Cell, Vol. 78, 203-209, July 29, 1994, Copyright 0 1994 by Cell Press The ABCs of Floral Homeotic Genes Review Detlef Weigel* and Elliot M. Meyerowltzt *Salk Institute for Biological Studies Plant Biology Laboratory 10010 North Torrey Pines Road La Jolla, California 92037 Zalifornia Institute of Technology Division of Biology 158-29 Pasadena, California 91125 Homeotic mutants, that is, mutants with a normal organ in a place where an organ of another type is typically found, were first recognized in plants. The earliest descriptions of mutants in which petals replace stamens, giving doubleflow- ers, go back to ancient Greece and Rome. Similar accounts can be found in the botanical literature of China more than a thousand years ago, and in the books of the herbalists of Renaissance Europe (Meyerowitz et al., 1989). The use of such mutants (and similar but noninherited developmental abnormalities) to understand developmental processes in plants is more recent, dating from Linnaeus in the mid- eighteenth century(seeCullen and Stevens, 1990), and from Goethe (1790), who derived the ideas of organ homology and homological comparison from plants showing what was then called abnormal metamorphosis. Our term homeosis dates from Bateson’s work (1894) on organismal variation, in which he expanded Masters’treatment (1889) of abnormal metamorphosis in plants to animals and introduced the term homoeosis as a replacement for the older term. Goethe (1790) used homeotic variation in plants as the basis for a specific model explaining the developmental origin of differ- ent organ types in flowers. In his view, the four types of floral organs (sepals, petals, stamens, and carpels) are all modified leaves. As sap rises through developing flowers it is progressively refined, thereby inducing different organ types in different positions. Present Models for Flower Development Present models of floral organ identity, which are mecha- nistically quite different from those of Goethe, also derive from consideration of homeotic abnormalities. Mutations causing such abnormalities have been especially well studied in two species, the small crucifer Arabidopsis thali- anaand the distantly related snapdragon, Antirrhinum ma- jus. Wild-type flowers of Arabidopsis and snapdragon comprise four concentrically arranged whorls of organs in the sequence sepals, petals, stamens, and carpels, from outermost to innermost whorl. Figure 1 shows the disposi- tion of the four types of organs in an Arabidopsis flower. Many mutations in Arabidopsis and snapdragon change this arrangement of floral organs, and the corresponding wild-type genes have been found to be required for one or more of three different functions: they can directly control organ identity, presumably by activating the downstream genes that are characteristic of the cells of each organ type; they can be spatial regulators of the genes that con- trol organ identity; or they can be necessary for the initial induction of the genes that specify organ identity. Genes with the first activity are organ identity genes, whose func- tion is equivalent to that of homeotic selector genes in animals. Genes with the second type of action are called cadastral genes, because they set the boundaries for or- gan identity genes by preventing their ectopic expression. Genes that are positive inducers of organ identity genes are called meristem identity genes, because the absence of their activity usually causes partial or complete conver- sion of flowers into shoots. Organ identity mutations of Arabidopsis and snap- dragon fall into three separate classes, each of which al- ters organ identity in two adjacent whorls. That mutations affecting the same set of whorls cause similar organ trans- formations has led to the proposal that the three classes of genes reflect three classes of organ identity function, A, B, and C. Complete loss of A function causes transfor- mation of first-whorl sepals into carpels, and of second- whorl petals into stamens. In 6 loss-of-function mutants, sepals replace second-whorl petals, and third-whorl sta- mens are transformed into carpels. Finally, loss of C activ- ity transforms third-whorl stamens into petals, and fourth- whorl carpels into sepals (Figure 1; Table 1). The study of double mutants revealed that class B activ- ity is independent of A and C, but that A activity is ectopi- tally present in class C mutants and viceversa. Combining this observation with the activity domains as deduced from single mutant phenotypes led to the ABC model (Bowman et al., 1991 b; Coen and Meyerowitz, 1991; Meyerowitz et al., 1991) outlined in Figure 1. First, each whorl of a wild- type flower contains a unique combination of either one or two of the three organ identity activities, and these activi- ties combinatorially specify organ identity, with A activity specifying sepals, A and B activities leading to petals, B and C activities together giving stamens, and C activity specifying carpels. Second, A and C activities mutually repress each other; that is, at least some of the genes subserving A and C activity are cadastral as well as organ identity genes. Third, the effects of organ identity activities are independent of their relative position within the flower. With these three premises, all single- and double-mutant combinations can be explained (Figure 1). For example, in an AB double mutant, C activity alone is present in all four whorls, dictating development of carpels in all whorls (Bowman et al., 1991 b). The ABC model left at least one complication, though: what happens in the absence of all organ identity activity? Goethe (1790) had proposed that floral organs represent modified leaves, suggesting that a vegetative leaf is the ground state of floral organs. This has been confirmed by double and triple mutants. The ABC model predicts the absence of any organ identity activity in whorls 1 and 4 in AC double mutants, and, indeed, organs in these two whorls are very much like vegetative leaves- they develop with stipules, are green and covered by branched hairs, and senesce slowly, all characteristics of leaves but not of floral organs (Bowman et al., 1991 b). In triple mutants