Download Turning floral organs into leaves, leaves into floral organs Koji Goto

449
Turning floral organs into leaves, leaves into floral organs
Koji Goto*, Junko Kyozuka† and John L Bowman‡
The development of the floral organs is specified by the
combinations of three classes of gene for organ identity in the
‘ABC’ model. Recently, molecular genetic studies have shown
this model is applicable to grass plants as well as most eudicots.
Transcription factor complexes of ABC and homologous
proteins form the molecular basis of the ABC model.
divergent eudicot species — Arabidopsis thaliana and
Antirrhinum majus? Second, how is the activity of the floral
homeotic genes confined to flower meristems? Third, are
there additional genes that act in parallel with the floral
homeotic ABC genes to promote floral organ identity?
The floral homeotic mutants of Arabidopsis
Addresses
*Research Institute for Biological Sciences, Kayo-cho, Jobo, Okayama,
716-1241, Japan;
e-mail: [email protected]
† Department of Biosciences, Nara Institute of Science and Technology,
8916-5, Takayama, Ikoma 630-0101, Japan;
e-mail: [email protected]
‡ Section of Plant Biology, University of California Davis, Davis,
California 95616, USA;
e-mail: [email protected]
Correspondence: Koji Goto
Current Opinion in Genetics & Development 2001, 11:449–456
0959-437X/01/$ — see front matter
© 2001 Elsevier Science Ltd. All rights reserved.
Abbreviations
ag
agamous
agl
agamous-like
ap1
apetala1
ap2
apetala2
ap3
apetala3
cal
cauliflower
crc
crabs claw
MADS
MCM1-AGAMOUS-DEFICIENS-SRF1
OsMADS Oryza sativa MADS box
pi
pistillata
sep
sepallata
Si1
silky1
spt
spatula
ZAG
Zea mays AGAMOUS-LIKE
ZMM
Zea mays MADS box
Introduction
The application of developmental genetics has led to
progress in our understanding of how organ type is specified in the flower. The advances have been made through
genetic analyses of mutants that specifically disrupt floral
development, and through molecular cloning of the corresponding genes to reveal the nature of their biochemical
function. A model (now known widely as the ‘ABC model’;
Figure 1) based on genetic data was proposed to explain
how a limited set of genes acting alone and in combination
could specify the identity of the floral organs [1–4].
Subsequent molecular analyses of the relevant genes and
ectopic expression studies in Arabidopsis have largely supported this genetic model and have led to numerous
refinements and further insights (reviewed in [5–8]).
In this review we summarize recent progress made on three
outstanding issues. First, how widely applicable is the ABC
model, which was originally based on two evolutionarily
The Arabidopsis flower consists of four concentric whorls of
organs: sepals, petals, stamens and carpels. Mutations in a
set of floral homeotic genes result in the misinterpretation
of positional information in the developing flower, and
subsequent homeotic transformation of floral organ types.
These floral homeotic mutants fall into three classes, designated A, B and C, and each of the mutations results in
organ identity defects in two adjacent whorls.
Class A mutants (apetala2 [ap2] and apetala1 [ap1]) have
homeotic conversions in the first two whorls, with, in the
case of ap2, the first whorl organs developing as carpels
rather than sepals, and the second whorl organs developing
as stamens rather than petals [1,4,9–15]. Class B mutants
(pistillata [pi] and apetala3 [ap3]) have alterations in the
middle two whorls, with sepals instead of petals developing
in the second whorl and carpels instead of stamens in the
third whorl [1,4,16–18]. The inner two whorls are affected
in class C mutants (agamous [ag]), with petals developing
in place of stamens and another flower replacing the
carpels [1,4,19].
There are three basic tenets of the ABC model [4]: first,
each of the classes of homeotic gene function acts in a field
comprised of two adjacent whorls, the particular whorls
being those that are altered when the corresponding genes
are mutant; second, the combination of floral homeotic
gene activities specifies the type of organ that develops;
and third, the class A and class C activities are mutually
antagonistic, such that loss of A results in C activity in all
four whorls and vice versa.
Turning floral organs into leaves
The ABC model successfully predicts the phenotypes of the
floral organs for most of the singly, doubly and triply mutant
genotypes examined. But when all of the A, B and C classes
of floral homeotic activities are removed, as in an ABC triple
mutant, the model does not predict the type of organ that
will develop. One might suppose that if all genes required for
the specification of floral organ identity were removed, the
identity of the resulting organs might represent a ground
state, possibly a leaf-like organ. When the floral organs of the
ABC triple mutant are examined, they exhibit features of
both carpels (such as stigmatic tissue, fusion of organs along
their margins and ovules) and leaves (stellate trichomes and
stipules) [4,20••]. Thus, there must exist genes that promote
carpel development in the absence of AG gene function.
450
Pattern formation and developmental mechanisms
Figure 1
(a)
(b)
AP3 + PI
AP2
+
AP1
B
se
pe
st
AP2
+
AP1
B
AG
A
ca
AP3 + PI
A
C
se
pe
st
ca
st
pe
se
1
2
3
4
3
2
1
Current Opinion in Genetics & Development
The ABC model and the specification of floral organ identity.
(a) A wild-type flower and its floral diagram. (b) The ABC model of the
specification of floral organ identity depicts how three classes of floral
homeotic genes can specify the identity of each of the four whorls of
floral organs. Class A alone specifies sepals, classes A + B specify
petals, classes B + C specify stamens, and class C alone specifies
carpels. Abbreviations: ca, carpel; pe, petal; se, sepal; st, stamen.
A section through a floral primordium, depicted as a set of boxes with
the regions representing each whorl indicated beneath each column.
The top boxes each represent a single field (A, red; B, yellow; C, blue).
The distribution of floral homeotic gene products present in each of the
whorls is indicated inside the boxes, with the phenotype of the organs
in each whorl indicated beneath the lower set of boxes: sepal (red),
petal (orange), stamen (green), carpel (blue).
In a series of elegant genetic experiments, Alvarez and
Smyth [20••] have demonstrated that CRABS CLAW (CRC)
and SPATULA (SPT) act in an AG-independent manner to
promote several aspects of carpel differentiation. Both spt
and crc mutations have a phenotypic effect in an ABC
triple mutant background, reducing the amount and type
of carpel tissues that develop, with mutations in spt having
the more marked effect ([20••]; Figure 2). In the ap2 pi ag
spt quadruple mutant, residual occasional ovule-like
structures develop at the margins of the phylloid floral
organs. Some of these marginal outgrowths also develop
in ap2 pi ag spt crc pentuple mutants [20••], which suggests
that additional genes also promote AG-independent
develop-ment of marginal carpel tissues, candidates being
LEUNIG and AINTEGUMENTA [21••]. Consistent with
the presence of additional redundant genes is the observation that spt single mutants do not lack most marginal
tissues, but instead primarily affect the differentiation of
septal tissues [20••]. Because ag mutations are epistatic to spt
mutations, SPT, like AG, may also be negatively regulated
by A class genes [20••].
mutants is mediated by ectopic SPT activity, as confirmed
by the epistasis of SPT mutations over ettin mutations with
respect to this phenotype [22••,24].
SPT encodes a basic helix–loop–helix transcription factor
and its expression in the developing carpel is consistent
with the proposed role of promoting the growth of marginal
tissues [22••]. SPT is also expressed in many different
tissues outside the carpel, suggesting that it may act redundantly in diverse developmental processes. The negative
regulation of SPT by the A class genes is at the transcriptional level and, furthermore, the restriction of SPT
expression to the marginal tissues of the carpel is mediated
by ETTIN activity [22••]. In ettin mutants, marginal tissue
(e.g. septum) develops ectopically in non-marginal
positions [23]. The ectopic development of septum in ettin
Is ABC model applicable to the grass flower?
Grass species have flowers with highly derived structures,
and the identity of the lodicules, palea and lemma, which
surround the reproductive organs has been unclear
(Figure 3; [25–27]). Issues regarding the evolution of floral
organs in grass species are now being addressed using the
ABC model as a baseline.
Grass flower homologs of ABC genes
The isolation of putative class A, B and C genes from rice
and maize suggests that the basic mechanisms of flower
development are probably conserved between grasses and
eudicots [28–33,34••,35••]. In both maize and rice, class C
genes are expressed in the inner two whorls, class B gene
transcripts accumulate in stamens and lodicules, and a
putative rice class A gene, RAP1A, is expressed in lodicules,
the palea and lemma [34••]. Although expression patterns
can be correlative, a functional assay is needed to further
assess any potential homology.
Recently, Ambrose et al. [35••] have identified silky1 (si1)
as the AP3 ortholog in maize. Remarkably, in si1
mutants, stamens and lodicules are homeotically transformed into carpels and palea/lemma-like structures,
respectively [35••]. Likewise, reduced function of the
rice PI ortholog (OsMADS4) by antisense methodology
results in a similar phenotype [36]. These data imply
that there is a homologous relationship between lodicules and petals, and that B function is conserved in
grass flowers.
Turning floral organs into leaves, leaves into floral organs Goto, Kyozuka and Bowman
Figure 3
Figure 2
(a)
(b)
le
st
ap2 pi ag
451
ca
ap2 pi ag spt
Current Opinion in Genetics & Development
ap2 pi ag (ABC) triple mutants develop placentae bearing ovules,
septum containing transmitting tract tissue, style tissue, and stigmatic
papillae along the margins of their floral organs [4,20••]. The only major
carpel tissue not found in ap2 pi ag triple mutants is the specialized
histology of the ovary wall [20••]. In contrast, floral organs of ap2 pi ag
spt quadruple mutants lack most of the carpelloid marginal tissues
found in the ABC triple mutant, indicating that SPT promotes the
differentiation of all these tissue types — a role not obvious from the spt
single mutant phenotype in which only the septum is lacking [20••].
Identity of lemma and palea
In contrast to the progress in understanding the identity of
lodicules, the nature of lemma and palea is still uncertain.
Palea/lemma-like structures develop in place of the
lodicules in si1 mutants, which suggests that there is a
possible homology between palea/lemma and sepals [35••].
In addition, the expression pattern of the RAP1A is consistent
with the palea/lemma representing the calyx [34••].
In contrast, an absence of any morphological changes in the
palea or lemma in Act1::RAG plants (J Kyozuka, unpublished
data) argues against this view and raises the possibility that
the palea and lemma may not be floral organs whose identities are controlled by class A, B and C genes. However, it is
also possible that ectopic expression of the class C gene is
not sufficient to specify carpel identity in grasses.
Recently, Jeon et al. [37] demonstrated that a mutation in
OsMADS1, an AGL9 subfamily rice MADS-box gene, resulted
in the elongation of palea and lemma and a reduction in
floral meristem determinacy. Analysis of loss-of-function
phenotypes of the grass class A genes, as well as genes with
related sequences, such as OsMADS1, will be critical in
elucidating the nature of the palea/lemma.
Homology between lodicules and eudicot petals
In eudicots, the ABC model has enabled the prediction of
modified flower structures through manipulating the
expression of the floral organ identity genes. For example,
ectopic expression of AG by a constitutive promoter results
in homeotic transformations of sepals to carpels and petals
to stamens in eudicot flowers [38,39]. In rice, the ectopic
expression of RAG/OsMADS3, a rice AG ortholog driven by
the strong Actin1 promoter, caused homeotic conversions
of lodicules to stamens (J Kyokuka, unpublished data).
pa
ca
le
lo
lo
pa
st
Current Opinion in Genetics & Development
A rice spikelet (a) and diagram of a transverse section through a flower
(b). A rice flower, which is enclosed by a pair of bract-like structures
called the lemma (le) and palea (pa), is composed of a pistil comprising
three carpels (ca), six stamens (st) and two lodicules (lo). The lemma is
detached from original position (arrow) to show lodicules.
This increases the evidence in favour of lodicules being
genetically homologous to petals. Together, homology
between lodicules and eudicot petals is supported by three
different lines of evidence: first, analyses of RNA
expression patterns of class A and B genes; second, loss-offunction mutant phenotypes of class B genes; and third,
gain-of-function alleles of class C genes. Together, these
results suggest that the ABC genes control floral organ
development in a similar manner in the grasses and the
eudicots, which span the majority of angiosperm phylogenetic diversity [40].
Carpel development in grass flowers
Grass species may have acquired unique mechanisms for
carpel development. It has been proposed that in maize
the C function is shared by two AG orthologs, ZAG1 and
ZMM2 [29,30]. The expression patterns of ZAG1 and
ZMM2 suggest that these genes may be involved in determining the carpel and stamen identities, respectively.
In the zag1 mutant, however, in spite of a biased expression
of ZAG1 in the carpel, there were no clear morphological
alterations in this organ and only floral meristem determinacy was affected [29]. This raises the possibility that
carpel identity may not depend solely on the class C
homeotic genes in grass species, and that the function of
another unknown gene(s) may also be required for the
specification of carpels.
Turning leaves into floral organs
Molecular cloning of the ABC genes in Arabidopsis has
revealed that all except AP2 share a conserved DNAbinding domain, called the MADS domain or ‘MADS
box’ [3,14,15,17–19]. By manipulating the expression of
the ABC genes, one can construct flowers with of any
floral organs in any whorl [4,39,41]. Ectopic expression of
the ABC genes in leaves fails, however, to convert them
452
Pattern formation and developmental mechanisms
Figure 4
(a)
AP3::GUS reporter gene expression in plants
constitutively expressing (a) PI–AP3 and
(b) PI:VP16–AP3. AP3::GUS is activated by
PI–AP3 in the floral organs, but not in the
vegetative organs (i.e. leaves). When the viral
transactivation domain VP16 is fused to PI
(PI:VP16), AP3::GUS becomes activated in
the leaves. This implies that a flower-specific
cofactor with a transactivation domain is
required for complete B gene activity.
(b)
Current Opinion in Genetics & Development
into floral organs [39,41]. Thus, the ABC genes are necessary for the formation of floral organs, but they are
not sufficient for the conversion from vegetative leaves
into floral organs.
Another factor is needed
More than 200 years ago, Goethe proposed that floral
organs are the result of a transformation (‘metamorphosis’)
of the basic leaves. Thus, there should exist as yet unidentified factors required for this transformation or,
alternatively, it might be that vegetative leaves are not the
‘basic organ’ from which the floral organs were derived.
Recently, Honma and Goto [42••] found the missing factor
by searching for proteins that interact with the ABC
MADS-box proteins.
The B gene proteins, PI and AP3, act as a heterodimer and
autoregulate their own transcription ([41,43–45]; reviewed
in [8]). The transcription of an AP3::GUS reporter gene is
activated by PI–AP3 without de novo protein synthesis in
the flower [43], but is not activated outside the flower
even when PI and AP3 are expressed constitutively
([41,43]; Figure 4). However, AP3::GUS expression is
observed in the leaves when a viral transcriptional activator domain, VP16, is fused with PI (35S::PI:VP16;
Figure 4). This suggested that a flower-specific cofactor
might supply a transcriptional activator domain to the
PI–AP3 complex.
Thus, the putative missing factor was isolated by fishing
for proteins that interact with the PI–AP3 complex, and
was identified as another MADS-box gene, AGL9 (agamous-like 9) [42••,46]. Other kinds of proteins were not
isolated in the yeast two-hybrid screening, suggesting that
the entire complex may be composed solely of MADS-box
proteins, and that AGL9 may supply a transcriptional
activator domain. Notably, Davies et al. [47] and EgeaCortines et al. [48••] have demonstrated that Antirrhinum
ABC MADS-box proteins exhibit a higher affinity and
specificity with target DNA sequences when part of a
ternary complex than when part of a dimer.
AGL9 (SEP3) is the missing factor
Recently, AGL9 was renamed SEPLALLATA3 (SEP3)
based on its mutant phenotype [49••]. The sep3 mutant
itself shows only a subtle phenotype, but in combination
with sep1 and sep2 mutants (knockouts of the closely related
genes AGL2 and AGL4, respectively), all floral organs
develop as sepal-like organs. Thus, the triply mutant
sep123 flowers resemble those of bc double mutants [49••].
The most striking evidence demonstrating that SEP3 is
the missing factor is the phenotypes of doubly, triply or
quadruply transgenic plants combining ectopic expression
of SEP3 with ectopic expression of the ABC genes.
Remarkably, leaves are converted into petals by
ectopic expression of PI–AP3–SEP3, AP1–PI–AP3 [42••]
or AP1–PI–AP3–SEP3 [50••], into stamens by
PI–AP3–AG–SEP3 [42••], and into carpels by AG–SEP3
(K Goto, unpublished data; Figure 5). These observations
indicate that when SEP3 gene function is added in combination with ABC genes, vegetative leaves can be
converted into floral organs, supporting Goethe’s theory.
Complexes of the MADS-box proteins are the
molecular basis of the ABC model
Further analyses of protein–protein interactions suggest
that SEP3 not only interacts with PI and AP3, but also
serves a scaffold between PI–AP3 and AG [42••]. Although
PI–AP3 and AG (the B and C proteins) cannot interact
directly, if SEP3 is added then the quartet complex,
PI–AP3–SEP3–AG (third whorl complex), can form. The
AG–SEP3 interaction suggests that the fourth whorl
complex should be AG–SEP3. Likewise, PI–AP3 can
interact with both AP1 and SEP3, and AP1 and SEP3
interact with each other [42••]; therefore, the second whorl
complex should be AP1–PI–AP3–SEP3.
What about the first whorl? The SEP proteins may not be
required for a first whorl complex as the sep123 triple
mutant develops normal sepals. Because MADS-box
proteins form a dimer to bind their target DNA sequence
(called the ‘CArG-box’; reviewed in [8]), AP1 might form
Turning floral organs into leaves, leaves into floral organs Goto, Kyozuka and Bowman
453
Figure 5
Phenotypes of (a,b) wild-type and
(c–f) transgenic plants. A similar
developmental stage (shortly after bolting) is
shown in (a,c,e). The inflorescence stem (is),
cauline leaf (cl) and lateral shoot (ls) are
depicted in (b,d,f). Rosette leaves (rl) are
transformed (c) into petals by the complex
PI–AP3–SEP3 and (e) into carpels by the
complex SEP3–AG. Cotyledons (ct) are not
transformed. Cauline leaves (cl) are converted
(d) into petals by the complex AP1–PI–AP3
and (f) into stamens by the complex
PI–AP3–SEP3–AG.
(a)
(c)
(e)
rl
ct
rl
ct
ct
rl
(d)
(b)
(f)
Is
Is
Is
cl
cl
cl
is
is
is
Current Opinion in Genetics & Development
homodimers or heterodimers with CAULIFLOWER
(CAL). AP1 and CAL can interact with each other
(K Goto, unpublished results), but cal single mutants do
not exhibit any aberrant phenotype although they enhance
ap1 phenotypes [13,51]. Ectopic expression of AP1 or CAL
does not result in a transformation of leaves into sepals
[51,52], however, which suggests the existence of an as yet
unidentified factor required for the promotion of sepal
identity in conjunction with AP1. On these molecular
bases, the classical ABC model should be modified by
adding SEP as a limiting factor that restricts the activity of
the ABC genes to the floral organs (Figure 6).
the floral organs. If all the ABC gene activities were compromised, one might expect a ground state of the floral
organ to be revealed — what Goethe referred to as the
‘ideal basic organ’. abc triple mutant flowers comprise not
leaves, but organs that have characteristics of both leaves
and carpels.
It is tempting to speculate that the pathways mediated by
SPT and other marginal-tissue promoting genes might represent evolutionarily ancient genetic networks directing
the development of sporophylls that predate the evolution
Figure 6
The functional redundancy of the SEP genes has been
shown recently by both loss-of-function alleles [49••] and
gain-of-function alleles [42••,50••]. Ectopic expression of
AP1–PI–AP3–SEP3, as well as of AP1–PI–AP3–SEP1–SEP2,
can convert leaves into petals [50••]. The three SEP genes
form a monophyletic clade within the MADS-box genes of
Arabidopsis (Figure 7, SEP clade).
1
se
3
st
2
pe
4
ca
B: PI, AP3
A: AP1, CAL
C: AG
SEP3
The observation that both AP1–PI–AP3 and PI–AP3–SEP3
can convert leaves into petals when constitutively
expressed [42••] argues that AP1 and SEP3 are also
redundant in some of their functions. This is supported
by the fact that the SEP genes and AP1 belong to the
SEP/AP1 superclade (Figure 7). One possible redundant
function may be to act as a transactivation component in
the complexes. B and C genes do not show any transactivation activity, but genes in the SEP/AP1 superclade
shows such activity, although their relative activities vary
(Figure 7).
Conclusions and perspectives
The ABC model has been surprisingly successful in
explaining how a small number of regulatory genes,
acting alone and in combination, specify the identity of
AP1
CAL
PI AP3
AP1
PI AP3
SEP3
AG
SEP3
SEP3
AG
Current Opinion in Genetics & Development
A revised ABC model. In addition to the original ABC genes, the SEP
genes have a crucial role in providing transactivation activity and
serving as a scaffold between B and C proteins. Boxes indicate the
region of gene expression detected by in situ RNA hybridization. Ovals
show proteins, and contact between ovals indicates a protein
interaction. For simplicity, the homodimer is not indicated. ca, carpel;
pe, petal; se, sepal; st, stamen.
454
Pattern formation and developmental mechanisms
Figure 7
(a)
FRUITFULL
(b)
CAL
AP1 clade
PI/AP3 clade
AP3
AG
SEP3
SEP2
0
SHATTERPROOF1
PI
SEP1
SHATTERPROOF2
CAL
AG
AG clade
50
AP1
SEP1
AGL11
100
PI-VP16+AP3
SEP2
PI+AP3
SEP3
AP3
SEP clade
150
PI-VP16
AGL3
PI
AGL6
Control
AP1/SEP super clade
Relative LUC/R-LUC activity
AP1
AGL13
Current Opinion in Genetics & Development
Phylogenetic tree of (a) the Arabidopsis MADS-box proteins and
(b) transactivation activity of ABC and SEP genes. Protein
sequences were aligned by ClustalW (http://www.ddbj.nig.ac.jp/
E-mail/clustalw-e.html), and the results are depicted using
TreeView (http://taxonomy.zoology.gla.ac.uk/rod/treeview.html).
The ABC MADS-box proteins are located in three distinct clades:
the AP1/SEP superclade, the AG clade and the PI/AP3
superclade. Although not all members have been tested, proteins
belonging to the AP1/SEP superclade show transactivation
activity. Transactivation assays were performed by particle
bombardment into onion epidermal cells using a CArG::Luciferase
reporter gene [42••].
of flowers. Subsequently, the ABC genetic network would
have been recruited and integrated with these pre-existing
genetic programs, leading to the evolution of the flower in
angiosperms. In this scheme, the marginal tissues and nonmarginal tissues of the Arabidopsis carpel would have
separate evolutionary origins, and a ground state of the
angiosperm floral organ might be a sporophyll. Studies of
orthologous genes in other angiosperms and in non-flowering plants are needed to address this issue.
organ activity. Biochemical studies are now required to
reveal how DNA-binding affinities are modulated by these
complexes in vivo, because all MADS-box proteins bind to
CArG boxes in vitro.
The ABC model is widely applicable to the angiosperms,
including grasses. Grass flowers are morphologically quite
different from those of other angiosperms, especially in the
peripheral two whorls. Molecular genetic studies of maize
and rice suggest that the palea and lemma may be similar
to the sepals of eudicots, and that lodicules are probably
homologous to petals of eudicots.
Protein complexes are the molecular basis of the genetic
ABC model: A + B + SEP3 specifies petals; B + C + SEP3
specifies stamens; C + SEP3 specifies carpels. Because
leaves can be converted into floral organs, these complexes must be sufficient for floral organ identity. It is
noteworthy that SEP3 as well as the ABC genes are homologous MADS-box transcription factors, and that different
complexes of homologous proteins result in specific floral
It is also intriguing that some MADS-box proteins belonging to the AP1/SEP superclade have transactivation
activity, whereas others belonging to the PI/AP3 or AG
clades do not. When and how they obtained or lost such
activity during their evolution might have influenced the
evolution of floral organs.
Acknowledgements
Work on floral organ identity in K Goto’s laboratory is supported by the
Japan Society for the Promotion of Science (JSPS-RFTF96L00403).
J Kyozuka’s project is partly supported by CREST, JST. J Bowman is
supported by a grant from National Science Foundation.
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• of special interest
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