Pii: s1369-5266(99)00036-9

Three ways to learn the ABCs
Medard Ng* and Martin F Yanofsky†
The ABC model of flower development represents a milestone carpels. An example of the A gene is APETALA1 (AP1), the in explaining how the fate of emerging floral organ primordia is B genes are APETALA3 (AP3) and PISTILLATA (PI) and specified. This model states that organ identity is specified by the C gene is AGAMOUS (AG) [3–8]. Subsequent cloning of different combinations of the activities of the A, B and C class AP1, AP3, PI and AG show that they are all members of the homeotic genes. In spite of the remarkable simplicity of this MADS-box gene family and are expressed only in regions model, the complex regulatory interactions that establish the of the developing flowers that require their activities initial pattern of A, B and C gene activity have yet to be fully (Figure 1, reviewed in [9]). Although these results explain explained. It has been shown that the LEAFY gene functions their region-specific requirement in specifying floral organ early to promote flower meristem identity, and that it is identities, they also raise the issue of how the floral subsequently required for the normal expression of the ABC homeotic genes are activated in floral meristems, and how genes. Recently, LEAFY has been identified as an immediate they come to be expressed in spatially restricted domains.
upstream regulator of the floral homeotic genes, thus openingup an avenue to examine the transcriptional interactions that In order to address these issues, genes acting upstream of the floral homeotic genes must be identified. The meris-tem identity genes, which include LEAFY (LFY), Addresses
UNUSUAL FLORAL ORGANS (UFO) and AP1, are excel- Department of Biology, University of California at San Diego, La Jolla, lent candidates for such upstream acting genes [3,7,10–14].
Plants carrying mutations in any of the meristem identity genes produce flowers with shoot-like characters, which suggests these genes normally instruct the meristems to Current Opinion in Plant Biology 2000, 3:47–52
adopt a floral fate. As the determination of floral meristemidentity precedes that of floral organ identity, the meristem 1369-5266/00/$ — see front matter 2000 Elsevier Science Ltd. All rights reserved.
identity genes must act upstream of the floral homeoticgenes. LFY encodes a novel transcription factor, whereas Abbreviations
UFO encodes an F-box-containing protein [12,14,15,16••].
LFY, UFO and AP1 are expressed very early during flower FIM
development, consistent with the idea that they can acti- LFY
vate the expression of the floral homeotic genes (Figure 1).
Three recent papers now convincingly show that AP1 and UFO
AG are direct targets of LFY, and that LFY activates AP1,AP3 and AG using different mechanisms [16••–18••].
AG is a direct target of LFY
The Arabidopsis flower is arguably the best understood Mutations in AG result in flowers with third-whorl petals, plant model system pertaining to pattern formation.
and the fourth whorl develops as a new ag mutant flower Flowers originate from small groups of undifferentiated [4]. Transcripts of the C class gene AG can be detected in cells called floral meristems, which, in turn, are derived the center of a wild-type flower from floral stage 3, corre- from the shoot apical meristem (SAM). Similar to most sponding to whorls three and four (Figure 1, [4,19]). The other dicotyledonous plants, an Arabidopsis flower consists first indication that LFY may be critical for AG expression of four types of floral organs arranged in four concentric came from analyzing the expression pattern of AG in strong whorls. Four sepals, four petals, six stamens and two fused lfy mutants, in which the early arising flowers are trans- carpels can be found from the periphery to the center of formed into leaves with associated shoots, whereas the later arising flowers develop bracts in whorl one, lackpetals and stamens, and develop irregularly fused carpels In order to understand how flowers develop into their final in the center [12,20,21]. In the later arising flowers the shape and form, a genetic approach has been used to iden- onset of AG expression is delayed, although AG eventually tify genes that when inactivated will perturb the flower morphology. In this review, we focus on the meristem iden-tity genes and the floral homeotic genes. Analyses of To begin probing into the mechanism by which LFY acti- mutations in the latter class of genes led to the formulation vates AG expression, Parcy et al. [16••] generated a of the ‘ABC’ model of flower development (reviewed in gain-of-function LFY allele, called LFY:VP16, that is consti- [1,2]). According to this model, the A genes specify sepals, tutively active by inserting the transcriptional activation the A and B genes together specify petals, the B and C domain of VP16 into LFY. This experiment aimed to address genes together specify stamens, and the C gene specifies whether the role of LFY in activating floral homeotic genes Growth and development
Expression patterns of some meristem identitygenes and floral organ identity genes thatfunction early in flower development. Theexpressions of the meristem identity genes overlap spatially and temporally with the organidentity genes, consistent with the idea thatthe former acts upstream of the latter.
Numbers indicate floral stages.
could be separated from its earlier role in specifying the iden- This observation is consistent with the fact that ubiquitous tity of floral meristems. It turned out that LFY:VP16 expression of LFY:VP16 in the vegetative tissue also leads transgenic plants have unaltered ability to initiate flowers, to parallel ubiquitous expression of AG.
whereas the flower morphology is clearly affected, implicat-ing LFY in regulating floral homeotic genes.
If LFY:VP16 can activate AG in all tissue types, why doesLFY, which is present throughout the floral meristem from As with all gain-of-function alleles, it is important to show floral stages 1 to 3, normally induce AG only in the center that the LFY:VP16 phenotypes reveal the normal functions of the flower [12,13,16••]? Parcy et al. [16••] have proposed of the endogenous LFY gene. Therefore, Parcy et al. [16••] two models to explain this conundrum. First, a repressor performed two elegant control experiments. First, the activity, such as APETALA2, is present in the periphery of LFY:VP16 phenotypes are enhanced by decreasing the the floral meristem and prevents LFY from activating AG gene dosage of the endogenous LFY, which strongly sug- expression [24]. Second, the repressor activity is selective- gests that LFY:VP16 competes for the same target genes as ly overcome in the center of the stage 3 floral meristem. In the endogenous LFY. Furthermore, LFY:VP16 rescues the either model, regional expression of AG requires LFY, flower initiation defects of lfy mutants. Second, a mutant which provides floral meristem-specific cue, and an unde- LFY:VP16 version (called LFY:mVP16), in which a mutant fined molecule ‘X’, which provides the C-region cue. Parcy VP16 domain that is inactive in transcriptional activation et al. [16••] have suggested further that the VP16 transcrip- was inserted into LFY, fully rescues lfy mutants but does tional activation domain renders the LFY protein not affect floral morphology. These results show that inser- independent of other regulators of AG, leading to the acti- tion of a foreign polypeptide per se does not activate or vation of AG expression throughout the flower.
In a follow-on study, LFY has been shown to activate AG A detailed examination of LFY:VP16 plants shows that expression directly by binding to an enhancer in the first sepals are converted to carpels, and petals to stamens [16••].
intron of AG [17••]. It was previously demonstrated that the In short, they resemble plants constitutively expressing AG first intron of AG is crucial for its expression [25]; Bush et al.
[23]. RNA in situ hybridizations confirm that AG expression [17••] have gone on to show that transcriptional enhancers is ectopic, precocious and at high levels in LFY:VP16 plants.
present in the first intron of AG are sufficient to confer a Three ways to learn the ABCs Ng and Yanofsky 49
wild-type AG expression pattern. They embarked on a ‘tour Wagner et al. [18••] fused the hormone-binding domain of de force’ approach to define the smallest piece of DNA that the rat glucocorticoid receptor to LFY [32]. The chimeric retains full activities of the AG enhancer, and found that protein is expressed constitutively under the control of the two non-overlapping fragments from the intron can confer 35S promoter (35S::LFY-GR). In the absence of glucocor- AG-specific expression. Busch et al. [17••] decided to focus ticoid, LFY-GR should be tethered in the cytoplasm by on the smaller 3′ enhancer because its expression seems to interaction with the chaperon proteins, rendering the tran- be less complex. Further deletions of the 3′ enhancer led to scription factor LFY inactive [18••,32,33•]. Upon progressive reduction of its activity; however, LFY respon- treatment with glucocorticoid, LFY-GR dissociates from siveness could be followed using LFY:VP16. This approach the chaperons, translocates to the nucleus, and regulates defines a LFY responsive element to a 230 bp region. Using target gene expression. As activation of LFY-GR is post- an in vitro DNA-binding assay, two closely spaced LFY translational, the immediate effect of LFY activation on binding sites were identified in the 230 bp fragment of the transcription of any LFY target genes can be monitored in AG intron. To assess the functional significance of these the presence of a protein synthesis inhibitor.
sites in vivo, a small deletion including the LFY bindingsites, and point mutations abolishing LFY binding in vitro The 35S::LFY-GR construct was introduced into strong lfy were introduced into the AG 3′ enhancer. Mutating both mutants. To show that the translational fusion does not binding sites inactivates the enhancer, whereas mutating compromise LFY activity, Wagner et al. [18••] examined one site significantly attenuates the enhancer. Taken the phenotype of these plants upon dexamethasone (a together, these results show that LFY is a direct upstream strong glucocorticoid) treatment. They found that, after such treatment, 35S::LFY-GR mostly rescues the floralmorphology of lfy mutants. In addition, an early flowering AP1 is also a direct target of LFY
phenotype and the shoot-to-flower conversions were AP1 is both a meristem identity gene and an A function observed in these dexamethasone treated plants; there- organ identity gene, as mentioned above. Plants homozy- fore, 35S::LFY-GR has the same activities as 35S::LFY gous for strong ap1 alleles develop bracts in the first floral [18••,29]. To evaluate whether AP1 is a direct target of whorl, usually lack petals, and have secondary flowers in LFY, AP1 expression was analyzed in lfy mutants carrying the axils of the first floral organs [3,7]. AP1 is initially the 35S::LFY-GR transgene treated with dexamethasone expressed throughout the floral meristem from floral stages and cycloheximide. Cycloheximide treatment, which pre- 1 to 3 (Figure 1, [6]). Expression then abates in the two vents protein synthesis, ensures that only genes directly central whorls because of negative regulation by AG [6,26].
activated by LFY are induced upon dexamethasone addi- To explain how AP1 is expressed in the outer two whorls of tion. AP1 RNA could be detected in young flower a mature flower, therefore, one needs to explain how AP1 primordia of these plants eight hours after dexamethasone is initially expressed throughout the floral meristem.
Numerous experiments suggest that AP1 activity is mostly Activation of AP3 by LFY and UFO
downstream of LFY. AP1 expression is significantly Plants carrying mutations in AP3 or PI have sepals in the delayed and reduced in lfy mutants [27•,28•]. Constitutive second and carpels in the third whorl [5,8]. AP3 starts to be expression of LFY (35S::LFY) leads to precocious expres- expressed in the second and third whorls from floral stage sion of AP1 [29]. In addition, ap1 mutants attenuate the 3 (Figure 1, [5]). Whereas the initiation of AP3 expression shoot-to-flower conversion phenotype of the 35S::LFY is unchanged in ap3 and pi mutants, continued expression plants, whereas the gain-of-function phenotype of 35S::AP1 of AP3 after floral stage 6 depends on wild-type activities plants is mostly unaffected by mutations in LFY [27•,29,30]. These observations prompted Parcy et al. [16••]to examine AP1 expression in LFY:VP16 plants, although Several lines of evidence suggest that LFY and UFO are the phenotype of these plants suggests no a priory reason key upstream regulators of AP3. Flowers from strong lfy for altered AP1 expression. They found that the level of and ufo mutants lack petals and stamens [12–14,20,21]; early AP1 expression is greatly elevated, although its early AP3 expression is significantly reduced in strong lfy and ufo pattern of expression is unaltered. In vitro DNA-binding mutants [13,22]; and constitutive expression of AP3 and PI assays showed that a high-affinity LFY binding site is pre- partially restores stamens and petals in lfy and ufo mutants, sent in the AP1 promoter [16••,17••]. Although this site is whereas constitutive expression of UFO does not rescue present in a minimal AP1 promoter, its in vivo function is ap3 and pi mutants [15,35].
unknown [31]. Consistent with the idea that AP1 expres-sion is directly regulated by LFY, LFY:VP16 activates the Consistent with its upstream regulatory role, UFO RNA expression of a reporter gene in yeast under the control of accumulates in the floral meristem before the onset of AP3 an AP1 promoter containing the LFY binding site [16••].
expression [15,36]. UFO is first expressed in the centraldome, including the presumptive third and fourth whorls, Another recent study provides evidence that LFY is a during floral stage 2 (Figure 1, [15]). During floral stage 3, direct transcriptional activator of AP1 in vivo [18••].
its expression domain broadens, with the concomitant loss Growth and development
of UFO RNA in the center. During late floral stage 3, UFO identified, therefore, one might also start looking for LFY- RNA can be detected in the second and third whorls, sim- binding sites in the AP3 promoter [38•,39•].
ilar to the AP3 expression domain at the same stage.
During floral stage 4, the UFO domain becomes mainly As UFO is not a transcription factor, it is unlikely to direct- restricted to the petal primordia. From embryonic to repro- ly activate AP3 transcription. Analyses of the Antirrhinum ductive phases of development, UFO is also expressed at UFO orthologue FIMBRIATA (FIM) provide good insights high levels at the periphery and at low levels at the center into how UFO may function [40]. Antirrhinum proteins with strong similarity to Skp1 from yeast and animals have beenshown to interact with FIM [40]. In yeast and humans, How do LFY and UFO activate AP3 expression? Clearly, Skp1 proteins interact with F-box containing proteins to the simple hierarchical models of UFO acting downstream form a complex targeted for degradation, which is required of LFY and LFY acting downstream of UFO are incorrect.
for cell cycle progression [41–43]. Furthermore, it has also This is because constitutive expression of UFO fails to res- been shown that an F-box protein, E3RSIκB, targets IκB, a cue lfy mutants, and, conversely, constitutive expression of repressor of the transcription factor NK-κB, for ubiquitin- LFY does not rescue ufo mutants [15,29]. Plants doubly proteasome-mediated degradation [44]. On the basis of transgenic for 35S::LFY and 35S::UFO have ubiquitous these results, it is tempting to speculate that a protein com- expression of AP3 throughout the developmentally arrest- plex formed by UFO and the Arabidopsis Skp1-like ed seedings [16••]. In contrast, AP3 cannot be detected in proteins might act by promoting degradation of a tran- seedlings expressing either LFY or UFO. On the basis of scriptional repressor of AP3. The absence of the repressor these results, Parcy et al. [16••] have suggested that during in the second and third whorls, and the presence of the normal development the expression domain of AP3 is activator LFY throughout the floral meristem may be nec- defined by LFY, which is expressed throughout the devel- essary for spatially restricted AP3 expression.
oping flower, and UFO, which is expressed in the emergingpetal and stamen primordia. In this context, LFY provides Conclusions
the floral meristem specificity and UFO provides the While significant progress has been made toward elucidat- regional specificity for AP3 expression, analogous to the ing how the floral homeotic genes are expressed in spatially proposal that LFY and the unknown factor ‘X’ activate AG restricted patterns, our understanding of the transcriptional expression in the center of the flower.
regulation of these genes is clearly incomplete. We nowknow that the LFY meristem identity gene directly acti- Although this model provides a good framework for AP3 vates AP1 and AG, and perhaps AP3, although these studies activation, some results cannot be easily reconciled with it.
indicate that additional factors (e.g., UFO, factor ‘X’) must Much evidence has shown that co-expression of LFY and also interact with LFY in this process. We also know that UFO is not sufficient for AP3 expression. First, the shoot many other genes are involved in regulating the ABC apex of 35S::LFY plants, which expresses endogenous genes, including AP1, AP2, CAULIFLOWER, CURLY UFO, does not express AP3 [16••]; similarly, AP3 cannot be LEAF, SUPERMAN and LEUNIG, although their mecha- detected in the shoot apex of plants expressing LFY under nistic roles have yet to be clearly defined [7,22,45–50].
the control of UFO promoter [15]. Second, constitutive Given the long-term goal of elucidating the cascade of tar- expression of UFO fails to initiate AP3 expression during get gene regulation beginning in the floral meristem with floral stage 1 of the floral primordia, which express high genes such as LFY, and ending with fully differentiated flo- levels of LFY [15]. These observations led Lee et al. [15] ral organs, it is clear that we are only scratching the surface to propose that induction of AP3 expression by UFO and of what promises to be a very deep and interesting story.
LFY is dependent on additional factors. It should beemphasized that the model proposed by Parcy et al. [16••] Acknowledgements
is not necessarily rejected by the results described above.
We thank François Parcy and Detlef Weigel for comments. MN received along-term post-doctorate fellowship from The Human Frontier Science For example, high levels of both LFY and UFO may be Program Organization (LT-367/97). Research in the laboratory of MFY is required for AP3 expression, and this condition may be supported by grants from the National Science Foundation and the achieved only in seedlings expressing LFY and UFO under the control of the 35S promoter, and in wild-type flowers.
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