Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, S-90183 Umeå, Sweden
Author for correspondence (e-mail:
ove.nilsson{at}genfys.slu.se)
Accepted 23 February 2005
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SUMMARY |
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Key words: Arabidopsis, Leaf development, Flower organ abscission, BLADE ON PETIOLE1, JAGGED, knox genes, LEAFY
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Introduction |
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The identity of the Arabidopsis SAM is controlled by class I knox
genes including BREVIPEDICELLUS (BP), KNOTTED-like
from Arabidopsis thaliana2 (KNAT2), KNAT6 and
SHOOTMERISTEMLESS (STM)
(Reiser et al., 2000). In
order to promote normal leaf development, the expression of these genes needs
to be tightly suppressed in the incipient leaf primordium and in the
developing leaf. This suppression is partly attributable to the action of
genes like ASYMMETRIC LEAVES1 (AS1), AS2 and
BLADE ON PETIOLE1 (BOP1)
(Byrne et al., 2000
;
Ha et al., 2004
;
Ha et al., 2003
;
Ori et al., 2000
;
Semiarti et al., 2001
).
Loss-of-function mutations in AS1 and AS2 lead to ectopic
knox-gene expression in the leaf, which is associated with the
formation of lobed rosette leaves with ectopic leaf-like organs on their
petioles (Byrne et al., 2000;
Ori et al., 2000
;
Semiarti et al., 2001
). This
phenotype is also seen, although much weaker, in a bop1 null mutant
(Ha et al., 2004
). BOP1 has
recently been shown to belong to a family of proteins containing BTB/POZ
domains and ankyrin repeats that have not previously been associated with the
regulation of plant development (Ha et
al., 2004
). Ectopic leaf formation is also caused by strong
constitutive expression of BP (previously KNAT1) from the
Cauliflower Mosaic Virus 35S promoter
(Chuck et al., 1996
;
Lincoln et al., 1994
),
suggesting that the as1, as2 and bop1 mutant phenotypes are
caused, at least partly, by the ectopic knox-gene expression.
However, the originally described bop1-1 mutant also displays another
leaf development phenotype that is not seen in as1, as2 or
bop1 null mutants. It develops extensive growth of the proximal parts
of the leaf lamina, leading to enlarged leaves without petioles
(Ha et al., 2003
). It has been
suggested that the strong bop1-1 mutant phenotype is caused by a
dominant-negative interaction between the mutant allele and the wild-type
allele, which may interfere with the normal function of other proteins in the
leaf morphogenesis pathway (Ha et al.,
2004
). It has also been suggested, but not shown, that the very
weak phenotype of the bop1 null mutant may be attributed to
functional redundancy with a similar gene
(Ha et al., 2004
).
Recently, several genes have been identified that control the balance
between cell division and cell differentiation in the proximal versus distal
parts of the leaf. The JAGGED (JAG) gene encodes a
transcription factor with a C2H2 zinc finger domain
(Dinneny et al., 2004;
Ohno et al., 2004
). In
jag mutants, the growth of distal parts of leaves, sepals, petals and
stamens is suppressed, leading to these organs being smaller than wild type,
with serrated margins (Dinneny et al.,
2004
; Ohno et al.,
2004
). JAG is expressed in the distal parts of leaves and
petals, and appears to have a role in the maintenance of cell-division
activity. JAG expression is necessary for the development of bracts
in lfy mutants, as well as for the development of bract-like organs
in ap1 and ap2 mutant backgrounds
(Dinneny et al., 2004
;
Ohno et al., 2004
).
Interestingly, ectopic JAG expression in a wild-type background leads
to the production of bracts and to ectopic growth of the proximal parts of the
leaf, a phenotype that is very similar to that of bop1-1 mutants,
suggesting that these genes may interact functionally
(Dinneny et al., 2004
;
Ha et al., 2003
;
Ohno et al., 2004
).
We have cloned and characterized the Arabidopsis BOP1 gene as well as a functionally redundant closely related gene that we call BOP2. Through analysis of double mutants, we show that the BOP genes have a previously uncharacterized role in the suppression of bract formation and that this suppression is achieved through a strong synergistic interaction with the flower meristem-identity gene LFY. We also show that the BOP genes are expressed in proximal parts of plant organs in a region that is non-overlapping with that of JAG expression, and that bop1 bop2 mutants display ectopic JAG expression in regions corresponding to the regions of wild-type BOP expression. Taken together, our data show that BOP1 and BOP2 are important repressors of both knox gene and JAG expression in the developing leaf, and that the coordination of LFY, BOP and JAG expression is important for the balance between cell-division activity and differentiation sculpting the architecture of the leaf and the development of lateral organs.
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Materials and methods |
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Wild type was Columbia (Col-0). The bop2-1 and bop2-2
mutants were identified after screening of the Salk T-DNA insertion lines
(Alonso et al., 2003), and seed
was obtained from the Nottingham Arabidopsis Stock Center (NASC). The seed
stock numbers were N533520 (bop2-1) and N575879 (bop2-2).
The bop1-5 was identified after screening of the Syngenta SAIL T-DNA
insertion lines (Sessions et al.,
2002
) as line 14.c02. The bop1-6D mutation was identified
after screening of activation tagged lines transformed with pSK1015
(Weigel et al., 2000
). Seeds
from jag-1 and jag-5D
(Dinneny et al., 2004
) were
kindly provided by José Dinneny and Detlef Weigel. The lfy-12
mutant is a null mutant in Col-0.
Cloning of BOP1 and BOP2 cDNA
Plasmid rescue of bop1-6D genomic DNA was performed as described
previously (Weigel et al.,
2000). 5' and 3' RACE (rapid amplification of cDNA
ends) of BOP1 and BOP2 cDNA was performed using the SMART
RACE cDNA amplification kit (CLONTECH) according to the manufacturer's
instructions. Full-length cDNA was generated using gene-specific primers B1-1
and B1-2 for BOP1, and B2-1 and B2-2 for BOP2 (see Table S1
in the supplementary material for oligonucleotide sequences).
Protein alignment and phylogenetic analysis
Protein sequences were aligned using the Clustal W program
(Thompson et al., 1994)
followed by a phylogenetical analysis using the PAUP* program
(version 4.0b10) (Swofford,
2003
).
Construction of transgenic lines
The 35S::BOP1 and 35S::BOP2 vectors were constructed by
placing the full-length cDNA sequences from BOP1 and BOP2
downstream of the Cauliflower Mosaic Virus (CaMV) 35S promoter in the
binary vector pPCV702 (Walden et al.,
1990). The BOP1::GUS and BOP2::GUS vectors were
constructed by placing 2 kb of the genomic region 5' of the
BOP1 and BOP2 translational start sites upstream of the
reporter gene uidA (GUS) in the binary vector pPCV812
(Walden et al., 1990
). The
BOP1 promoter region was amplified using the gene specific primers
B1p-1 and B1p-2, whereas the BOP2 promoter was amplified with B2p-1
and B2p-2. Transgenic Arabidopsis lines were generated by the floral
dipping method (Clough and Bent,
1998
).
Northern blot
RNA was extracted from 9-day-old bop1-6D and Col-0 wild-type
plants using a Qiagen RNA plant minikit (Qiagen). Total RNA (10 µg) was run
on a 0.8% formaldehyde gel and blotted on a Hybond-N+ membrane (Amersham
Biosciences) as described (Sambrook et
al., 1989). The membrane was probed with
[
32P]dATP labelled DNA from a 500 bp fragment from exon 1 of
the BOP1 gene, and washed as described
(Church and Gilbert,
1984
).
RT-PCR
Total RNA was isolated from 11- and 25-day-old Col-0 wild-type plants using
the RNAqueous kit (Ambion). cDNA synthesis was performed using the SuperScript
II Reverse Transcriptase (Invitrogen) according to the manufacturer's
instructions. The primers used were B1-3 and B1-4 for BOP1, and B2-3
and B2-4 for BOP2. The primers are flanking the intron of both
BOP1 and BOP2 in order to selectively amplify the respective
cDNA. The PCR program used was 94°C for 3 minutes, then 94°C for 15
seconds, 57°C for 30 seconds and 72°C for 30 seconds for 29-31 cycles
(as indicated in Fig. S2 in supplementary material), followed by 72°C for
10 minutes. An 18S ribosomal RNA fragment was amplified as a control
using the QuantumRNA Universal 18S kit according to the manufacturer's
instructions (Ambion). 18S competimers in a ratio of seven to three
were added to equalize the expression of the target gene with that of the
18S control.
Real-time RT-PCR
RNA was extracted from 8- and 11-day-old Col-0 wild-type and bop1-5
bop2-2 double mutant plants grown in long days. Leaf 1 and 2 were sampled
together with the apical part of the shoot carrying leaves smaller than 1 mm.
Poly(dT) cDNA synthesis was performed using the iScript cDNA Synthesis Kit
(BIO-RAD) according to the manufacturer's instructions. Quantification was
performed on an iCycler iQ real-time PCR detection system (BIO-RAD) using the
BIO-RAD iQ SYBR Green Supermix. PCR was carried out in 96-well optical
reaction plates heated to 95°C for 3 minutes, followed by 45 cycles of 10
seconds at 95°C and 30 seconds at 54°C, followed by a melting curve
analysis from 54°C to 95°C with 0.5°C per step to verify that
quantification was not caused by primer self-amplification but by a pure and
common PCR product. For each quantification conditions were, 1>E>0.95
and r2>0.98, where E is the PCR efficiency and r2
corresponds to the correlation coefficient obtained with the standard curve.
Three replicate assays were preformed with independently isolated RNA and each
sample was loaded in triplicates. Results were normalized to the expression of
18S ribosomal RNA, then to the value of the wild-type control. The
primers used to detect JAG were J-1 and J-2, whereas JGL was
detected using JG-1 and JG-2.
In situ hybridization
In situ hybridization was performed on 10 µm thick sections as described
previously (Jackson, 1992).
Templates for the digoxigenin-labelled RNA probes were generated by amplifying
gene-specific sequences using the primers B2-5 and B2-6 for the BOP2
probe, and J-3 and J-4 for the JAG probe. The BOP2 probe
spans the end of exon 2, which is divergent between BOP1 and
BOP2. The products were ligated into the vector pGEM-T easy
(Promega), linearized using NcoI (BOP2) and HindIII
(JAG); ligation was followed by in vitro transcription using SP6
(BOP2) and T7 (JAG) polymerase to generate antisense probes.
As a control, in situ hybridization using the BOP2 probe on sections
from the bop2-2 mutant and the JAG probe on sections from
the jag-1 mutant was performed. None of these hybridizations resulted
in a detectable signal (results not shown).
Analysis of GUS activity
For analysis of GUS activity in BOP1::GUS and BOP2::GUS
plants, plants were harvested and tissue samples were subjected to
histochemical staining of the GUS activity as described
(Weigel and Glazebrook, 2002).
Samples for histological analysis were fixed in 50% ethanol, 40% LR-WHITE
(TAAB Laboratories) and 10% PEG 400 for 20 minutes at room temperature. The
samples were transferred to 90% LR-WHITE with 10% PEG 400, put into a capsule
and baked overnight at 65°C. Sections (10 µm) were mounted in glycerol
before microscopy.
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Results |
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Defects caused by loss of BOP1 and BOP2 function
The BOP1 and BOP2 genes display a high level of
functional redundancy. The bop2-2 mutant plants have no discernible
mutant phenotypes (not shown), whereas the bop1-5 loss-of-function
mutant plants display a very weak mutant phenotype that can only be detected
under growth in short-day conditions. In short days, all bop1-5
mutants form a few ectopic leaves on the rosette leaves
(Fig. 2A), a phenotype that is
also seen, but more weakly and in only 2-3% of the plants, in the previously
described bop1-3 and bop1-4 mutants
(Ha et al., 2004). By
contrast, the bop1 bop2 double mutants display severe developmental
defects that are very similar to all previously described bop1-1
mutant phenotypes (Fig. 2). The
double mutant combinations bop1-5 bop2-1 and bop1-3 bop2-2
both show the same, but slightly weaker, mutant phenotype as the bop1-5
bop2-2 double mutant (data not shown). The bop1 bop2 double
mutant has a retarded growth compared with wild type
(Fig. 2B), but eventually
reaches the same overall height. The most dramatic developmental effect is on
leaf development, where bop1 bop2 leaves display extensive lobe
formation and ectopic growth of the leaf lamina, producing larger leaves
without petioles. This is true for all leaves, but is especially evident for
leaves 1 and 2 (Fig. 2C). In
wild-type plants these leaves stop growing at a much earlier stage than the
other rosette leaves and are consequently much smaller. In bop1 bop2
plants the proximal parts of the leaves continue growing throughout
development and, therefore, reach gigantic proportions compared with leaves 1
and 2 in wild-type plants (Fig.
2C). As previously shown for the bop1-1 mutant, leaves of
the bop1 bop2 double mutants frequently develop ectopic organs along
the petioles and midveins (results not shown).
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Expression patterns of BOP1 and BOP2
BOP1 and BOP2 transcripts were detected in all plant
organs tested, although at various levels (see Fig. S2 in supplementary
material). BOP1 is not as strongly expressed as BOP2, but
can be detected in all the tissues displaying BOP2 expression. This
is not unexpected given that the two genes display almost complete functional
redundancy.
A more detailed picture of BOP1 and BOP2 expression was
obtained by in situ localization of BOP1 and BOP2 mRNA.
BOP1 has previously been shown to be expressed in leaf and flower
primordia, and at the base of developing leaves, sepals and petals
(Ha et al., 2004). In our
analysis BOP1 and BOP2 displayed very similar expression
patterns (BOP1 expression is not shown here), but the BOP2
signal was always stronger. In vegetative shoot apical meristems weak
expression of BOP2 can be detected in incipient leaf primordia
(Fig. 4A). Later in
development, BOP2 expression is restricted to the base of the
developing leaf (Fig. 4A). In
inflorescence meristems, BOP2 is expressed at stronger levels at the
sites of the incipient floral primordia
(Fig. 4B). The expression then
disappears in the young flower primordia. At later stages the expression
reappears, but is confined to the proximal parts of the developing floral
organs (Fig. 4B).
To further analyze the expression patterns of BOP1 and BOP2, transgenic plants expressing promoter fusions to the reporter gene ß-glucuronidase (GUS; uidA) were analyzed. GUS expression corresponded well with the patterns found in the in situ localization analysis, showing that the BOP genes are expressed in the proximal margins of young developing leaves and along the midveins (Fig. 4C-E). At later stages, BOP expression is confined to the base of the petioles (Fig. 4F,G) and the proximal parts of the floral organs (Fig. 4H). At even later stages strong BOP expression can be seen at the base of the floral organs in an area overlapping the floral organ abscission zone (Fig. 4I). There is also expression at the base of the pedicels (Fig. 4I).
BOP1 and BOP2 regulate the expression of JAGGED and JAGGED-LIKE
It has previously been shown that expression of the putative transcription
factor JAG is necessary for the proper development of distal parts of
leaves and petals, as well as for bract formation in the lfy, ap1 and
ap2 mutants (Dinneny et al.,
2004; Ohno et al.,
2004
). Furthermore, ectopic JAG expression is sufficient
to induce growth of proximal parts of leaves, and leads to bract formation in
the wild type (Dinneny et al.,
2004
; Ohno et al.,
2004
). These bracts are tipped with stigmatic papillae in late
development stages, and JAG has been shown to suppress floral
meristem identity (Dinneny et al.,
2004
). Because all of these phenotypes are also seen in bop1
bop2 mutants, we decided to investigate how BOP1 and
BOP2 affect the expression of JAG. However, because
JAG has a close homolog in Arabidopsis called
JAGGED-LIKE (JGL) and it has been speculated that
JAG and JGL might be at least partially functionally
redundant (Dinneny et al.,
2004
; Ohno et al.,
2004
), we also analyzed the expression of JGL.
In 11-day-old leaves 1 and 2 of bop1 bop2 mutants, and in shoot
apices, JAG and JGL expression was dramatically increased
when compared with wild type (Fig.
5A,C). As it has been shown previously that ectopic expression of
JAG is sufficient to promote leaf growth
(Dinneny et al., 2004;
Ohno et al., 2004
), this
suggests that the increased growth of leaves 1 and 2 in bop1 bop2
mutants could at least partially be caused by the increased JAG
expression, and that BOP1 and BOP2 function as repressors of JAG and
JGL transcription. This hypothesis was further corroborated by
analyzing the expression of JAG and JGL in bop1-6D
plants. In leaves 1 and 2, as well as in shoot apices, JAG and
JGL expression was decreased in bop1-6D when compared with
wild type (Fig. 5B,D). In situ
localization of JAG mRNA in wild-type and bop1 bop2 mutant
plants showed that JAG and BOP display non-overlapping
expression patterns in the leaves and flowers of wild-type plants
(Fig. 6A,B). Whereas
JAG is expressed in the distal parts
(Fig. 6A), the BOP
genes are expressed in the proximal part of the leaves and flowers
(Fig. 6B). Interestingly, the
bop1 bop2 double mutants display ectopic JAG expression in
the areas of wild-type BOP expression
(Fig. 6C), confirming that
BOP expression represses JAG, and that the balance between
BOP and JAG expression is an important determinant of leaf
architecture. By contrast, BOP1 and BOP2 expression was not
significantly altered in either the jag-1 loss-of-function mutant or
the jag-5D activation-tagged mutant, as determined by RT-PCR (data
not shown). Furthermore, although JAG is not expressed in wild-type
incipient flower primordia, it is strongly expressed in the bract primordia
that form in bop1 bop2 double mutants
(Fig. 6D). This suggests that
the formation of bracts in bop1 bop2 mutants is at least partially
caused by upregulation of JAG expression in the cryptic bract and
that the BOP genes contribute to suppression of Arabidopsis
bracts by repressing JAG.
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Discussion |
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The regulation of flower organ abscission
Here we show that the bop1-5 bop2-2 mutants display additional
mutant traits to those previously described for the bop1-1 mutant
(Ha et al., 2003). These
include the suppressed abscission of flower organs
(Fig. 2I-K), bract formation
(Fig. 2D-G,
Table 1) and delayed flower
initiation under short-day conditions (Fig.
2H). The flower organ abscission phenotype correlates to strong
expression of the BOP genes in the presumed flower organ abscission
zone (Fig. 4I). Interestingly,
this expression overlaps with that of the INFLORESCENCE DEFICIENT IN
ABSCISSION (IDA) gene, and ida mutants, just like
bop1 bop2, never shed their flower organs
(Butenko et al., 2003
). As
ectopic expression of neither JAG nor knox genes has been
reported to cause suppression of floral organ abscission, this phenotype might
reflect a BOP-specific function. IDA belongs to a family of small
proteins encoding putative receptor ligands. It will be interesting to
determine whether the BOP proteins and IDA physically interact.
Suppression of bract formation
Our data reveals that there is a strong functional cooperation between the
BOP genes and LFY in the suppression of Arabidopsis
bract formation. The BOP genes are already expressed at weak levels
in the incipient leaf primordia and at considerably higher levels in the
incipient floral/bract primordia (Fig.
4A,B), although at this point we cannot determine whether
BOP expression is specifically localized to the cryptic bract. The
expression pattern is consistent with a role in bract suppression and is very
similar to that of LFY (Blazquez
et al., 1997). The cooperation between the BOP genes and
LFY also provides an explanation to the floral initiation defect seen
in bop1 bop2 mutants grown under short-day conditions. Floral
initiation in Arabidopsis requires the simultaneous action of two
tightly connected developmental processes: suppression of leaf development and
activation of flower development. We show here that bop1-5 bop2-2
mutants are late flowering under short-day conditions and form more leaves
than wild-type plants before the first flower is initiated
(Fig. 2H, Table S2 in
supplementary material). Under short-day conditions LFY expression is
lower than under long-day conditions
(Blazquez et al., 1998
). It is
possible that, in a bop1 bop2 mutant grown under short days, the
ability of LFY to suppress the leaf development program is severely
reduced. The development of the leaf could affect the ability of LFY
to promote the development of the floral primordium, leading to the production
of more leaves. Later in development, LFY might be able to induce
floral meristem identity, although the associated leaf still develops into a
bract. That the LFY-BOP cooperation is important also for
the development of the floral meristem can be deduced from the fact that the
inflorescences of bop1 bop2 lfy mutants, in contrast to
lfy-12 or bop1 bop2 mutants, revert to forming leaves with
no growth of axillary meristems after forming flower-like structures
(Table 1). In this context it
is also interesting to note that ectopic expression of JAG can
suppress flower meristem identity and cause a lfy mutant-like
phenotype (Dinneny et al.,
2004
; Ohno et al.,
2004
) very similar to that of bop1 bop2 in short
days.
The BOP genes and JAG/JGL
We show here that BOP1 and BOP2 are repressors of JAG and
JGL transcription, as in bop1 bop2 mutants JAG and
JGL both display strong ectopic expression. Because many aspects of
the bop1 bop2 mutant phenotype are very similar to the phenotype of
35S::JAG overexpressors, including bract formation, enhanced
outgrowth of stipules, ectopic leaf lamina formation and suppression of flower
meristem identity (see above) (see also
Dinneny et al., 2004;
Ohno et al., 2004
), it seemed
likely that these aspects of the bop1 bop2 phenotype could be
explained by the ectopic expression of JAG. It has also been shown
that JAG expression is necessary for the outgrowth of bracts in
lfy and ap1 mutants
(Dinneny et al., 2004
;
Ohno et al., 2004
). However,
we show here that in a bop1 bop2 jag triple mutant, JAG
expression is no longer necessary for the outgrowth of bracts, and there is no
suppression of the bop1 bop2 mutant phenotype. Obviously, the need
for JAG expression in the developing bract has been replaced by
another factor regulated by the BOP genes. We propose that the
simplest explanation to this result is the fact that the BOP genes
repress the expression of both JAG and the very similar gene
JGL (Fig. 5), and that
JGL can functionally replace JAG when overexpressed. This
hypothesis could be tested in a bop1 bop2 jag jgl quadruple mutant,
but that analysis will have to await the characterization of a jgl
mutant.
Molecular function of the BOP genes
The BOP proteins are predicted to contain BTB/POZ domains and ankyrin
repeats, suggesting a role in protein-protein interaction
(Fig. 1). The BTB/POZ domain is
thought to provide a scaffold for the organization of higher-order structures,
such as the cytoskeleton, chromatin, and ubiquitin ligase substrate complexes
(Ahmad et al., 1998;
Geyer et al., 2003
;
Kobayashi et al., 2000
).
Interestingly, the BTB/POZ domain-containing gene PLZF has been shown
to mediate transcriptional repression by recruiting histone deacetylase
complexes (Lin et al., 1998
),
providing an interesting parallel to the transcriptional repression activity
of the BOP genes. Furthermore, the BTB/POZ domain has been shown to
interact with elements of the basal transcriptional machinery suggesting that
this domain can perform many different functions in transcriptional complexes
(Pointud et al., 2001
). The
only previously characterized proteins containing both BTB/POZ domains and
ankyrin repeats are the transcription factors NPR1 and NPR4, which have been
shown to interact differentially with members of the TGA family of
basic-domain/Leucine zipper (bZIP) transcription factors (reviewed by
Dong, 2004
;
Liu et al., 2005
). Although
most of the TGA family members have been implicated in the regulation of
glutathione S-transferase and pathogenesis-related (PR) genes
(reviewed by Dong, 2004
), one
TGA factor gene, PERIANTHIA (PAN), has been shown to be
involved in the restriction of organ initiation from the flower meristem
(Chuang et al., 1999
). The PAN
protein is localized in both floral and vegetative tissues, and it has been
suggested that PAN exerts its action through interaction with spatially and/or
quantitatively regulated factors that might heterodimerize with PAN. It will
be interesting to investigate whether the BOP proteins interact with PAN or
other members of the TGA factor family.
In conclusion, we show here that the BOP genes affect leaf growth and development by influencing two different processes. First, together with AS1 and AS2, the formation of ectopic meristem activity on the leaf is prevented, most likely through their mutual repression of knox gene activity in the leaf. Secondly, probably through repression of JAG/JGL and through a strong cooperation with the flower meristem-identity gene LFY, the development of proximal parts of the leaf and the development of the bracts are suppressed. As the BOP proteins contain domains indicative of a role in protein-protein interaction it will be very interesting to investigate whether the BOP proteins interact with any of the known proteins affecting knox gene regulation or the regulation of cell-cycle activity in the leaf. Elucidating such phenomena should significantly advance our understanding of how the network of regulators affecting leaf initiation and growth interact in order to sculpt the development of the leaf as well as other lateral organs.
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ACKNOWLEDGMENTS |
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Footnotes |
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Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/132/9/2203/DC1
* These authors contributed equally to this work
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