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 ). 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••]. AG AP LFY, UFO and AP1 are expressed very early during flower
development, consistent with the idea that they can acti-
vate the expression of the floral homeotic genes (Figure 1). PI
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••]. Introduction 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
. 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 . 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 ; Bush et al.
. 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 . 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, ). 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 . In addition, ap1 mutants attenuate the
3 (Figure 1, ). 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 . 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, ). 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 . Antirrhinum proteins with
strong similarity to Skp1 from yeast and animals have beenshown to interact with FIM . 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 . 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
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, CURLYUFO, 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 . 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 . These observations led Lee et al. 
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••]
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. References and recommended reading
At present, it is unclear whether LFY directly activates AP3
Papers of particular interest, published within the annual period of review,
transcription. However, it should be very straightforward to
address this issue by analyzing the lfy 35S::LFY-GR plants. If
these plants carry an AP3::GUS reporter gene, they will stainpositive for GUS activity after dexamethasone treatment
Coen ES, Meyerowitz EM: The war of the whorls: genetic interactions controlling flower development. Nature 1991, 353:31-37.
[18••], and, if AP3 is a direct target of LFY, then AP3 and
Weigel D, Meyerowitz E: The ABCs of floral homeotic genes. Cell GUS RNA should be detected in these plants after treatment
with dexamethasone and cycloheximide. Regulatory ele-
Irish VF, Sussex IM: Function of the apetala1-1 gene during
ments crucial for AP3 expression are beginning to be
Arabidopsis floral development. Plant Cell 1990, 2:741-751. Three ways to learn the ABCs Ng and Yanofsky 51
Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz
25. Sieburth LE, Meyerowitz EM: Molecular dissection of the
EM: The protein encoded by the Arabidopsis homeotic gene AGAMOUS control region shows that cis elements for spatial agamous resembles transcription factors. Nature 1990, 346:35-39. regulation are located intragenically. Plant Cell 1997, 9:355-365.
Jack T, Brockman LL, Meyerowitz EM: The homeotic gene
26. Gustafson-Brown C, Savidge B, Yanofsky MF: Regulation of the APETALA3 of Arabidopsis thaliana encodes a MADS box and is Arabidopsis floral homeotic gene APETALA1. Cell 1994, 76:131-143. expressed in petals and stamens. Cell 1992, 68:683-697.
Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS,
Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF: Molecular
Yanofsky MF: Interactions among APETALA1, LEAFY, and characterization of the Arabidopsis floral homeotic gene TERMINAL FLOWER1 specify meristem fate. Plant Cell 1999, APETALA1. Nature 1992, 360:273-277. 11:1007-1018.
Interactions among APETALA1, LEAFY and TERMINAL FLOWER1 are
Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR: Control
described in this paper. The authors show that AP1 can activate LFY expres-
of flower development in Arabidopsis thaliana by APETALA1 and
sion, and vice versa. By contrast, AP1 and TFL1 negatively regulate each
interacting genes. Development 1993, 119:721-743.
other’s expression. It is concluded that these interactions contribute to thesharp transition that occurs from vegetative to reproductive growth phases.
Goto K, Meyerowitz EM: Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 1993, 8:1548-1560.
28. Ratcliffe OJ, Bradley DJ, Coen ES: Separation of shoot and floral identity in Arabidopsis. Development 1999, 126:1109-1120.
Riechmann JL, Meyerowitz EM: MADS domain proteins in plant
This paper describes the hierarchy among several genes (APETALA1, CAU-development. Biol Chem 1997, 378:1079-1101. LIFLOWER, LEAFY and TERMINAL FLOWER 1) which affect the shootmeristems and floral meristems identities. The meristem identity genes (AP1,
10. Schultz EA, Haughn GW: LEAFY, a homeotic gene that regulates CAL and LFY) prevent TFL1 transcription in the floral meristems; converse-
inflorescence development in Arabidopsis. Plant Cell 1991,
ly, TFL1 delays the upregulation of the meristem identity genes, and prevents
the shoot meristems from responding to LFY and AP1. The authors con-
11. Huala E, Sussex IM: LEAFY interacts with floral homeotic genes to
clude that the relative timing of upregulating TFL1 and the meristem identity
regulate Arabidopsis floral development. Plant Cell 1992, 4:901-913.
genes determine their final expression patterns.
12. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM: LEAFY
29. Weigel D, Nilsson O: A developmental switch sufficient for flower controls floral meristem identity in Arabidopsis. Cell 1992, initiation in diverse plants. Nature 1995, 377:495-500. 69:843-859.
30. Mandel MA, Yanofsky MF: A gene triggering flower formation in Arabidopsis. Nature 1995, 377:522-524.
13. Levin JZ, Meyerowitz EM: UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell
31. Hempel FD, Weigel D, Mandel MA, Ditta G, Zambryski PC,
Feldman L, Yanofsky MF: Floral determination and expression of floral regulatory genes in Arabidopsis. Development 1997,
14. Wilkinson MD, Haughn GW: UNUSUAL FLORAL ORGANS controls 124:3845-3853. meristem identity and organ primordia fate in Arabidopsis. Plant Cell 1995, 7:1485-1499.
32. Lloyd AM, Schena M, Walbot V, Davis RW: Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid-
15. Lee I, Wolfe DS, Nilsson O, Weigel D: A LEAFY co-regulator inducible regulator. Science 1994, 266:436-439. encoded by UNUSUAL FLORAL ORGANS. Curr Biol 1997, 7:95-104.
33. Sablowski RWM, Meyerowitz EM: A homolog of NO APICAL
16. Parcy F, Nilsson O, Busch MA, Lee I, Weigel D: A genetic framework MERISTEM is an immediate target of the floral homeotic genes for floral patterning. Nature 1998, 395:561-566. APETALA3/PISTILLATA. Cell 1998, 92:93-103.
This paper describes the phenotype of plants carrying a gain-of-function
APETALA3 and PISTILLATA function are placed under post-translational
allele of LEAFY, called LFY:VP16, which was constructed by inserting the
control by use of a steroid-inducible AP3 (35S::AP3-GR). Using differential
transcriptional activation domain of VP16 into LFY. It was found that
display, three direct targets of AP3/PI are identified and one of them is
LFY:VP16 has different effects on the expression of the A, B and C class flo-
called NAP (NO APICAL MERISTEM-LIKE, ACTIVATED BY AP3/PI). The
ral homeotic genes. The authors conclude that LFY activates different floral
expression pattern of NAP and the phenotypes caused by its mis-expression
homeotic genes using different mechanisms.
suggest that NAP is important for cell division and cell expansion in stamensand petals.
Busch MA, Bomblies K, Weigel D: Activation of a floral homeotic gene in Arabidopsis. Science 1999, 285:585-587.
34. Jack T, Fox GL, Meyerowitz EM: Arabidopsis homeotic gene
This is an extension of the previous study [16••]. The authors analyze the
APETALA3 ectopic expression: transcriptional and
enhancer elements controlling AGAMOUS expression. They find that two
posttranscriptional regulation determine floral organ identity. Cell LEAFY binding sites in the first intron of AG are necessary for LFY directed
1994, 76:703-716. AG expression in vivo. Therefore, LFY is formally a direct upstream activatorof AG expression.
35. Krizek BA, Meyerowitz EM: The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class
18. Wagner D, Sablowski RWM, Meyerowitz EM: Transcriptional organ identity function. Development 1996, 122:11-22. activation of APETALA1 by LEAFY. Science 1999, 285:582-584.
By using a steroid-inducible LFY, called 35S::LFY-GR, the authors show that
36. Ingram GC, Goodrich J, Wilkinson MD, Simon R, Haughn GW,
early, but not late, expression of APETALA1 results from direct transcrip-
Coen ES: Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 1995, 7:1501-1510.
19. Drews GN, Bowman JL, Meyerowitz EM: Negative regulation of the
Long JA, Barton MK: The development of apical embryonic pattern Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. in Arabidopsis. Development 1998, 125:3027-3035. Cell 1991, 65:991-1002.
38. Hill TA, Day CD, Zondlo SC, Thackeray AG, Irish VF: Discrete spatial
20. Schultz EA, Haughn GW: LEAFY, a homeotic gene that regulates and temporal cis-acting elements regulate transcription of the inflorescence development in Arabidopsis. Plant Cell 1991, Arabidopsis floral homeotic gene APETALA3. Development 1998, 3:771-781. 125:1711-1721.
21. Haula E, Sussex IM: LEAFY interacts with floral homeotic genes to
This paper describes molecular dissection of the APETALA3 promoter. The
regulate Arabidopsis floral development. Plant Cell 1992,
authors identify regions of the promoter require for petal-specific and sta-
men-specific expression, and show that AP3, PISTILLATA, UNUSUAL FLO-RAL ORGANS and APETALA1 are required for AP3::GUS expression in
22. Weigel D, Meyerowitz EM: Activation of floral homeotic genes in
the petals. The authors also demonstrate that AP1, AP3, PI and AG bind to
Arabidopsis. Science 1993, 261:1723-1726.
three sequence elements, called CArG boxes, present in the AP3 promoter. See also [39•].
23. Mizukami Y, Ma H: Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ
39. Tilly JJ, Allen DW, Jack T: The CArG boxes in the promoter of the identity. Cell 1992, 71:119-131. Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 1998, 125:1647-1657.
24. Bowman JL, Smyth DR, Meyerowitz EM: Genetic interactions
To understand how the expression of APETALA3 is regulated, the authors ana-
among floral homeotic genes of Arabidopsis. Development 1991,
lyze the AP3 promoter using AP3::GUS fusions. A 496 bp fragment of the AP3112:1-20.
promoter, or a synthetic AP3 promoter containing three tandem repeats of a
Growth and development
143 bp fragment, directs GUS activity in the same spatial and temporal expres-
receptor component of the IκBα-ubiquitin ligase. Nature 1998,
sion pattern as the endogenous AP3 gene. Mutations of the three CArG
(CArG1–CArG3) boxes, which are present in the 143 bp fragment, affectsGUS expression in the context of the synthetic promoter. The authors conclude
45. Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM:
that CArG1 binds a positively acting factor(s), CArG2 is required for petal spe-
SUPERMAN, a regulator of floral homeotic genes in Arabidopsis.
cific expression, and CArG3 binds a negatively acting factor(s). See also [38•]. Development 1992, 114:599-615.
40. Ingram GC, Doyle S, Carpenter R, Schultz EA, Simon R, Coen ES:
46. Jofuku DK, den Boer BGW, Van Montagu M, Okamuro JK: Control of Dual role for fimbriata in regulating floral homeotic genes and cell Arabidopsis flower and seed development by the homeotic gene division in Antirrhinum. EMBO J 1997, 16:6521-6534. APETALA2. Plant Cell 1994, 6:1211-1225.
41. Zhang H, Kobayashi R, Galaktionov K, Beach D: p19Skp1 and p45Skp2
Kempin SA, Savidge B, Yanofsky MF: Molecular basis of the are essential elements of the cyclinA-CDK2 S phase kinase. Cell cauliflower phenotype in Arabidopsis. Science 1995, 267:522-525.
48. Liu Z, Meyerowitz EM: LEUNIG regulates AGAMOUS expression in
42. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge S: SKP1 Arabidopsis. Development 1995, 121:975-991. connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 1996, 86:263-274.
49. Sakai H, Medrano LJ, Meyerowitz EM: Role of SUPERMAN in
43. Connelly C, Hieter P: Budding yeast SKP1 encodes an maintaining Arabidopsis floral whorl boundaries. Nature 1995, evolutionarily conserved kinetochore protein required for cell 378:199-203. cycle progression. Cell 1996, 86:275-285.
50. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM,
44. Yaron A, Hatzubai A, Davis M, Lavon I, Amit S, Manning AM,
Coupland G: A Polycomb-group gene regulates homeotic gene
Andersen JS, Mann M, Mercurio F, Ben-Neriah Y: Identification of the expression in Arabidopsis. Nature 1997, 386:44-51.
Consultant Clinical Management/Operational Research Supervision and support of clinical activities in the HIV program Providing advice and assistance in the organization of the HIV/ARV program Advanced training of the FHI team and health care staff in HIV care Development and implementation of an observational database Support for operational research activities Support for statistical analy
TechTopics September 17,1999 Michigan Tech’s Faculty/Staff Newsletter Published weekly by University Relations Senate at odds with president over committee appointmentsTompkins says appointments needed to balance committee representationThe University Senate passed a resolution"This calls into serious question the idea oftoday that MTU alumnus John Opie and his September 15 c