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First published online April 24, 2009
doi: 10.1242/10.1242/dev.033647
1 Max-Planck Institute for Developmental Biology, D-72076 Tübingen,
Germany.
2 Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
3 University of Heidelberg, D-69120 Heidelberg, Germany.
¶ Author for correspondence (e-mail: jlohmann{at}meristemania.org)
Accepted 6 March 2009
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SUMMARY |
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MATERIALS AND METHODS
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DISCUSSION
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Key words: PERIANTHIA, AGAMOUS, Stem cells, Arabidopsis
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INTRODUCTION |
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).
Flowers of the reference plant Arabidopsis thaliana contain four
major organ types: sepals, petals, stamens and carpels, which are arranged in
four concentric rings or whorls. Organ identity is specified by the
overlapping activities of three classes of homeotic genes, termed A, B and C,
as predicted in the ABC model (Bowman et
al., 1991; Coen and
Meyerowitz, 1991). The activity of a floral homeotic gene is
typically confined to two adjacent whorls, with the A class represented by
APETALA1 (AP1) and APETALA2 (AP2) acting
in whorls one and two, the B class genes APETALA3 (AP3) and
PISTILATA (PI) in whorls two and three, and the C class gene
AGAMOUS (AG) in whorls three and four (reviewed by
Lohmann and Weigel, 2002).
With the exception of AP2, all floral homeotic genes code for MADS
domain transcription factors. Essential co-regulators in this process are the
MADS domain transcription factors of the SEPALLATA class (SEP1, SEP2, SEP3 and
SEP4), which form tetrameric complexes with different combinations of homeotic
ABC factors (Ditta et al.,
2004; Honma and Goto,
2001; Melzer et al.,
2009; Pelaz et al.,
2000).
While the primary function of floral homeotic genes appears to be the
specification of floral organ identity, several of them have additional roles.
The most prominent example is the C class gene AG. In addition to
specifying reproductive organs, stamens and carpels, it has a key role in
limiting stem cell proliferation in the center of emerging flowers
(Bowman et al., 1989;
Bowman et al., 1991;
Mizukami and Ma, 1995;
Sieburth et al., 1995).
Although the molecular nature of AG was uncovered almost two
decades ago (Yanofsky et al.,
1990) our understanding of AG regulation is far from
complete. The proper spatiotemporal expression of AG RNA is dependent
on sequences located in the second intron, which is one of the longest found
in the A. thaliana genome
(Sieburth and Meyerowitz,
1997). Functional characterization of this intragenic enhancer
demonstrated that multiple redundant regulatory modules mediate the response
to competing activating and repressing inputs
(Bomblies et al., 1999;
Busch et al., 1999;
Deyholos and Sieburth, 2000).
One of the most prominent direct regulators is the meristem identity factor
LEAFY (LFY) (Busch et al.,
1999; Parcy et al.,
2002; Parcy et al.,
1998), which acts in concert with the homeodomain transcription
factor WUSCHEL (WUS) to activate AG in the center of developing
flowers (Lohmann et al.,
2001). Additional inputs are provided by SEP3, which can act as
activator (Castillejo et al.,
2005) or repressor of AG transcription
(Sridhar et al., 2006),
depending on the regulatory environment. Once AG transcription has
been activated, an autoregulatory mechanism is in place to ensure stable
expression throughout flower development
(Gomez-Mena et al., 2005).
Important repressors of AG expression are LEUNIG (LUG) and SEUSS
(SEU), which act as co-repressors in higher order complexes with DNA-binding
transcription factors, such as AP1, SEP3 and AGAMOUS-LIKE 24
(Franks et al., 2002;
Gregis et al., 2006;
Liu and Meyerowitz, 1995;
Sridhar et al., 2006). In
addition, AG expression is repressed in the outer whorls by the AP2
transcription factor (Drews et al.,
1991), which in turn is under negative regulation by the microRNA
miR172 (Aukerman and Sakai,
2003; Chen,
2004).
An additional layer of regulatory complexity is introduced by epigenetic
silencing of the AG locus, which is mediated by trimethylation of
lysine 27 on histone H3 proteins. It has been shown that these modifications
are dependent on a complex containing CURLY LEAF (CLF) and EMBRYONIC FLOWER 2
(EMF2), two members of the polycomb group protein family, as well as the
plant-specific protein EMBRYONIC FLOWER 1 (EMF1)
(Calonje et al., 2008).
Consequently, mutations in the corresponding genes cause ectopic AG
expression (Goodrich et al.,
1997). The activity of the repressor complex is antagonized by
ARABIDOPSIS HOMOLOG OF THRITHORAX 1 (ATX1)
(Alvarez-Venegas et al.,
2003).
As the proper spatiotemporal expression of AG involves a plethora
of regulators, which act through redundant modules in the large intragenic
enhancer, direct identification of important cis-regulatory elements has been
difficult. Candidates for cis-regulatory motifs have instead been identified
using phylogenetic footprinting and shadowing
(Hong et al., 2003), although
many of the corresponding trans-factors have remained unknown. Recent studies
have shown that regulatory elements have been a driving force for the
evolution of floral diversity (Causier et
al., 2009). Here, we identify a new activator of AG, the
bZIP factor PERIANTHIA (PAN), which was previously known to affect floral
organ number (Chuang et al.,
1999; Running and Meyerowitz,
1996), but not homeotic gene expression.
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). In
situ hybridizations were performed in accordance with standard protocols
(Weigel and Glazebrook, 2002)
with the addition of 10% PVA to the staining solution. RNA probes were
prepared from full-length cDNAs. Real-time RT-PCR analyses were performed on
three replicates of independently grown plant material. RNA from a pool of
primary inflorescences was prepared using RNeasy Plant Mini Kit (Qiagen),
followed by cDNA synthesis with RevertAid H Minus First Strand cDNA Synthesis
Kit (Fermentas). PCR was carried out in the presence of SYBR Green using
BETA-TUBULIN-2 (At5G62690) for normalization. Primer sequences can be
obtained upon request.
Plasmids
A list of all constructs is given in
Table 2.
|
) and the
5'AG enhancer was cloned in forward orientation into pDW294
(Busch et al., 1999) by
BamHI/HindIII restriction sites. pSST210 was obtained using
the QuikChange Site-Directed Mutagenesis Kit (Stratagene) on KB8 following the
manufacturer's protocol and subcloning of the 5' enhancer into pDW294
using BamHI/HindIII. Primer sequences can be obtained upon
request.
Yeast one-hybrid screen
As bait for the yeast one-hybrid screen, the 33 bp AAGAAT box was
trimerized using XhoI and SalI sites, inserted in the
XhoI site of pEMBLYi22 (Baldari
and Cesareni, 1985) to yield pSST90, linearized and integrated
into the URA3 locus of the W303-A1a yeast strain (for detailed
information see:
http://wiki.yeastgenome.org/index.php/CommunityW303.html).
Using standard protocols the screen was performed with a cDNA library
constructed of RNA from young floral tissue in pEXPAD-502
(Wigge et al., 2005). Double
transformants were selected on CSM-TRP/-HIS + 15 mM 3AT plates. Plasmids of
positive clones were rescued, re-transformed and confirmed by X-Gal
filter-lift-assay before sequencing. For independent confirmation, full-length
cDNAs of candidate factors were cloned into pGEM-T easy (Promega) and
subcloned into pEXPAD-502 (TRP1, Invitrogen). All were transformed
stably into the yeast strain EGY48
(Golemis et al., 1996) that
contained wild-type or mutated versions of the trimerized AAGAAT box upstream
of the lacZ reporter in the vector KF1, a derivative of pLG718
(Guarente and Mason, 1983).
pSST093 contained the wild-type AAGAAT box sequence, for pSST197 two
nucleotides of the putative binding sites for bZIP were mutated [using the
QuikChange Site-Directed Mutagenesis Kit (Stratagene) following the
manufacturer's protocol] and the resulting 
bZIP AAGAAT box trimer was
inserted using SpeI/XbaI sites into KF1. For pSST209 the
same procedure was followed by mutating two nucleotides in each of the
putative GARP-binding sites as described in
Fig. 2A and inserting the
fragment into KF1.
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), respectively, and co-transformed into yeast. Liquid
cultures were assayed for β-galactosidase activity to quantify
transcriptional activation of the AAGAAT box reporter gene. Color reactions
were carried out using ONPG (o-nitrophenyl-beta-D-galactoside) as a substrate
and an ELISA reader. Relative reporter gene activity was calculated according
to Miller (Miller, 1972). |
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;
Deyholos and Sieburth, 2000;
Hong et al., 2003). One of the
least variable sequences was the 33-bp-long AAGAAT box, which is not an
obvious candidate for a motif bound by known regulators such as LFY, WUS or
MADS domain factors (Fig. 1A).
Recently, Causier et al. (Causier et al.,
2009) have shown that the AAGAAT box has been conserved in
sequence and relative position in monocots and dicots, suggesting that it
arose before the split of the two lineages roughly 140 million years ago. The
enhancer in the second AG intron is composed of two redundant regions
(Bomblies et al., 1999;
Busch et al., 1999;
Deyholos and Sieburth, 2000),
and the AAGAAT box is located in the 5' fragment defined by the
KB14 reporter (Fig.
1A), which drives GUS reporter expression in the
AG domain (Fig. 1B)
(Busch et al., 1999). The
deletion of the AAGAAT box in this context (RH146) caused a severe
reduction of reporter gene expression (Fig.
1B-D), indicating that this element is essential for activity of
the 5'AG enhancer. The AG activator LFY acts through
DNA motifs contained in KB14, which are distinct from the AAGAAT box.
Thus, we crossed KB14 and RH146 to plants expressing an
activated form of LFY, LFY:VP16
(Busch et al., 1999;
Parcy et al., 1998), to test
the functionality of the RH146 reporter. We observed strong and
ectopic GUS expression, confirming that the regulatory input of other factors
binding to the 5'AG enhancer is not impaired in the
RH146 lines (see Fig. S1 in the supplementary material).
|
) and an
AAGAAT box trimer as bait (pSST90). Two independent screens of more than 2.5
million transformants identified 50 positive clones, which contained inserts
coding for transcription factors of the GARP or bZIP families. We found four
different bZIPs, At1g08320/ATBZIP21, At1g68640/PERIANTHIA (PAN),
At3g12250/TGA6, and At5g06960/TGA5, and five GARP factors, At1g79430/ALTERED
PHLOEM DEVELOPMENT (APL), At3g24120, At4g13640/UNFERTILIZED EMBRYO SAC 16
(UNE16), At4g16110/ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2), and At4g37180.
Full-length cDNAs of all but ARR2 were fused with the GAL4 activation domain
and interaction with the AAGAAT box was confirmed.
|
;
Hosoda et al., 2002). Within
the AAGAAT box, these elements were almost invariant, even outside the
Brassicacae (Hong et al.,
2003; Causier et al.,
2009), supporting the conserved functional importance of these
sequences. To determine if the consensus motifs are indeed bona fide binding
sites for the identified transcription factors, we selectively mutated them in
the context of the yeast reporter construct. Mutations in the putative
bZIP-binding site (bZIP) (Fig.
2A,B) resulted specifically in the loss of response to the four
bZIP factors. Conversely, mutations in the GARP motifs selectively interfered
with reporter gene expression in response to the GARP transcription factors
(GARP) (Fig. 2A,B).
These results demonstrated that the bZIP and GARP transcription factors
identified in the one-hybrid screen bind in a sequence-specific manner to
distinct motifs within the AAGAAT box.
The bZIP transcription factor PERIANTHIA acts on AG enhancer sequences in vivo
If any of the identified transcription factors were to play a role in the
activation of AG transcription, one would expect overlapping
expression in early flowers, where AG mRNA is first detected. To
address this issue, we queried the AtGenExpress database
(Schmid et al., 2005). From
the nine candidates, only the bZIP transcription factor gene PAN
showed strong and specific expression in apices and flowers
(Fig. 2C)
(Chuang et al., 1999), while
the other mRNAs are expressed more uniformly across the various tissues.
pan mutants have prominent defects in floral organ number
(Fig. 3G,H)
(Chuang et al., 1999;
Running and Meyerowitz, 1996),
whereas T-DNA insertion mutants for the other factors identified in the
one-hybrid screen did not have any floral phenotypes (see
Table 1), suggesting that among
the one-hybrid candidates only PAN has important roles in flower
development, or that genetic redundancy is masking the function of the other
regulators.
In situ hybridization confirmed a large overlap of PAN and AG expression domains in flowers (Fig. 3A,B). To investigate the importance of PAN for the activity of AG regulatory sequences, we introduced the KB14 reporter into a pan T-DNA insertion mutant, in which PAN RNA expression was reduced below the levels detectable by in situ hybridization (Fig. 3B,C). 5'AG::GUS reporter activity was drastically reduced in early pan flowers (Fig. 3D,E; see Fig. S4 in the supplementary material), with some residual GUS activity at later stages of flower development (Fig. 3E, white arrowheads). These results demonstrated that PAN is required for activity of AG regulatory elements and were in agreement with PAN not being expressed beyond floral stage 7 (Fig. 3B).
A similar effect on AG::GUS expression as in the pan mutant background was observed when the bZIP-binding site was mutated in the context of the KB14 reporter (Fig. 3F; see Fig. S4 in the supplementary material). In 18 of 25 primary inflorescences from T1 plants, GUS activity could not be detected at all, while the remaining seven apices showed only weak staining in young flowers. This was consistent with results of transactivation assays in yeast, which showed that PAN can synergistically activate transcription from the AAGAAT box in concert with a GARP transcription factor, At4g37180 (see Fig. S2 in the supplementary material), which is expressed in an overlapping domain with PAN mRNA (see Fig. S3 in the supplementary material). Interestingly, the closely related TGA proteins showed repressive activity in the same assay (see Fig. S2 in the supplementary material). Taken together, these results confirmed the relevance of PAN and the bZIP-binding motif for transcriptional activation mediated by AG enhancer sequences.
|
), and with the 5' enhancer fragment (KB14)
from the second AG intron acting redundantly with the non-overlapping
3' enhancer fragment (Fig.
1A) (Busch et al.,
1999; Deyholos and Sieburth,
2000).
PAN is essential for AG activation in early flowers of short-day-grown plants
In contrast to the pan mutant defects, which are restricted to
flowers, PAN protein is much more widely expressed, indicating that PAN has
redundant functions in several different regulatory networks
(Chuang et al., 1999;
Running and Meyerowitz, 1996).
We speculated that genetic perturbations have so far not been able to fully
expose PAN function, and we therefore tested whether variations in
environmental conditions could be a means to elucidate the role of
PAN in AG activation. Photoperiod has been shown before to
affect the phenotypes of plants that are homozygous for a mutation in
AG, or heterozygous for a mutation in the AG activator
LFY (Okamuro et al.,
1996).
Thus, we compared pan mutants and wild-type plants grown under
short days (SD; 8 hours light), long days (LD; 16 hours light) and continuous
light (CL), all at 23°C. Whereas the floral defects of pan
mutants grown under CL and LD were limited to the floral organ number defects
known before, SD caused a loss of determinacy, reminiscent of ag
loss-of-function defects (Fig.
4A-F). The phenotypes ranged from partially unfused carpels, which
developed into deformed and bulged siliques, to fully unfused central organs
that had carpeloid features and on which new floral meristems arose. These
meristems in turn produced mostly petaloid, stamenoid and carpeloid tissues
(Fig. 4D,F; see Fig. S5 in the
supplementary material). These strong phenotypes were most apparent among the
first ten flowers of the primary inflorescence. Later-arising flowers showed
less severe defects consisting mainly of bulged carpels
(Fig. 4B; see Fig. S5A in the
supplementary material), which after dissection showed growth of floral organs
in an aberrant fifth whorl. Together, these defects were detectable in roughly
half of all fruits on the primary inflorescence
(Fig. 4G). Similar defects were
found in plants carrying other pan mutant alleles grown in SD (not
shown) and plants expressing dominant-negative alleles of PAN in LD
(Das et al., 2009). Whereas
the reduction of KB14 activity in pan mutant inflorescences (see Fig.
S6 in the supplementary material) was similar to that observed in LD-grown
plants, SD-grown pan mutants showed in addition a marked reduction in
AG mRNA expression in early flowers
(Fig. 5A,B; see Fig. S7 in the
supplementary material), which was in agreement with the phenotypic
defects.
|
|
). In
wild-type flowers, WUS expression is terminated in an
AG-dependent fashion around stage 6, when patterning of the flower is
accomplished (Lenhard et al.,
2001; Lohmann et al.,
2001). In line with the observation of ectopic meristems
initiating inside the developing gynoecium of SD-grown pan mutants,
we observed WUS expression in these tissues
(Fig. 5F, black arrowhead; see
Fig. S9A in the supplementary material). Although during early stages
WUS expression was rather diffuse in the emerging meristems, once
these meristems had firmly established themselves, WUS mRNA was
confined to the organizing center (see Fig. S9B in the supplementary
material). We conclude that ectopic expression of AG and WUS
at later stages of flower development reflects indirect effects of compromised
PAN activity during earlier stages, and that redundant activators of
AG are normally active throughout flower development. Taken together, our results show that PAN plays an essential role in the activation of AG and that both genes are embedded in a regulatory network that is sensitive to environmental conditions.
PAN and AG are engaged in a negative-feedback loop
The fact that PAN mRNA is not restricted to flowers but is also
highly expressed in proliferating cells of the shoot apical meristem suggested
more general functions of PAN in meristem maintenance. A similar case
is represented by WUS, which has dual roles in stem-cell induction
and floral patterning via AG activation. Consequently, WUS
expression and thus stem-cell maintenance is terminated during flower
development to allow for tissue differentiation, and this process is dependent
on AG activity (Lenhard et al.,
2001; Lohmann et al.,
2001). Thus, we tested whether a similar feedback interaction
existed between PAN and AG. Consistent with such a scenario,
we found that strong PAN RNA expression persisted much longer in
ag mutant flowers than in wild type
(Fig. 6A,B), demonstrating that
PAN is not only an essential activator of AG during early floral
stages, but that at the same time PAN expression is under control of
AG at later stages. As the PAN expression domain in large parts
overlaps with WUS RNA, and because PAN expression also
persists in clavata mutants
(Chuang et al., 1999), in
which WUS is ectopically expressed, we investigated whether WUS
activity might mediate the feedback between AG and PAN. To this end,
we analyzed PAN RNA distribution in flowers ectopically expressing
WUS from the CLAVATA3 (CLV3) promoter
(Brand et al., 2002). Flowers
of plants with intermediate phenotypes develop meristematic tissues from which
stamenoid and carpeloid organs arise, due to the activation of AG in
these cells. In agreement with the hypothesis that WUS mediates at least a
good part of the regulatory interaction between AG and PAN, we
observed ectopic PAN expression as well as accumulation of
AG transcripts in WUS-positive cells
(Fig. 6C,D).
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;
Running and Meyerowitz, 1996),
but also in the regulation of floral determinacy through the direct activation
of AG. The identification of PAN, which is also expressed in
shoot meristems (Running and Meyerowitz,
1996), as an AG activator supports the model that
flower-specific factors such as LFY interact with factors expressed in similar
patterns in both shoot and floral meristems to control region- and
flower-specific expression of floral homeotic genes
(Lee et al., 1997;
Lenhard et al., 2001;
Lohmann et al., 2001;
Parcy et al., 1998).
PAN belongs to the D-group of bZIP transcription factors, which share a
high degree of sequence similarity in the bZIP region
(Jakoby et al., 2002).
Intriguingly, all bZIP transcription factors isolated in our screen fall into
this group. Despite the fact that we have recovered multiple clones for all
factors identified in the screen, we did not isolate all D-group members in
our screen. As at least TGA2 and TGA3 are expressed at
substantial levels in meristematic and floral tissue and therefore should have
been represented in our library, it is tempting to speculate that these
factors might have different DNA-binding specificities.
The findings that PAN can synergize in yeast with the GARP transcription
factor At4g37180 and that both share overlapping expression domains in the SAM
and early flowers suggest that At4G37180 and related GARP transcription
factors are co-factors of PAN in AG regulation. Regulators of diverse
molecular nature can act together in a redundant fashion during flower
development and in particular during the activation of AG, as
recently demonstrated by Prunet et al.
(Prunet et al., 2008).
However, because the family of GARP transcription factors is rather large
(Riechmann et al., 2000), and
because we have found members of both GARP subgroups (ARR-B and GARP-G2), it
will be difficult to identify and functionally test the most promising
candidates for roles in AG regulation.
|
;
Lohmann et al., 2001), PAN not
only contributes to AG activation but in turn is under negative
control by AG during later stages. The finding that WUS is able to ectopically
activate PAN expression, along with the fact that PAN RNA
also persists in clv mutants
(Chuang et al., 1999),
suggests that WUS could at least partially mediate this feedback
regulation. In such a scenario, WUS at the same time contributes to the
activation of PAN and AG in a feed-forward loop at early
stages of flower development, while the repression of WUS by AG at
later stages would also lead to a reduction of PAN expression
(Fig. 7). The lack of
WUS repression in ag mutants
(Lenhard et al., 2001;
Lohmann et al., 2001) would in
turn cause ectopic activation of PAN. However, as only the regulatory
interactions between WUS and AG and PAN and AG have been
characterized mechanistically, the true nature of this regulatory module
remains to be elucidated. Finally, our work has revealed that other factors must act redundantly with PAN and that this network is sensitive to variation in environmental conditions. This finding shows that the combination of genetic perturbation with environmental variation can be a powerful tool to uncover redundant regulatory mechanisms that are normally not thought to be under environmental control.
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Footnotes |
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Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/136/10/1613/DC1
We thank Jürgen Berger for help with SEM, Christoph Schuster for plant material, Sascha Laubinger for discussion and Sarah Schilli for technical assistance. This work was supported by fellowships from the Konrad Adenauer Stiftung (A.T.M.) and Boehringer Ingelheim Fonds (H.W.), by NIH grant GM62932 (D.W.) and DFG-AFGN grant LO1450/2-1 (J.U.L.), as well as funds from the EMBO Young Investigator Programme and the HFSP Career Development Award to J.U.L., and the Max Planck Society. Deposited in PMC for release after 12 months.
* These authors contributed equally to this work 
Present address: Whitehead Institute for Biomedical Research, Cambridge, MA
02142, USA
Present address: California State University, Northridge, CA 91330, USA
Present address: Institute for Clinical Pharmacology, University of
Stuttgart, D-70376 Stuttgart, Germany
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DISCUSSION
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