mysterious factors that, along with the ABC genes, are required to specify floral organ identity? The answer is clearly 'yes'. In genetically engineered plants that express B + (A or E) genes throughout development, Honma and Goto found that leaves are transformed into petal-like organs, and that ubiquitous expression of class B, C and E genes transforms leaves into stamen-like organs.
With these findings1,5, improved successors of the ABC model can be developed. An example is the 'quartet model' which directly links floral organ identity to the action of four different tetrameric transcription factor complexes composed of MADS-box proteins (Fig. 1; for details, see ref. 6). Goals for the future will be to define the exact structures of these transcription-factor complexes inside the living plant cell, to identify the target genes whose transcription is regulated by the binding of the complexes, and to explain the gene specificity of that binding.
The results of Honma and Goto1 also promise progress in answering one of the enduring puzzles of botany: the evolutionary origin of the flower9. The identity of floral organs is totally dependent on the activity of the MADS-type floral homeotic genes, so gene duplication and diversification within the MADS-box gene family must have been key processes in flower evolution4.
The MADS-type floral homeotic genes can be separated into three different gene clades (sets of genes that share a last common ancestor not shared with any of the other MADS-box genes)4,10. From phylogenetic reconstructions it seems that these clades — including the class B, class C + D and class A + E genes, respectively — were established within a relatively short period of time well before the origin of the flowering plants. But once established, these gene clades have changed very little4,10.
Does this unusual pattern of gene evolution reflect the 'invention' of heterotetramer formation and subsequent coevolution of the constituents? Were novel specificities in DNA-binding8 and in the regulation of target genes, generated by the establishment of tetramer formation, required for the specification of more sophisticated reproductive organs, such as flowers or cones? Such questions can now be answered by studying the phylogeny, function and interaction of MADS-box proteins in various groups, including non-flowering plants4,9,10.
It was prescient of Goethe to recognize floral organs as modified leaves. But is there even more to it? In his novel Die Wahlverwandtschaften (The Elective Affinities), Goethe described the rapid establishment of new ways of sexual reproduction when a married couple (a 'dimer') decided to live together with another man and women. By inventing this quartet, did Goethe even anticipate the molecular basis of floral-organ specification?
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Journal of Plant Biology (2018)