1 Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo
113-8657, Japan
2 Graduate School of Biological Sciences, Nara Institute of Science and
Technology, Ikoma, Nara 630-0101, Japan
3 CREST, Japan Science and Technology Corporation, Tokyo 101-0062, Japan
* Author for correspondence (e-mail: akyozuka{at}mail.ecc.u-tokyo.ac.jp)
Accepted 24 April 2003
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SUMMARY |
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Key words: Rice inflorescence, Meristem identity, ERF transcription factor
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INTRODUCTION |
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The spikelet is the ultimate unit of the grass inflorescence and comprises
a series of modified leaves called bracts and florets. Among the bracts, the
one subtending the floral meristem is specifically called a lemma. The floral
meristem produces the floral organs palea, lodicules, stamens and
carpel that together with the subtending lemma are termed as a floret.
The number of florets per spikelet varies between grass species and in the
case of rice, a single floret is subtended by two pairs of bracts called empty
glumes and rudimentary glumes (Fig.
1E, Fig. 2C,D).
Usually, the structure containing the floret and the empty glumes, but not the
rudimentary glumes, is considered to be a rice spikelet
(Hoshikawa, 1989;
Bell, 1991
;
Takeoka et al., 1993
). Despite
the distinct terminology, molecular analyses based on the well-established ABC
model of floral organ identity have proved that lodicules are the counterparts
of dicot petals and indicate that the palea and possibly the lemma are
equivalents to sepals (Kang et al.,
1998
; Ambrose et al.,
2000
; Kyozuka et al.,
2000
; Goto et al.,
2001
). However, although grass florets are similar to dicot
flowers, the nature of the spikelet remains unclear.
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With the completion of the rice genome sequence
(http://rgp.dna.affrc.go.jp/)
and the availability of an abundant collection of mutants affecting
reproductive development (Kinoshita and
Takahashi, 1991; Murai and
Iizawa, 1994
; Kyozuka,
1999
), the forward genetics approach in rice is expected to be a
powerful strategy to identify genes involved in grass inflorescence
development. Among rice inflorescence mutants, frizzy panicle
(fzp) is of particular interest
(Fig. 2E-L). Although
inflorescence mutations tend to influence more than one type of meristem
(McSteen et al., 2000
;
Battey and Tooke, 2002
),
fzp shows defects only in spikelet development. In the inflorescence
of the fzp mutant, primary branch meristems develop normally but
secondary branch meristems are produced in place of all spikelets, resulting
in the formation of an abnormal inflorescence composed of a mass of branch
shoots (Komatsu et al., 2001
).
The reversion of spikelet meristems to branch meristems is very similar to the
phenotype observed in the ear of maize bd1 mutants and indicates that
FZP is also required to specify spikelet meristem identity. Here we
describe a more detailed analysis of the fzp phenotype and the
isolation of the FZP gene, which encodes an ERF transcription factor
and is the rice ortholog of the maize BD1 gene. Our data suggest that
FZP prevents the outgrowth of the axillary meristem within the
rudimentary glume and maintains the transition from spikelet to floral
meristem identity.
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MATERIALS AND METHODS |
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The fzp-4 and fzp-5 alleles were obtained from a pool of
approximately 9000 selfed lines carrying the maize Ac transposon as
previously described (Enoki et al.,
1999); fzp-3, fzp-KH1 and fzp-KH56 were obtained
by EMS-induced mutagenesis and fzp-FM44 was obtained by spontaneous
mutation. All alleles and fzp-like mutants were of the
japonica variety of Oryza sativa L. and the background
cultivars were: M201 for fzp-1; Shiokari for fzp-2;
Hanaetizen for fzp-3; Toride for fzp-4 and fzp-5;
Koshihikari for fzp-KH1 and fzp-KH56, and unknown for
fzp-FM44 (Table 1).
The wild-type cultivar used was Toride. Plants were grown at 27°C in a
greenhouse with 16 hours light and 8 hours darkness.
|
Mapping
Rough mapping of the FZP locus was performed using cleaved
amplified polymorphic sequence (CAPS) markers, which were constructed on the
basis of the sequence information provided by the National Institute of
Agrobiological Sciences (NIAS, Japan). dCAPS markers, constructed according to
Michaels and Amasino (Michaels and
Amasino, 1998), were utilized for the fine mapping of the
FZP locus. In the F2 generation of our mapping population
of fzp-3 japonica cv. Hanaetizen crossed to wild-type indica
cv. Kasalath, we detected linkage of the fzp mutation to the markers
RA1789 and 3817R with 5 mutant plants each out of 178. Recombinants were then
genotyped with dCAPS markers in the interval between 4016R and 3997R. This
delimited the FZP locus to a region of 119 kb on chromosome 7 covered
by the overlapping PAC clones AP004300 and AP004570. Further mapping was not
continued after the identification of the transposon-tagged allele.
Southern blot analysis and cloning of the FZP gene
DNA (5 µg) extracted from fzp-4 seedlings were digested with
EcoRI, separated by electrophoresis and blotted as described
previously (Enoki et al.,
1999). The C-terminal half of the maize Ac element was
amplified by polymerase chain reaction (PCR) using primers
5'-TCCAACAATGATTGGTGATCTCG-3' and
5'-CATATTTAACTTGCGGGACGGAAAC-3', and the resultant product was
used as probe. Inverse PCR (Trigrlia et
al., 1988
) of EcoRI-digested DNA was applied to isolate
the sequences flanking the Ac elements using primers
5'-CGGTTATACGATAACGGTCGGTAC-3' and
5'-TGAAGTGTGCTAGTGAATGTGACTTG-3' for the N-terminal flanks and
5'-TAAGGCATCCCTCAACATCAAATAG-3' and
5'-GATTACCGTATTATCCCGTTCG-3' for the C-terminal flanks. The
GenBank accession number of the FZP cDNA is AB103120.
Transient expression
The GAL4-responsive reporter construct (GAL4-LUC) contained five copies of
the GAL4 binding site in tandem and a minimal TATA region of the CaMV 35S
promoter, the firefly gene for luciferase (LUC) and a nopaline synthase (NOS)
terminator (Ohta et al.,
2000). The effector constructs were driven by the CaMV 35S
promoter and contained a GAL4 DNA-binding domain (GAL4DB) or the coding region
of FZP fused to the latter (GAL4DB-FZP). A translational enhancer
sequence from the tobacco mosaic virus (
) was placed upstream of the
translation initiation sites. Transient assays in Arabidopsis leaves
were performed by using the particle gun bombardment method as described
previously (Fujimoto et al.,
2000
; Ohta et al.,
2001
). Luciferase assays were performed with the dual-luciferase
reporter assay system. To normalize values after each transfection, the
Renilla luciferase gene under the control of the CaMV 35S promoter
was used as an internal control (Ohta et
al., 2000
). The values cited are averages, with standard
deviations, of results obtained from 3 independent experiments. Normalized
luciferase activity recorded after transfection with the GAL4-LUC plasmid
alone was set arbitrarily at 1.
In situ hybridization
The N-terminal and the C-terminal halves of the FZP coding region
excluding the ERF domain were amplified by PCR using three sets of primers as
follows: 5'-GTCATGAACACTCGAGGC-3' and
5'-CTCCCTGGCTCCTGCGC-3', 5'-CACATTGGCTCGTACGGTC-3' and
5'-GAGAAGAGGAAGTCGTGG-3', 5'-CCACGACTTCCTCTTCTCCG-3'
and 5'-CCGGCGACCATCTGC-3'. PCR products were cloned into p-GEM-T
vectors (Promega Corporation, Madison, USA), linearized and used as templates
for making digoxigenin-labeled sense and anti-sense RNA probes. The three
probes were used simultaneously for hybridization. Tissue fixation and in situ
hybridization procedures were performed as described previously
(Kyozuka et al., 2000), except
that sections were washed in SSC solution and two washes of 20 minutes were
performed after RNase treatment.
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RESULTS |
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We have previously described the phenotype of fzp2, a rice
inflorescence mutant that resembled the fzp mutant reported by
Mackill et al. (Mackill et al.,
1991; Komatsu et al.,
2001
). Complementation tests showed that fzp2 is allelic
to fzp (Materials and Methods) and, therefore, we redesignated the
later as fzp-1 and the former as fzp-2
(Table 1). Further analyses of
the morphology of fzp-2 inflorescences were performed. In
fzp-2 plants, the development of the SAM did not differ from
wild-type plants until primary branches were formed
(Komatsu et al., 2001
).
However, all meristems on a primary branch initiated secondary branches
without forming spikelets (Fig.
2E,F). These secondary branches were composed of several
bract-like structures arranged in an alternate phyllotaxy (inset in
Fig. 2F). Tertiary branches
were formed in the axils of the bract-like structures in the upper part of the
secondary branch, and they were also composed of bract-like structures with
apical higher order branches (Fig.
2G,H, Fig. 3A). SEM
analyses of fzp-2 tertiary branches revealed that higher order branch
meristems were formed at 90° to the previous order branches
(Fig. 3A,C). Considering that
spikelet meristems and spikelet organs are formed in an alternate phyllotaxy
in wild-type inflorescences, the phyllotaxy of bract-like structures in
fzp-2 indicates that the defect on the mutant occurs after the
acquisition of spikelet meristem identity, as we have observed previously
(Komatsu et al., 2001
).
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Rudimentary glumes with axillary meristems are produced in
fzp mutants
Every ectopic branch in the plants with weak and severe fzp
alleles produced several bract-like structures that developed alternately from
the main axis and appeared very similar to wild-type rudimentary glumes
(compare Fig. 2C,D with G,H,L).
Molecular markers for rudimentary glumes are not available at present.
Therefore, in order to establish if the bract-like structures were actually
rudimentary glumes, the cell types of these structures were examined more
closely by SEM.
In wild-type spikelets whereas the empty glumes had flat cells of regular shape that rarely exhibited hairs resulting in an overall smooth appearance, the rudimentary glume cells had an irregular shape and had hairs that could be short or long resulting in a rugous appearance (Fig. 4A-D). The bract-like structures of the mutants showed a cell type very similar to the one observed for rudimentary glumes with irregular shape and a protruding hair (Fig. 4E,F), strongly indicating that the bract-like structures were actually rudimentary glumes. Although empty glumes were only rarely observed in spikelets of the weak fzp-3 mutant, some had empty glume-like structures. SEM analyses revealed that their cell type was similar to that of wild-type empty glumes (Fig. 4G).
|
FZP is the rice ortholog of the maize BD1 gene
A map-based approach was initially applied to clone the FZP gene
(Materials and Methods). The FZP locus was delimited to a 119 kb
interval on chromosome 7 covered by two overlapping PAC clones, AP004570 and
AP004300 (Fig. 5A). At the same
time, one line showing the severe fzp phenotype (fzp-4) was
found in a population of transgenic rice plants carrying the maize Ac
element (Fedoroff et al.,
1983; Izawa et al.,
1997
). After detecting co-segregation of two tightly linked
Ac elements with the fzp phenotype
(Fig. 5B), the region flanking
these elements was isolated and sequenced. Both Ac elements were
inserted on the region of chromosome 7 corresponding to the AP004570 PAC clone
approximately 3 kb apart from each other
(Fig. 5A). No genes were
predicted around the proximal Ac element, however, the distal
Ac element was inserted in an ORF encoding a putative protein
containing a sequence similar to the ethylene-responsive element-binding
factor (ERF) domain. Alterations in this ORF were found in the other four
fzp alleles and also in fzp-FM44, fzp-KH56 and
fzp-KH1, which were then redesignated as fzp-6, fzp-7 and
fzp-8, respectively (Fig.
6A, Table 1). The
sum of the results obtained from the map-based analysis, the transposon
tagging and the finding of alterations in all fzp lines, led us to
conclude that this ERF domain gene indeed represents the FZP
gene.
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The ERF domain of FZP is composed of 58 amino acids and is localized close
to the N terminus of the protein. From the length and position of the ERF
domain within the amino acid sequence, FZP was classified as a class II ERF
protein (Fujimoto et al.,
2000). The ERF domain of FZP showed high sequence similarity to
the domains of other class II ERFs, such as the Arabidopsis LEAFY
PETIOLE (LEP) (van der Graaff,
2000
) and ENHANCER OF SHOOT REGENERATION1 (ESR1)
(Banno et al., 2001
), with
which FZP shares 90% and 72% identity, respectively
(Fig. 6B). However, no
significant homology was found outside the ERF domain. No other genes with
significant overall identity to FZP were found in homology searches
of the public databases, but the cloning of FZP/BD1-like
genes from other grass species has been reported
(Chuck et al., 2002
).
The ERF domain and the acidic domain are essential for proper FZP
function
ERF transcription factors were first isolated as proteins that bound to the
cis-acting motif known as the GCC-box found in the promoters of defense genes,
the expression of which is induced by ethylene
(Sessa et al., 1995;
Ohme-Takagi and Shinshi,
1995
). The fzp-2 and fzp-7 mutations caused an
alteration of one of six conserved amino acids of the ERF domain that are
thought to confer GCC box-specific binding
(Allen et al., 1998
;
Hao et al., 1998
) and resulted
in severe fzp phenotypes (Fig.
6, Table 1).
Alteration of a conserved amino acid of the ERF domain not required for
specific GCC-box binding in fzp-3, however, resulted in the weak
fzp phenotype, suggesting that the FZP transcription factor may also
regulate its target(s) by GCC box-mediated gene expression.
Three other alleles had mutations in the conserved C-terminal region
(Fig. 6A). In fzp-4
and fzp-1, the insertion of an Ac element and a
Houba copia-type retroelement
(Panaud et al., 2002) caused
the formation of putative premature stop codons upstream and at the beginning
of the acidic domain, respectively, and resulted in severe phenotypes
(Table 1). In fzp-6,
an insertion of a putative copia-like retrotransposon caused the formation of
a stop codon at the end of the acidic domain, leading to the
temperature-sensitive phenotype. The formation of premature stop codons before
the acidic region in fzp-1 and fzp-4 might have resulted in
the formation of proteins lacking transcriptional activation activity, leading
to the severe phenotypes observed. Although the molecular basis of the
temperature-sensitive phenotype of fzp-6 is unknown, the fact that
three fzp alleles had mutations at the C terminus strongly indicate
that this conserved region must also be necessary for proper FZP function in
addition to the ERF domain.
In addition, two more alleles produced the severe fzp phenotype.
In fzp-8, a single nucleotide base change resulted in the formation
of a premature stop codon at the end of the ERF domain that might result in a
non-functional product. In fzp-5, no mutation was detected within the
FZP sequence, but an insertion of Karma, a LINE-type
retroelement (Komatsu et al.,
2003), was found approx. 2.5 kb upstream of the FZP gene
at a site that is 9 bp distant from the insertion point of the second
cosegregating Ac element of fzp-4. As a severe phenotype is
observed for fzp-5, this region might be a cis-acting element of
FZP and, in this case, may also account for the severe phenotype
observed for fzp-4 alleles. Alternatively, as transposon activity has
been associated with epimutations found in a variety of organisms from plants
to mammals (reviewed by Martienssen and
Colot, 2001
; Whitelaw and
Martin, 2001
), we cannot rule out the possibility that the
insertion of Karma causes the epigenetic effects in
fzp-5.
FZP functions as a transcriptional activator
The ability of FZP to regulate transcription in plant cells was tested by
using transient assays (Fig.
6C). A luciferase (LUC)-encoding reporter gene, GAL4-LUC, which
contains five copies of the yeast GAL4-binding site fused to LUC, and an
effector plasmid, GAL4DB-FZP, consisting of the coding region of FZP
fused to the GAL4 DNA-binding domain under the control of the cauliflower
mosaic virus (CaMV) 35S promoter (Fig.
6C left) were delivered to Arabidopsis leaves by particle
bombardment. LUC activity increased 16.6-fold when the reporter plasmid was
co-expressed with the FZP effector plasmid
(Fig. 6C right). The GAL4
DNA-binding domain alone (GAL4DB) also increased LUC activity 4.7-fold.
Nevertheless, the increase in LUC activity induced by GAL4DB-FZP was 3.5 times
higher than the one induced by GAL4DB, and indicates that FZP functions as a
transcriptional activator.
FZP is expressed at the axils of rudimentary glumes
primordia
The temporal and spatial expression of FZP was determined by in
situ hybridization analyses. FZP expression was restricted to a very
short period during the development of inflorescences
(Fig. 7). FZP RNA was
first detected at the early stage of spikelet meristem (SM) development, when
the primordium of the outer rudimentary glume is starting to become apparent
(Fig. 7A,B). The examination of
several consecutive sections revealed that FZP expression extended to
a half-ring domain, at the base of which the rudimentary glume (RG) primordium
developed (Fig. 6E-G). While
the expression level in the outer RG axil decreased, expression at the
opposite side of the SM, where the inner RG develops, increased
(Fig. 7C). FZP
expression in the axil of the inner RG could be detected until the time the
outer empty glume primordium began to form
(Fig. 7D). It should be noted
that no axillary meristem formation was observed in the axils of rudimentary
glume primordia in wild-type spikelets. No signal was observed for sense probe
controls (data not shown). A scheme representing the pattern of FZP
expression is shown in Fig. 7J. The expression pattern of the FZP gene was very similar to the one
observed for BD1, whose transcripts were detected in a semicircular
domain above the developing glumes, and it strongly supports our proposal that
rudimentary glumes are the actual counterparts of the glumes of other grass
species.
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DISCUSSION |
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FZP maintains floral fate
The phyllotaxy of ectopic branch meristem formation and the generation of
ectopic rudimentary glumes indicated that the meristems formed in the
inflorescence of fzp mutants had acquired spikelet meristem (SM)
identity. In addition, the phenotype caused by the weak alleles indicated that
these SMs had the capacity to form floral organs if they acquired floral
meristem identity. In the wild-type inflorescence, the SM proceeds to the
generation of empty glumes without forming axillary meristems from rudimentary
glumes. In contrast, the defect of fzp mutants was the generation of
meristems in the axils of rudimentary glumes. By integrating the information
above, it is possible to explain the function of FZP in two ways
(Fig. 8). First, the primary
function of FZP is the suppression of shoot branching within the spikelet
(Model 1). Second, FZP is a positive regulator of floral meristem identity
(Model 2). We showed that FZP is expressed in a half-ring pattern in
a region immediately above where rudimentary glumes are formed, which also
coincides with the region where axillary meristems are generated in
fzp mutants. From this data we favor the first interpretation that
FZP inhibits axillary meristem formation, but the second possibility cannot be
ruled out. In both cases, the transition from spikelet to floral identity is
prevented in fzp mutants and ectopic axillary meristems behave as SMs
generating rudimentary glumes with axillary meristems that reiterate the same
process.
|
The ERF domain exhibits a novel mode of DNA recognition by a ß-sheet
structure. NMR analyses revealed that the majority of the conserved residues
in ERF sequences are necessary for either the stabilization of the protein
structure or DNA recognition. Six of these residues have both attributes and
are responsible for the specific recognition of the GCC-box by the ERF domain.
It has been proposed that alteration of these residues could cause truncation
in the binding geometry, affecting specificity
(Allen et al., 1998;
Hao et al., 1998
). Among the
eight fzp alleles examined in this study, three showed an amino acid
exchange within the ERF domain. Substitution of one of these six residues
caused severe phenotypes in fzp-2 and fzp-7. In contrast, in
the weak fzp-3 allele substitution of an amino acid that was shown to
confer only structural stability by NMR analysis was found. Our data is
therefore consistent with the results obtained from in vitro analyses of
GCC-box mediated DNA-protein interaction. Although the features of ERF
proteins as transcription factors are well studied in vitro, their actual in
vivo functions are less understood owing to the lack of loss-of-function
mutants. So far, Arabidopsis ABI4 and the maize BD1 are the
only ERF family genes for which loss-of-function mutants are reported
(Finkelstein et al., 1998
;
Chuck et al., 2002
). The
identification of a series of fzp mutant alleles will therefore be
useful for further studies on the molecular function of ERF transcription
factors in plant development.
A conserved mechanism of inflorescence formation unique to
grasses
We have determined that the phenotype of fzp mutants is analogous
to the phenotype of bd1 mutants. Similarly, the expression patterns
and the predicted functions of FZP and BD1 are extremely
similar. The conservation of function of two ERF transcription factors, whose
expression is specific to spikelet meristems and whose sequence is conserved
in other grass species but is not found in the model dicot specie
Arabidopsis, indicates that an additional level of genetic regulation
is required for the formation of inflorescences in grasses. The identification
of other genes acting upstream or downstream in this regulatory pathway is
expected to clarify the genetic framework that directs the transition from
branch to spikelet and spikelet to floret meristems, and possibly the
integration with the already known genes that regulates the formation of
floret organs (McSteen et al.,
2000; Goto et al.,
2001
).
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ACKNOWLEDGMENTS |
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