1 Graduate School of Agricultural and Life Sciences, University of Tokyo,
Bunkyo-ku, Tokyo 113-8657, Japan
2 Bioscience and Biotechnology Center, Nagoya University, Chikusa-ku, Nagoya
464-8601, Japan
3 Japan Tobacco Incorporated, Aoba-ku, Yokohama 227-8512, Japan
4 Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-8657,
Japan
* Author for correspondence (e-mail: ahirano{at}boil.s.u-tokyo.ac.jp)
Accepted 14 September 2004
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SUMMARY |
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Key words: CLV signaling, Floral meristem, FLORAL ORGAN NUMBER1, Flower development, Rice
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Introduction |
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The clv1, clv2 and clv3 mutations cause enlargement of
the vegetative and inflorescence meristems, in addition to the floral
meristem, leading to abnormal phyllotaxy, inflorescence fasciation and
enlargement of floral meristems (Clark et
al., 1993; Clark et al.,
1995
; Kayes and Clark,
1998
). Genetic analysis has shown that these three genes act in
the same pathway to regulate meristem size. CLV1 encodes a
receptor-like protein consisting of an extracellular leucine-rich repeat (LRR)
domain, a small transmembrane domain, and a cytoplasmic serine/threonine
kinase domain (Clark et al.,
1997
). CLV2 encodes a similar protein that has an LRR
domain but lacks the cytoplasmic kinase domain
(Jeong et al., 1999
). Both
proteins are thought to form heterodimers and the LRR domains appear to act in
ligand binding. CLV3 encodes a small peptide that is secreted into
the intercellular region and acts as a putative ligand for the CLV1-CLV2
signal transduction complex (Fletcher et
al., 1999
; Rojo et al.,
2002
).
This CLV signaling pathway negatively regulates the gene WUSCHEL
(WUS), which controls stem cell fate in the meristem
(Brand et al., 2000;
Laux et al., 1996
;
Mayer et al., 1998
;
Schoof et al., 2000
).
Mutations in the CLV genes fail to repress WUS activity,
resulting in expansion of the WUS expression domain and enlargement
of the meristem. Conversely, WUS positively regulates the expression
of CLV3 and maintenance of the stem cell domain. This regulatory
feedback system is required to maintain appropriate meristem size throughout
Arabidopsis development.
In spite of much progress in our understanding of the regulation of floral
organ number and maintenance of the meristem in Arabidopsis, the
regulation of such events in monocots is poorly understood. The fasciated
ear2 (fea2) gene is exceptionally well characterized in Zea
mays (Taguchi-Shiobara et al.,
2001). Mutations in fea2 cause enormous enlargement of
the inflorescence meristem but have a more modest effect on floral meristems
and organ number. The fea2 gene encodes an LRR receptor-like protein
that is most closely related to Arabidopsis CLV2. This finding
indicates that the CLV signaling pathway for regulating meristem maintenance
is conserved in monocots as well as in dicots. In rice (Oryza
sativa), two loci responsible for floral meristem size and number have
been identified, FLORAL ORGAN NUMBER1 (FON1) and
FON2 (Nagasawa et al.,
1996
). Floral organ number is also increased in rice by antisense
suppression of the genes OsLRK1 and OsFOR1, which encode an
LRR receptor kinase-like protein and a polygalacturonase-inhibiting protein,
respectively (Kim et al.,
2000
; Jang et al.,
2003
).
In this report, we describe in detail a new allele, fon1-2, which
is stronger than the fon1-1 (formerly fon1) allele
previously reported by Nagasawa et al.
(Nagasawa et al., 1996). In
fon1-2, the floral meristem is severely affected and accumulates a
large number of cells. Consequently, unlike in fon1-1, the number of
all organs in the floret increase and the effect of the mutation is more
evident in the inner whorls than in the outer whorls in fon1-2. We
isolated FON1 by positional cloning and found that this gene encodes
an LRR receptor-like kinase that is orthologous to CLV1 of
Arabidopsis. Our results suggest that the CLV signal transduction
pathway for regulating floral meristem size and number is conserved in rice.
Although FON1 is expressed in all of the meristems responsible for
development of the aerial part of rice, marked changes are not observed in
meristem size or in the phenotypes of the vegetative or inflorescence organs
even in the strong fon1-2 mutant, suggesting that there may be
genetic redundancy in the maintenance of both vegetative and inflorescence
meristems in rice.
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Materials and methods |
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Scanning electron microscopy (SEM) and meristem size measurement
For observation by SEM, young panicles and flowers were fixed using the
methods of Itoh et al. (Itoh et al.,
2000). Samples were dried at their critical point, sputter-coated
with platinum, and observed with a scanning electron microscope (model S-4000;
Hitachi, Tokyo, Japan) at an accelerating voltage of 10 kV. For observation by
Nomarski microscopy, shoot and floral apices were fixed by the methods of Itoh
et al. (Itoh et al., 2000
).
After clearing them in benzyl-benzoate-fourand-a-half fluid, specimens were
observed with a microscope equipped with Nomarski differential
interference-contrast optics (model M-2; Olympus, Tokyo, Japan). The width and
height of the meristems were measured by the methods of Nagasawa et al.
(Nagasawa et al., 1996
).
Positional cloning of FON1
The fon1 locus was mapped by using an F2 population of
fon1-1 and Kasalath (spp. indica). First, the locus was
mapped to a region between CAPS markers R1028 and E10139 on the distal end of
the long arm of chromosome 6 by using 119 fon1 homozygotes. Then, by
using 2,419 F2 plants, the locus was narrowed to a region between two closely
linked CAPS markers, M11 (5'-AGACCTGATACGATGCGAAC-3',
5'-TCCTTCATGGTTGGAACTAG-3'; AfaI digestion) and M54
(5'-CACCGCCACCTTCTACGG-3', GTGGCCGTCACCGTCACC-3';
HhaI digestion), which were designed by comparing genomic sequences
of the japonica and indica. This region of 150 kb in length
was present in two YAC contigs, AP003614 and AP003769.
Ten putative genes were identified by using a gene prediction program, Rice
Automated Annotation System
(http://RiceGAAS.dna.affrc.go.jp).
Because a gene highly similar to Arabidopsis CLV1 was found among
these ten putative genes, the genomic sequences of the FON1 candidate
gene in the fon1-1 and fon1-2 mutants were determined by a
method of direct sequencing after PCR amplification. Primers were selected on
the basis of the CLV1 gene using the database of the rice genomic
sequence. A genomic DNA fragment including the FON1 candidate was
isolated from the genomic library. For complementation, a 7.7 kb fragment
including 2.2 kb of sequence directly upstream of the initiation codon was
cloned into a binary vector and introduced into fon1-1 by
Agrobacterium-mediated transformation
(Hiei et al., 1994). A
FON1 cDNA was synthesized and amplified from poly(A)+ RNA
isolated from young panicles. Exon-intron structures were determined by
comparing the genomic and cDNA sequences.
In situ hybridization
To detect FON1 transcripts unambiguously, two probes derived from
independent regions of the gene were used: the first region (probe A; 437 bp),
consisting of the last 241 bp of the coding region and 196 bp of the 3'
UTR, was amplified with the primers 5'-ACTGGGTCCGCAAGGTGAC-3' and
5'-AGATCATTAGCCCCGGAG-3'; the second region (probe B; 396 bp),
consisting of 381 bp of the 5' UTR and 15 bp of the coding region, was
amplified with the primers 5'-ACCCCTACTAGTTCAAACG-3' and
5'-GAGAGTAGGAGGCATTGTGA-3'. The amplified DNA fragments were
cloned into TA cloning vector (Novagen, Madison) and used for RNA synthesis
and labeling. The FON1 expression patterns detected with these two
probes coincided with each other. OSH1 and DL probes were
prepared as described in the original papers
(Sato et al., 1996;
Yamaguchi et al., 2004
).
Plant materials were fixed and dehydrated by the methods of Itoh et al.
(Itoh et al., 2000). They were
embedded in Paraplast Plus (Oxford Labware, St Louis) after replacement with
xylene. Microtome sections (8 µm) were mounted on glass slides coated with
Vectabond (Vector Laboratories, Burlingame). RNA probes were labeled with
digoxigenin using a DIG labeling kit (Roche, Mannheim). In situ hybridization
and immunological detection of the signals were carried out by the methods of
Kouchi and Hata (Kouchi and Hata,
1993
).
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Results |
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Flower organ development in earlier stages
To study the abnormalities in fon1 flowers in detail, we examined
the phenotypes of the strong fon1-2 mutant flowers in the early
stages of development by SEM. In wild-type rice, the lemma initiated at the
flank of the flower meristem close to the inflorescence axis and the palea
initiated at the flank opposite to the lemma
(Fig. 3A). By contrast, ectopic
palea/lemma-like organs developed on the lateral side
(Fig. 3D) or on the palea side
of the meristem in fon1-2 (Fig.
3E). In the former case, a pair of palea/lemma-like organs
developed on the inside of the palea, suggesting that an additional whorl had
formed (Fig. 3D). In the latter
case, an additional palea/lemma-like organ developed on the inside of the
palea (data not shown) or two palea-like organs developed next to each other
in the original whorl (Fig.
3E). These palea-like organs, which were arranged in parallel,
were thinner than wild-type palea in the mature flower. In wild type, two
lodicules formed at the flank of the meristem adjacent to the lemma. In
fon1-2, extra lodicules, usually two, were produced at the flank
adjacent to the palea (data not shown). Six stamens developed in a concentric
whorl in wild-type flowers. In many of the fon1-2 flowers, by
contrast, extra stamens were produced in the same whorl as the original
stamens (Fig. 3D). The maximum
number of stamens formed within the same whorl was ten. In other
fon1-2 flowers, extra stamens developed in two concentric whorls,
suggesting that an extra whorl for stamens was produced in these flowers
(Fig. 3F).
|
A few fon1-2 flowers produced a small secondary floret adjacent to the stamens (Fig. 3K). This secondary floret consisted of a pistil, a few stamens, and a pair of palea and lemma that enclosed the reproductive organs. This structure might be associated with a splitting of the flower meristem after the initiation of palea primordia in the primary flower: after separation, the detached meristem could result in the development of a secondary flower independent of the primary flower. Floral organ identity was affected by the fon1-2 mutation at only a low frequency. For example, lodicules were transformed into palea/lemma-like organs (data not shown) or an anther was partially transformed into stigma-like organs (Fig. 3L).
To verify the results of this phenotype analysis, we examined the
expression patterns of two genes, DROOPING LEAF (DL) and
OSH1. DL regulates carpel identity in rice and is expressed
exclusively in carpel primordia (Yamaguchi
et al., 2004). DL expression in wild type was detected in
carpel primordia, which then developed into a pistil enclosing an ovule
(Fig. 3M), whereas DL
transcripts in fon1-2 were detected in the multiple sets of carpel
primordia, which developed into independent pistils
(Fig. 3N). OSH1 is a
molecular marker of meristematic indeterminate cells in rice and is expressed
in the floral meristem (Sato et al.,
1996
; Yamaguchi et al.,
2004
). In wild type, OSH1 expression was downregulated
when the floral organs began to initiate and completely disappeared when the
carpel primordia began to develop (Fig.
3O). However, expression of OSH1 continued in the region
around the carpel primordia in fon1-2
(Fig. 3P). Together with the
phenotypic analysis by SEM, this result suggests that the floral meristem
maintains its activity and loses its determinacy in fon1-2, even
after the initiation of several sets of carpel primordia.
fon1 affects predominantly floral meristem size
The control of floral organ number is closely associated with floral
meristem size in Arabidopsis clv mutants
(Clark et al., 1993;
Clark et al., 1995
;
Kayes and Clark, 1998
). We
examined meristem sizes in the strong fon1-2 allele. At an early
flowering stage, the floral meristem of fon1-2 was apparently larger
than that of wild type (Fig.
4A,B; Table 1).
After initiation of the stamens, the fon1-2 floral meristem became
considerably larger and increased in length along the palea-lemma axis
(Fig. 3D,F). The expression
pattern of OSH1 suggested that the number of meristematic cells
increased in the fon1-2 floral meristem
(Fig. 4C,D). Consistent with
the floral phenotype, the floral meristem size of fon1-2 was larger
than that of fon1-1.
|
|
Isolation of FON1
To elucidate the molecular function of FON1, we set out to isolate
the gene by positional cloning (Fig.
5A). First, the fon1 locus was mapped to the distal end
of the long arm of rice chromosome 6. Using about 2400 F2 plants, we
subsequently confined the fon1 locus to a region of about 150 kb.
Using the rice genomic sequence database and the RiceGAAS program, which
efficiently predicts putative genes in rice, we identified ten genes in this
region. Among them, we identified a putative gene that encodes an LRR-type
receptor kinase similar to Arabidopsis CLV1
(Clark et al., 1997).
|
FON1 encodes a CLV1-like receptor kinase
We determined the positions of introns in FON1 by sequencing the
RT-PCR product generated with FON1-specific primers and the predicted
open reading frame. FON1 encodes a putative protein of 994 amino
acids (Fig. 5B), comprising a
putative hydrophobic signal peptide, LRRs, a transmembrane domain and a
cytoplasmic serine-threonine kinase domain. This overall structure of FON1
closely resembles that of CLV1 (Clark et
al., 1997). The number of LRRs (22) and the two cysteine pairs
that flank the LRR domain are conserved in both proteins
(Fig. 5C). Between FON1 and
CLV1, the amino acid identities of the LRR and kinase domains are 55.1 and
73.2%, respectively (Fig.
5B-D). In fon1-1, proline (903) is substituted for
leucine. This amino acid is located just downstream of subdomain IX of the
kinase domain (Die'vart and Clark,
2003
), and is shared by other plant LRR-type receptor-like kinases
such as CLV1, BRI1 and HAR1 (Clark et al.,
1997
; Li and Chory,
1997
; Nishimura et al.,
2002
). In fon1-2, glycine (205) is substituted for serine
in the sixth repeat of the LRR domain. This amino acid substituted in
fon1-2 is the same amino acid that is altered in clv1-4
(G201E), one of several strong alleles of CLV1 that has a
dominant-negative effect (Die'vart et al.,
2003
).
There are numerous LRR-type receptor-like kinases in plant genomes. To
clarify the evolutionary relationship between FON1 and CLV1,
we identified genes with high homology to FON1 and CLV1 from
rice and Arabidopsis genomic sequences and predicted the amino acid
sequences of these genes. Together with proteins known to belong to this
class, the kinase domains were used to construct a phylogenetic tree by the
neighbor-joining method (Fig.
5E). The result indicated that FON1 constitutes a small
clade with CLV1 and other genes encoding receptor-like kinases
responsible for hypernodulation in legumes such as HAR1
(Nishimura et al., 2002). Rice
and Arabidopsis genes other than FON1 and CLV1 are
not involved in this clade, which strongly suggests that FON1 is an
ortholog of CLV1 in rice.
Spatial expression patterns of FON1
To elucidate the function of FON1, we examined its mRNA expression
patterns by in situ hybridization. FON1 transcripts were initially
detected in the shoot meristem in the embryo
(Fig. 6A). Transcripts were
subsequently detected specifically in the shoot apical meristem, but not in
any other regions of the vegetative apex
(Fig. 6B). After transition to
the reproductive phase, FON1 transcripts were detected in the primary
and secondary rachis branch meristems (Fig.
6C), which correspond to the inflorescence meristems.
Subsequently, FON1 was expressed in the floral meristems from the
initial stage of floral development (Fig.
6D). FON1 continued to be expressed in the floral
meristem (Fig. 6E), and its
expression persisted even after the initiation of carpel primordia
(Fig. 6F). Thus, FON1
is expressed in all of the meristems responsible for development of the aerial
part of rice. FON1 transcripts were uniformly distributed throughout
all types of meristem. This expression pattern differs from that of
CLV1, which is mainly localized to L3 cells in Arabidopsis.
Therefore, we analyzed FON1 expression again using two probes derived
from independent regions of the gene and confirmed with both probes that
FON1 was expressed uniformly throughout the meristems.
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Discussion |
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FON1 regulates maintenance of the floral meristem
The increase in floral organ number in the fon1 mutants may be
closely associated with enlargement of the floral meristem. The meristem size
is much larger in fon1-2 than in fon1-1, and the increase in
floral organ number is consistently much greater in fon1-2 than in
fon1-1. Furthermore, the extent of meristem enlargement in
fon1-2 is much greater at later stages of floral development than at
earlier stages. Consistent with this, the increase in floral organ number is
more evident in the inner than in the outer whorls.
Floral organs increase in two ways: first, additional floral organs are
formed in the same whorl; and second, floral organs develop in the additional
whorls that form. In the innermost whorls, carpel primordia arise repeatedly
among the carpel primordia that have already been produced. This repetitious
production of carpel primordia is associated with the indeterminate nature of
floral primordia. For example, OSH1, which marks meristematic cells,
continues to be expressed in the center of the floral meristem even after the
carpel primordia have been produced, confirming that determinacy is lost in
the fon1 floral meristem. Although floral meristem determinacy is
affected in loss-of-function mutants of both DL and class C MADS-box
genes (Yamaguchi et al., 2004)
(T. Yamaguchi and H.-Y.H., unpublished), stamens and carpels, whose identities
are regulated by these genes, develop normally in the fon1 mutants.
Therefore, the loss of determinacy in fon1 seems to be independent of
the function of DL and class C genes. The continued expression of
OSH1 in the center of floral meristems in the fon1 mutant
and the uniform expression of FON1 throughout the meristem also
suggest that the control of floral meristem determinacy by FON1 is
indirect.
FON1 is expressed in all types of meristem in the aerial part of
rice, from the shoot apical meristem in embryos to the floral meristem. Unlike
the floral meristem, however, the vegetative and inflorescence meristems show
no or only slight abnormalities in fon1 mutants. Because
fon1 is inherited as a recessive trait, there may be genetic
redundancy in the pathways that maintain the vegetative and inflorescence
meristems. Because complete loss-of-function mutants of CLV1 show
weak clv phenotypes in Arabidopsis, the strong clv
phenotypes are thought to be caused by a dominant-negative effect of the
mutated protein, and the existence of an RLK-X protein that functionally
overlaps with CLV1 has been assumed in Arabidopsis
(Die'vart et al., 2003).
Analogous to this, it is possible that the gene corresponding RLK-X in rice is
not expressed in the floral meristem, but is expressed and functions in the
vegetative and inflorescence meristems. In the latter case, the mutation in
the FON1 proteins may not cause a dominant-negative effect in the
fon1 mutants. This hypothesis is consistent with both the recessive
nature of the fon1 mutation and the reduced effect of the mutation in
the vegetative and inflorescence phases. The phylogenetic tree shows that
three genes encoding LRR receptor kinase are close to FON1
(Fig. 5E). These genes are
possible candidates for sharing functional redundancy with FON1 in
the vegetative meristem.
Spatial expression patterns of FON1
FON1 transcripts are distributed throughout the whole meristem and
in all types of meristem. This pattern of expression is in high contrast to
that of CLV1, which is predominantly expressed in the L3 cell layer
of the meristems (Clark et al.,
1997). CLV1 functions on perception of CLV3 ligands that are
secreted from stem cells in the L1 and L2 layers
(Rojo et al., 2002
; Lehard and
Laux, 2003). CLV1 transfers a signal that negatively regulates WUS,
which is expressed in a putative organizing center within the CLV1
expression domain (Brand et al.,
2000
; Fletcher et al.,
1999
; Mayer et al.,
1998
; Schoof et al.,
2000
). Thus, CLV1 functions in a signaling pathway that
communicates between two distinct domains, the stem cell region and an
organizing center in the meristem. Expression of FON1 throughout the
whole meristem would therefore seem to be irrelevant to the communication
between two independent domains.
Although there is no evidence that homologs of CLV3 and
WUS are expressed and function in rice in a way similar to that in
Arabidopsis, we can propose two hypotheses for FON1 function on the
basis of the Arabidopsis CLV signaling system. If LRR-receptor
kinases work as heterodimers as proposed by Die'vart et al.
(Die'vart et al., 2003), it is
possible that a putative protein partner of FON1 may function only in the L3
layer; indeed, whereas CLV1 is expressed in a domain-specific manner,
CLV2, is expressed ubiquitously in Arabidopsis
(Jeong et al., 1999
).
Alternatively, mature FON1 proteins may be localized to the L3 layer in rice
through post-transcriptional regulation. Both hypotheses would result in the
distribution of a functional receptor complex of FON1, similar to the
distribution of CLV1 expression. However, we do not rule out a third
hypothesis that the signaling system in rice differs from that in
Arabidopsis. In this hypothesis, the presence of a WUS
homolog in an organizing center is not postulated; instead, it is assumed that
the FON1 receptor in stem cells transfers the signal from the ligand to a
putative factor that suppresses stem cell proliferation in the L1 and L2
layers without passing through an organizer (domain-autonomous regulation).
Finally, it is also possible that the difference in the expression pattern
between FON1 and CLV1 is not essential for the function of
both proteins because expression of CLV1 under the control of the
widely expressed ELECTA promoter does not cause any changes in the
meristem size in Arabidopsis
(Die'vart et al., 2003
).
To understand the genetic mechanism that regulates meristem maintenance in
rice, it will be necessary to isolate the genes that function in this pathway.
The fon2 mutant, the flowers of which have an increased number of
floral organs similar to those of fon1
(Nagasawa et al., 1996), may
provide clues towards identifying these genes. In addition, it will be
essential to determine whether a WUS-like organizer functions in rice
meristems.
FON1 transcripts are expressed in the primordia of all floral
organs including lemma, palea, lodicules, stamens and carpels, from their
inception to later floral stages. This expression of FON1 seems to be
specific to rice, because CLV1 is not expressed in the floral organ
primordia of Arabidopsis (Clark et
al., 1997). The sizes and identities of floral organs were almost
normal, even in the strong fon1-2 mutant. Therefore, even if
FON1 regulates the development of floral organs, the fon1
mutation may be masked by other genes that share functional redundancy with
FON1. We observed slight abnormalities in the floral organs at low
frequency. These defects seem to be side-effects of the enlargement of the
meristem and do not seem to be associated with the function of FON1
expressed in these floral organs, because the weaker allele fon1-1
also produces flowers with abnormal floral organ identities at a similar
frequency (Nagasawa et al.,
1996
). It will be of great interest to examine whether
FON1 is involved in the regulation of floral organ size.
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ACKNOWLEDGMENTS |
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