Anther-specific genes, which expressed through microsporogenesis, are temporally and spatially regulated in model legume, Lotus japonicus.
ABSTRACT Pollen germination and pollen tube elongation are important for pollination and fertilization in higher plants. To date, several pollen-specific genes have been isolated and characterized. However, there is little information about the precise spatial and temporal expression pattern of pollen-specific genes in higher plants. In our previous study, we identified 132 anther-specific genes in the model legume Lotus japonicus by using cDNA microarray analysis, though their precise expression sites in the anther tissues were not determined. In this study, by using in situ hybridization experiments, we determined the spatial and temporal expression sites of 46 anther-specific genes (ca. 35%), which were derived from two groups, cluster I-a and cluster II-a, according to flower developmental stages. In the case of the genes grouped into cluster I-a, thirteen clones were characterized. The specific hybridized signals were varied among the clones, and were observed in tapetum cells, microspores, and anther walls at the early developmental stage of anther tissues. In the case of the genes classified into cluster II-a, we used thirty three different cDNA clones encoding primary and secondary metabolism-related proteins, cell wall reconstruction-related proteins, actin reorganization-related proteins, and sugar transport-related proteins, etc., as a probe. Interestingly, all genes in these thirty three clones examined were specifically expressed in the bicellular pollen grains, though the signal intensity was varied among clones. From the data of the cluster II-a genes, the mRNAs related to pollen germination and pollen tube elongation were specifically transcribed and preserved in mature pollen grains.
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ABSTRACT: In order to understand the microspore and pollen development, recently, we have isolated a number of anther-specific genes in the model legume, Lotus japonicus. From these anther-specific genes, we identified one novel microspore-specific gene, LjImfb-c82. In order to determine the molecular characterization of LjImfb-c82, full-length cDNA clone was first isolated and sequenced. It encoded a protein of 286 amino acids (LjHIR1), which had sequence similarity to Hypersensitive-Induced Response like protein. LjHIR1 was specifically expressed in microspore on the in situ hybridization experiment. From the sequence similarity to prohibitin-domain protein, the LjHIR1 might be related to ion channel regulation in microspore development.Genes & Genetic Systems 11/2004; 79(5):307-10. · 1.13 Impact Factor
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ABSTRACT: In order to study gene expression in a reproductive organ, we constructed a cDNA library of mature flower buds in Lotus japonicus, and characterized expressed sequence tags (ESTs) of 842 clones randomly selected. The EST sequences were clustered into 718 non-redundant groups. From BLAST and FASTA search analyses of both protein and DNA databases, 58.5% of the EST groups showed significant sequence similarities to known genes. Several genes encoding these EST clones were identified as pollen-specific genes, such as pectin methylesterase, ascorbate oxidase, and polygalacturonase, and as homologous genes involved in pollen-pistil interaction. Comparison of these EST sequences with those derived from the whole plant of L. japonicus, revealed that 64.8% of EST sequences from the flower buds were not found in EST sequences of the whole plant. Taken together, the EST data from flower buds generated in this study is useful in dissecting gene expression in floral organ of L. japonicus.DNA Research 07/2000; 7(3):213-6. · 4.43 Impact Factor
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ABSTRACT: A 14-3-3 protein has been cloned and sequenced from a cDNA library constructed from mRNAs of mature pollen grains of Lilium longiflorum Thunb. Monoclonal antibodies (MUP 5 or MUP 15) highly specific against 14-3-3 proteins recognised a 30-kDa protein in the cytoplasmic fraction of many various lily tissues (leaves, bulbs, stems, anther filaments, pollen grains, stigmas) and in other plants (Arabidopsis seedlings, barley recombinant 14-3-3). In addition, 14-3-3 proteins were detected in a microsomal fraction isolated from pollen grains and tubes, and the amount of membrane-bound 14-3-3 proteins as well as the amount of the plasma membrane (PM) H+ ATPase increased during germination of pollen grains and tube growth. No change was observed in the cytoplasmic fraction. A further increase in the amount of 14-3-3 proteins in the microsomal fraction was observed when pollen grains were incubated in germination medium containing 1 microM fusicoccin (FC) whereas the number of 14-3-3s in the cytoplasmic fraction decreased. Fusicoccin also protected membrane-bound 14-3-3 proteins from dissociation after washing with the chaotropic salt KI. Furthermore, FC stimulated the PM H+ ATPase activity, the germination frequency and the growth rate of pollen tubes, thus indicating that a modulation of the PM H+ ATPase activity by interaction with 14-3-3 proteins may regulate germination and tube growth of lily pollen.Planta 06/2001; 213(1):132-41. · 3.35 Impact Factor
Genes Genet. Syst. (2006)
, p. 57–62
Anther-specific genes, which expressed through
microsporogenesis, are temporally and spatially
regulated in model legume,
, Makoto Endo
, Hiroshi Saito
, Yoshinobu Takada
, Hideyuki Takahashi
and Masao Watanabe
, Hirokazu Hakozaki
, Tomihiro Okabe
, Atsushi Higashitani
, Jong-In Park
Faculty of Agriculture, Iwate University, Morioka 020-8550, Japan
Graduate School of Life Sciences, Tohoku University, Sendai 980-8577, Japan
Laboratory of Biotechnology, National Institute of Crop Science, Tsukuba 305-8518, Japan
Promotion of Basic Research Activities for Innovative Biosciences, Bio-oriented Technology
Research Advancement Institution (BRAIN), Minato-ku, Tokyo 105-0001, Japan
Division of Natural Science, Osaka Kyoiku University, Kashiwara 582-8582, Japan
The 21st Century Center of Excellence Program, Iwate University,
Morioka 020-8550, Japan
(Received 14 November 2005, accepted 19 December 2005)
Pollen germination and pollen tube elongation are important for pollination and
fertilization in higher plants.To date, several pollen-specific genes have been iso-
lated and characterized.However, there is little information about the precise
spatial and temporal expression pattern of pollen-specific genes in higher plants.
In our previous study, we identified 132 anther-specific genes in the model legume
by using cDNA microarray analysis, though their precise expres-
sion sites in the anther tissues were not determined.
hybridization experiments, we determined the spatial and temporal expres-
sion sites of 46 anther-specific genes (ca. 35%), which were derived from two
groups, cluster I-a and cluster II-a, according to flower developmental stages.
the case of the genes grouped into cluster I-a, thirteen clones were characterized.
The specific hybridized signals were varied among the clones, and were observed
in tapetum cells, microspores, and anther walls at the early developmental stage
of anther tissues. In the case of the genes classified into cluster II-a, we used
thirty three different cDNA clones encoding primary and secondary metabolism-
related proteins, cell wall reconstruction-related proteins, actin reorganization-
related proteins, and sugar transport-related proteins, etc., as a probe.
ingly, all genes in these thirty three clones examined were specifically expressed
in the bicellular pollen grains, though the signal intensity was varied among
clones. From the data of the cluster II-a genes, the mRNAs related to pollen ger-
mination and pollen tube elongation were specifically transcribed and preserved in
mature pollen grains.
In this study, by using
, pollen-specific genes, mature
Microsporogenesis occurs in the anther locule.
mother cells form tetrads by meiosis.
spores released from tetrads have a single nucleus.
The free micro-
the case of model legume,
anther locule was filled with mature bicellular pollen
grains having vegetative cell and generative cells.
grains matured in the anther locule.
from the anther locule, pollen grains were quickly
hydrated on the stigma surface, and the pollen tube was
germinated.During the pollen tube elongation, two
sperm cells were formed by a single cell division of gen-
, after mitosis,
Edited by Koji Murai
* Corresponding author. E-mail: email@example.com
These authors equally contributed to this work
Higashi Shirakawa Agricultural High School, Tanakura 963-
58H. MASUKO et al.
erative cell (reviewed in McCormick 2004).
microsporogenesis, it is unknown how many genes func-
tioned in this process. Only approximately 8,000 genes
were estimated to be functioning in mature pollen grains
by two different methodologies, microarray analysis and
cDNA-poly (A) RNA hybridization kinetics (Honys and
Twell 2003; Mascarenhas 1990).
been no reports about global analysis of the spatial and
temporal expression pattern of these anther- and/or pol-
len-specific genes. An
useful for the characterization of the spatial and temporal
expression pattern of specific genes.
, the whole-mount
tion experiment was performed with 329 cDNA clones as
a probe, providing many new molecular markers for each
of the tissues and/or organs according to the developmen-
tal stages (Saitou et al. 2002).
identified 132 anther-specific genes in a model legume,
, by using cDNA microarray analysis.
From the cluster analysis, 21 genes which classified into
cluster I-a were specifically expressed in anther tissues
containing unicellular microspores, and 111 genes, classi-
fied into cluster II-a, were specifically expressed in the
anther tissues containing bicellular pollen grains (Endo
et al. 2002). As described above, determining the spatial
and temporal expression pattern of these specific genes
will give a basic data of anther development in the wild
. On the understanding the molecu-
lar function of the specific genes, theses basic data will be
informative for molecular dissection of mutant phenotype.
In this study, we determined the spatial and temporal
expression pattern of 46 different anthers-specific genes.
From the sequence similarity and expression pattern, we
estimated the function of the specific genes on anther
and/or pollen development.
a glass house (Endo et al. 2000, 2002).
the developmental stages of flower buds were classified
into five stages according to the length of flower buds and
the condition of microspore nuclei, which was determined
by staining nuclei with 4, 6’-diamidino-2-phenyllindole
However, there have
hybridization method is
In the model ascid-
In our previous study, we
(Gifu B-128) was grown in
(DAPI; Watanabe et al. 1991).
analysis was performed as described in Endo et al. (2004)
with slight modification.The modified points were as
follows; flower buds of
described in Fig. 1 were used; sections with 10
were prepared for
mental stage of the anther was divided into five stages, –
1, 0, 1, 2, and 3.Flower buds at each stage were 3–4, 4–
5, 5–6, 6–7 and 7–8 mm in length, and they contained tet-
rad and unicellular microspores, unicellular microspores,
unicellular microspores and bicellular pollen grains,
immature pollen grains and mature pollen grains,
respectively.From the viewpoint of the transverse sec-
tion, the size of anther at stage 3 was 1.6 times larger
than that at stage –1.Interestingly, the width of the
anther wall was almost similar at the all developmental
hybridization experiment, forty six different
anther-specific genes were used as a probe (Table 1,
2). For the selection, anther-specific genes were ran-
domly selected from each category of gene.
below, we also added ten kinds of genes, which have been
already characterized as a pollen-specific gene.
cluster I-a, thirteen genes encoding lipid transfer protein
(LTP), glutamine-synthesis related protein, histone dea-
cetylase (HD2), function unknown protein, etc., were
selected (Table 1). In the case of cluster II-a, thirty three
genes encoding cell wall metabolism related proteins
(pectin methylesterase (LjMfb-B69), ascorbate oxidase
-glucosidase (LjMfb-D80), reversibly glyco-
sylated polypeptide-2 protein (LjIMfb-E84)), sugar trans-
port related proteins (sucrose transporter (LjMfb-J60),
cell wall invertase (LjMfb-O34), monosaccharide trans-
porter (LjMfb-S523)), cytoskeleton related proteins (actin-
depolymerizing factor (LjMfb-I18)), methionine metabo-
lism related proteins (cobalamin-independent methionine
(LjMfb-9079)), primary and secondary metabolism related
proteins (cytochrome c (LjMfb-P913), plasma membrane
proton ATPase (LjMfb-3019),
in five stages as
connective; m, microspore; p, pollen grain; st, stomium; t, tapetum; v, vascular bundle; w, anther wall.
Cross-section of the anther at different developmental stages of
(A) Anther at stage –1. (B) Anther at stage 0.
.Each cross-section of anther was stained with
(D) Anther at stage 2. (E) Anther at stage 3.(C) Anther at stage 1. c,
analysis of mature pollen-specific genes
Table 1. Results of RNA
hybridization of cluster I-a in
histone deacetylase (HD2)
putative lipid transfer protein
allyl alcohol dehydrogenase
cytosolic glutamine synthetase
microspore and pollne grain
Weak signal detected in several tissues
Table 2.The list of mature pollen-specific genes used in RNA
hybridization of cluster II-a of
Category Clone no.
reversibly glycosylated polypeptide-2 protein
cell wall invertase
cobalamin-independent methionine synthase
plasma membrane proton ATPase
NADPH-dependent mannose-6-phosphate reductase
late embryogenesis abundant protein
3-ketoacyl-CoA thiolase B
putative suface protein
ACBF DNA binding protein
receptor-like protein kinase
cell wall metabolism related genes
sugar transport related genes
cytoskeleton related genes
methionine metabolism related proteins
primary and secondary metabolism related genes
function unknown genes
60H. MASUKO et al.
ferase (LjMfb-Q06)), a putative surface protein (LjMfb-
V66), etc., were used (Table 2).
Among the thirteen genes of cluster I-a, the hybridiza-
tion pattern was classified into three groups.
group, in which genes encoding LTP (LjMfb-S75) and
unknown protein (LjMfb-A28) were contained, the hybrid-
ization signal was specifically observed in the tapetum
(Fig. 2A).To date, tapetum-specific LTPs have been
identified and characterized (Lauga et al. 2000).
tapetum-specific LTP (LjMfb-S75) might be important for
transferring lipids from the tapetum to the pollen coat, as
indicated by maize tapetum-specific LTP (Lauga et al.
2000).The genes encoding histone deacetylase (HD2;
LjMfb-K81) and CDC50 (LjMbf-3045) were specifically
expressed in microspores (Fig. 2B), and were classified
into the second group.In our previous study, another
microspore-specific gene encoding hypersensitive-induced
response protein (LjHIIR1) was also specifically expre-
ssed in microspores (Hakozaki et al. 2004).
characteristics of these microspore-specific genes, these
genes might be involved in chromatin remodeling and cell
cycle in asymmetric division of microspores.
group, the genes, which were specifically expressed in
anther wall, were identified.
genes encoding allyl alcohol dehydrogenase (LjMfb-U53),
aldehyde dehydrogenase (LjMfb-E83), CER1 protein
(LjMfb-P53), ubiquitin protein (LjMfb-H13), and
line-5-carboxylate synthetase (LjMfb-5071).
protein is related to biosynthesis of long-chain fatty acid
and wax (Aarts et al. 1995).
In the first
As the third
This group contained the
late synthetase is a key enzyme of biosynthesis of proline
(Delauney and Verma 1993).
immature pollen grains are highly sensitive to the stress
of hydration, these wax and proline should be important
for protection of the microspores and immature pollen
grains from dehydration.In the remaining four genes,
because the weak hybridization signal was observed in
several tissues (mature pollen grain, tapetum, and anther
wall), we could not determine the precise expression in
the anther tissues, spatially and temporally (data not
In the case of thirty three genes grouped into cluster II-
a, the hybridization signal was specifically detected in the
mature pollen grain in all thirty three genes, though the
hybridization signal intensity was varied among different
clones (Fig. 2D, E, F). Within these thirty three genes,
it has been already demonstrated that ten kinds of genes
(plasma membrane proton ATPase, pectin methylesterase,
-glucosidase, poly galacturonase,
monosaccharide transporter, sucrose transporter, actin-
depolymerizing factor, receptor-like protein kinase, cobar-
amin-independent methionine synthase) were mature
pollen-specific genes (Gehwolf et al. 2001; Albani et al.
1991; Weterings et al. 1992; Rubinelli et al. 1998; Brown
and Crouch 1990; Stadler et al. 1999; Lemoine et al. 1999;
Chen et al. 2002; Tang et al. 2002; Chardin et al. 2001).
, these genes were also specifically expre-
ssed in mature pollen grains.
candidates of novel pollen-specific genes.
candidates, we found four interesting genes.
Because microspores and
Other genes should be
One is a
probes were hybridized to the cross-section of the anther tissues at different developmental stages of
encoding LTP specifically expressed in the tapetum at stages –1 and 0.
microspores at stages 0 and 1. (C) The gene encoding
at stages 2 and 3. (D–F) Genes specifically expressed in the bicellular pollen grains at stages 2 and 3.
methylesterase. (E) The gene encoding monosaccharide transporter.
microspore; p, pollen grain; t, tapetum; te, tetrad; w, anther wall.
localization of pollen-specific transcripts during anther development.DIG-labeled antisense and sense (control) RNA
(B) The gene encoding HD2 specifically expressed in the
-pyrroline-5-carboxylate synthetase specifically expressed in the anther wall
. (A) The gene
(D) The gene encoding pectin
(F) The gene encoding a putative surface protein.
Bar = 10
analysis of mature pollen-specific genes
gene encoding reversibly glycosylated polypeptide-2 pro-
tein (RGP2; LjImfb-E84). The RGP2 is a key enzyme of
biosynthesis of xyloglucan, which is one of the compo-
nents in the high molecular matrix of the cell wall
(Dhugga et al. 1997), indicating that this gene might be
important for cell wall re-organization in pollen
germination and pollen tube growth.
encoding putative surface protein, which has a
Fasciclin domain (fasciclin domain; LjMfb-v66).
fasciclin domain is involved in cell adhesion in yeast and
animal cells (Kim et al. 2003).
arabinogalactan-protein, which has a fasciclin domain,
was identified, and was specifically expressed in pollen
(Lalanne et al. 2003).Because it was estimated that the
function of the arabinogalactan-protein having fasciclin
domain might play a role in cell adhesion between pollen
and stigma (Lalanne et al. 2003), this putative surface
protein also might function in cell adhesion during the
pollination process. The remaining two genes encoding
-adenosyl-L-methionine synthetase (LjMfb-13038) and
-adenosyl-L-homocysteine hydrolase (LjMfb-9079), are
key enzymes of methionine metabolism.
-adenosyl-methionine is impor-
tant as a methyl donor for biosynthesis of nucleic acids,
proteins, carbohydrates, lipids (Lamblin et al. 2001).
During pollen tube elongation, methylated pectin is
transferred to the tip of pollen tube and is polymerized
after demethylation by pectin methylesterase catabolism
(Taylor and Hepler 1997).In fact, recently, a homolog of
methionine synthase was isolated and characterized from
tobacco pollen tubes (Moscatelli et al. 2005).
enzymes involved in methionine metabolism might be
important for cell wall re-organization.
data and previous data, in the mature pollen grains,
genes involved in cell wall re-organization, cell cytoskele-
ton, sugar transporter, proton pump, methionine metab-
olism, and cell-cell communication were specifically
expressed in mature pollen grains.
In this study, we clearly showed that the different
kinds of the transcripts involved in the pollen germina-
tion and pollen tube growth were specifically expressed in
mature pollen grain in model legume,
data will help to better understand pollen germination
and pollen tube growth at the molecular level.
Another is a gene
Recently, a gene encoding
This work was supported in part by a grant from the Ministry
of Agriculture, Forestry and Fisheries of Japan (Rice Genome
Project MA-2211) and Grants-in-Aid for the 21 Century Center
of Excellence Program from the Japan Society for Promotion of
Science (JSPS) to MW, and a grant for the Promotion of Basic
Research Activities for Innovative Biosciences from the BRAIN
to MKK. The authors are grateful to Ayako Chiba, Yukiko
Ohyama, and Hiroyuki Ishikawa (Iwate University) and Rui
Sato and Yukari Wakabayashi (Tohoku University) for technical
assistance.HH and YT are the recipients of Research Fellow-
ships of the JSPS for Young Scientists.
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