Chinese Science Bulletin
© 2009
SCIENCE IN CHINA PRESS
Springer
Stamen specification and anther development in rice
ZHANG DaBing1† & WILSON Zoe A2
1
Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders of Ministry of Education, School of Life Science
and Biotechnology, Shanghai Jiaotong University, Shanghai 200240, China;
2
Plant Sciences Division, School of Biosciences, University of Nottingham, Loughborough, Leics, LE12 5RD, United Kingdom
Male reproductive development is a complex biological process which includes the formation of the
stamen with differentiated anther tissues, in which microspores/pollens are generated, then anther
dehiscence and subsequently pollination. Stamen specification and anther development involve a
number of extraordinary events such as meristem transition, cell division and differentiation, cell to cell
communication, etc., which need the cooperative interaction of sporophytic and gametophytic genes.
The advent of various tools for rice functional gene identification, such as complete genome sequence,
genome-wide microarrays, collections of mutants, has greatly facilitated our understanding of mechanisms of rice stamen specification and anther development. Male sterile lines are critical for hybrid rice
breeding, therefore understanding these processes will not only contribute greatly to the basic
knowledge of crop developmental biology, but also to the development of new varieties for hybrid rice
breeding in the future.
rice, stamen specification, anther development, mechanism
The life cycle alternates between diploid sporophyte and
haploid gametophyte generations in flowering plants.
Male gametophytes develop from the initiation and generation of the male reproductive structure stamen within
the flower. The stamen consists of an anther structure
with multiple specialized tissues for generating pollen
grains and a filament supporting the anther. Pollen development requires cooperative functional interactions
between gametophytic and sporophytic tissues within
the anther, which includes a series of crucial events such
as male sporogenous cell differentiation, meiosis,
microspore formation and maturation. Recent reviews
on stamen and anther development include articles by
Scott et al.[1], Ma[2], Singh et al.[3] and Wilson and
Zhang[4]. Meiosis in plants including Arabidopsis, rice
(Oryza sativa) and maize (Zea mays) was also recently
reviewed by Mercier[5]. Moreover, there are a number of
excellent reviews on stamen specification and anther
development in plants published over the past twenty
years[1,6–12]. Here we mainly focus on reviewing the new
advances of stamen specification and pollen develop-
ment in rice.
Since the release of the rice genome sequence a large
number of tools have become available for the analysis
of gene function, such as collections of T-DNA insertion
mutants, full-length cDNAs, the highly efficient transformation system for both subspecies Oryza sativa ssp.
indica and Oryza sativa ssp. Japonica[13]. Moreover,
besides having a much smaller genome size (389 Mb)[14],
rice is relatively closely related to other agronomically
important cereal grasses such as wheat (Triticum aestivum), maize and barley (Hordeum vulgare). Rice is
therefore becoming an excellent model monocot crop for
developmental biology. Recent progress has increased
our understanding of stamen determination, anther-specific gene expression and anther development in rice.
Received February 25, 2009; accepted March 25, 2009
doi: 10.1007/s11434-009-0348-3
Corresponding author (email: [email protected])
Supported by the National Key Basic Research Development Program of China
(Grant Nos. 2007CB108700, 2009CB941500), National Natural Science Foundation
of China (Grant No. 30725022), and Shanghai Leading Academic Discipline Project
(Grant No. B205)
†
Citation: Zhang D B, Wilson Z A. Stamen specification and anther development in rice. Chinese Sci Bull, 2009, 54: 2342―2353, doi: 10.1007/s11434-009-0348-3
Figure 1 The rice flower. (a) An intact mature (stage 12) rice flower with seven types of organs, glumes (gl), lemma (le), palea (pa), lodicules
(lo), stamens (st), pistil (ps) and ovary (ov); (b) a scanning electron micrograph of a stage Sp 6 flower with six stamens. Two stamen primordia
emerged later than the others (red arrowheads), and one of them was covered by the lemma; (c) a longitudinal section of a stage Sp 9 flower,
when lemma and palea were locked together tightly. A small lodicule (lo) primordium can be seen on the side of lemma.
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Poaceae (grasses) is one of the largest flowering plant
families in angiosperms, with about 10000 species and
700 genera including many economically important
crops such as rice, barley and maize[15,16]. Evolutionary
changes in the organization and structure of inflorescence and flower caused a distinct morphology in
grasses diverging from those of higher eudicots and
even other monocots[17–20]. The rice inflorescence architecture is quite different from those of other major cereal
crops, instead of two or more florets in one spikelet as
seen in other cereal crops, such as maize and wheat, one
rice spikelet has only one floret surrounded by a pair of
empty glumes. In addition, rice florets have an asymmetric structure with five types of floral organs with
characteristic numbers, one lemma and one palea in the
first outer whorl, two lodicules in the second whorl, six
stamens in the third whorl and one pistil in the fourth
innermost whorl (Figure 1(a))[21]. Even though rice has a
quite different flower structure from that of Arabidopsis,
their reproductive organs, i.e. stamens and carpels, have
a similarity. Similar to the classic symmetry of floral
organ arrangement in eudicots, rice stamens are symmetrically arranged in the third whorl.
Each stamen contains a filament and an anther with
four lobes linked to the filament by connective tissues
(Figure 1). The rice anther is composed of two thecae
linked by the connective tissue, and each thecae has two
locules, one is longer at the base and the other is shorter.
The two locules are connected by septum and stomium
(consisting of small epidermal cells), which are crucial
for anther dehiscence[22]. Based on the morphological
cellular landmarks, rice inflorescence and spikelet de-
velopment have been divided into 13 stages and 8 stages,
respectively[23]. At the early stage, the inflorescence
meristem initiates and grows, and in rice stamen primordia appear during the inflorescence stage IN
7/spikelet stage SP 6 defined by Ikeda et al.[23] (Figure
1(b)). Previous reports divided rice anther development
course into eight stages from the archesporial cells (ACs)
differentiation at four corners of hypodermis of anthers
to mature pollen grain production[24], or from the premeiosis stage to the mature pollen stage[25,26]. In Arabidopsis, anther development has been divided into 14
stages based on morphological features[2,27]. We analyzed the cellular changes occurring in the rice anther (O.
sativa ssp. japonica cv.9522 and Zhonghua 11) by light
microscopy observation of transverse sections, and revealed the morphological, cellular, and molecular events
of rice anther development, which are very similar to
those of Arabidopsis. Thus we divide the rice anther
developmental courses into 14 stages, which is consistent with that of Arabidopsis (Figure 2).
At stage 1, the stamen (anther) primordium was
formed from cell divisions in the L1, L2, and L3 layers
of the floral meristem (Figure 2, stage 1). From stages 1
to 5, the anther primordia continued cell division and
differentiation, and developed the characteristic anther
structures with locule, wall, connective, and vascular
tissues (Figure 2). Anticlinal cell division occurred
within the L1 layer, and the epidermis formed, meanwhile the L3 cells divided and differentiated into connective and vascular tissues. Periclinal divisions of archesporial cells (ACs) in the four corners of the anther
primordia generated distinct 1° parietal cells and 1°
sporogenous cells. The 1° parietal cells then differentiated into two 2° parietal layers, the outer secondary pa-
DEVELOPMENTAL GENETICS
1 Stamen development
Figure 2 Developmental stages of the rice anther. Ar, Archesporial cell; C, connective tissue; BP, biceullar pollen; Dy, dyad cell; E, epidermis;
En, endothecium; L1, L2, and L3, the three cell-layers in stamen primordia; MC, meiotic cell; ML, middle layer; MMC, microspore mother cell;
MP, mature pollen; MSp, microspore; parietal cell; 1°P, primary parietal layer; 2°P, secondary parietal cell layer; Sp, sporogenous cell; St,
stomium; StR, stomium region; T, tapetum; Tds, tetrads.
rietal layer further generated the endothecium layer and
the middle layer, and the inner secondary parietal layer
developed the tapetum layer. The 1° sporogenous cells
divided and formed 2° sporogenous cells, then generated
microspore mother cells (MMCs) within the locule
(Figure 2, stage 5). During stages 7 to 9, MMCs underwent meiosis and formed dyads (Figure 2, stage 8a) and
tetrads of haploid microspores (Figure 2, stage 8b).
From stage 9, free microspores were released from the
tetrads with the degradation of callose wall at stage 8b
(Figure 2, stage 9), then the microspore vacuolated and
became round shape (Figure 2, stage 10). The vacuolated microspores underwent the first mitosis with
asymmetric cell division generating a much smaller
generative cell and a vegetative cell with one vegetative
nuclei (Figure 2, stage 11). Thereafter, at stage 12 the
generative cell in the microspore divided into two sperm
cells, and the mature pollen formed with three nuclei, i.e.
two smaller sperm nuclei, and a larger vegetative nucleus (Figure 2, stage 12). At stage 13, the lemma was
opened and the anther dehiscence occurred (Figure 2,
stage 13), and at stage 14, the anther continued the re2344
lease of mature pollen grains (Figure 2, stage 14).
2 Stamen specification
2.1 FON1-FON4/2 signaling pathway
Stamen formation in plants can be grouped into two
major steps including stamen primordial formation, and
stamen development. The developmental switch of the
shoot apical meristem (SAM) from vegetative to reproductive growth is critical for the formation of plant floral
organs including the stamen which is regulated by both
environmental and endogenous signals. One of the best
characterized SAM signaling pathways in Arabidopsis is
the CLAVATA (CLV)-WUSCHEL (WUS) pathway which
involves three CLV genes, CLV1-CLV3, and the WUS
gene. CLV1 is a putatively extracellular leucine-rich
repeat (LRR) receptor kinase, and CLV2 is a LRR protein lacking a kinase domain[28,29]. CLAVATA3 (CLV3)
is a putative secreted peptide ligand, which is thought to
interact with the CLV1/CLV2 heterodimeric receptor to
limit the size of the stem cell pool in the SAM[28–30].
Mutations in any one of the three CLV genes result in
enlarged SAM, as well as inflorescence and floral mer-
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2.2 ABC genes
There are several recent reviews on rice floral organ
determination[49–52], thus we will briefly discuss the determination of stamen identity in rice here (Figure 3).
Genetic and functional analyses of homeotic mutants in
Arabidopsis and Antirrhinum majus with altered identities of floral organs led to the ABC model of flower development[6]. Three classes of homeotic genes (named A,
B, and C) control the identity of floral organ primordia,
and later additional class D and SEPALLATA (SEP)
genes in Arabidopsis were revealed to work with the
ABC homeotic genes in determining the identity of stamens as well as petals and carpels. The B class genes
include APETALA3 (AP3) and PISTILLATA (PI) from
Arabidopsis and DEFICIENS (DEF) and GLOBOSA
(GLO) from Antirrhinum; AGAMOUS (AG) and PLENA
are the C genes. Mutants of any one of the B or C genes
cause homeotic conversion of the third-whorl stamens to
others, for instance, mutations of B class genes cause
conversion of stamens into carpels, mutation of C class
gene results in conversion of stamens to petals, and loss
of both B and C genes causes stamens to sepals. No obvious defect was observed in the single gene mutations
of the SEP genes, but the quadruple triple mutants of
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FON4/2, i.e. FON1 is expressed in throughout the whole
meristem[44], FON1 might be the receptor of FON4/2
required for regulating SAM size in rice.
Moreover, we treated wild type rice and the fon1 mutant with 50 μm a synthetic 14-amino acid peptide,
FON4p, corresponding to the predicted CLE (CLV3/
ESR-related) motif of FON4/2. Significant inhibition of
apical growth was observed in both the wild type plant
and the fon1 mutant, suggesting FON4p is the main
functional motif of FON4/2; this also implies that other
receptor(s) of FON4/2, but not FON1, exist(s) in rice
regulating SAM[48]. We therefore propose that the conserved feed-back loop regulatory systems consisting of
CLV-ligand-receptor system and the homeodomain protein WUS may exist in rice and play a central role in
regulating the stem cell number. This signaling pathway
is critical for the development of rice floral organs including stamens (Figure 3).
When the flag leaf is produced in rice, the vegetative
SAM is then converted to an inflorescence meristem. At
the stage IN 7/SP 6 the panicle length reaches more than
1.5 mm, and the floral meristem rapidly differentiates
floral organs including stamens[23].
DEVELOPMENTAL GENETICS
istems, leading to increased numbers of flowers and floral organs including stamens[31–33]. More recently a receptor kinase CORYNE (CRN) was shown to act with
CLV2 independently of CLV1 to limit stem cell proliferation and promote differentiation in the CLV3 signal
transduction pathway[34]. By contrast, the WUS gene
encoding a homeodomain transcription factor has the
ability to promote the SAM and reproductive meristem
sizes[33,35–38]. WUS is specifically expressed within the
organizing center of the SAM and is down-regulated by
the activation of CLV3. On the other hand, the CLV3
expression is positively regulated by WUS, forming a
positive-negative feedback loop to maintain the size of
merisitems throughout Arabidopsis development[39–41].
More and more evidence suggests that the CLV-WUS
pathway regulating SAM is functionally conserved in
both monocots and eudicots. The maize fasciated ear2
(fea2) locus is the first well characterized monocot gene
of the CLV pathway. The fea2 gene encodes a LRR receptor-like protein which is the most closely related to
CLV2, and the fea2 mutant displayed a dramatic
over-proliferation of the ear inflorescence meristem, and
a more modest effect on floral meristem size and floral
organ number[42]. Moreover, another maize gene, Thick
Tassel Dwarf1 (td1) encoding a CLV1-like protein, was
revealed to function in the inflorescence and flower to
restrict meristem sizes[43]. Furthermore, a rice mutant,
floral organ number 1 (fon1) shows an enlarged floral
meristem and an increase of organ number, with stamen
number increased to 7-12 in fon1-2[44]. FON1 is likely
the ortholog of td1 and CLV1. Another CLV1 homolog
in rice OsLRK1, and silencing of OsLRK1 caused an
increased floral organ number in the knock down
plants[45].
Recently the rice mutants floral organ number 4/2
(fon4/2) were identified with abnormal enlargement of
the SAM, inflorescence meristem and floral meristem,
causing the increase of floral organ number, and stamen
number increased to 7-10 in the fon4-1 mutant[46,47]. This
defect is very similar to that of fon1. Furthermore,
FON4/2 is mainly expressed in small groups of cells at
the apex of the vegetative SAM, the inflorescence meristem and the floral meristem, and encodes a putative
secreted peptide which appears to be an ortholog of
CLV3. Also ectopic expression of FON4/2 could reduce
the number of floral organs and flowers, and this function of FON4/2 requires the function of FON1. Although
the domain of FON1 expression is larger than that of
Figure 3 (a) The flower of the fon1 mutant; (b) the flower of the fon4 mutant; (c) the flower of the dl mutant, with arrowheads showing the increased number of stamen in these mutants; (d) diagram for rice anther specification and development based on the gene expression pattern.
sep1 sep2 sep3 sep4 transform floral organs into
leaf-like structure[53,54].
Similar to the function on specifying stamens by the
activity of AP3 in Arabidopsis[55,56], the rice B class
gene SUPERWOMEN1 (SPW1 or OsMADS16) orthologous to AP3 have been shown to be crucial for stamen
specification[57,58]. Mutation of SPW1 results in homeotic conversion of stamens to carpels, and lodicules to
palea/lemma-like structures. Although both OsMADS2
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and OsMADS4 are the putatively orthologs of Arabidopsis PI[59–61], the roles of these two genes in specifying
lodicules and stamens remain controversial. OsMADS4
is a likely partner of SPW1 in specifying both lodicules
and stamens because of the similar expression pattern of
these two genes in the primordia of lodicules and stamens, and their protein-protein interaction tested by the
yeast two-hybrid (Y2H) system. Also Kang et al.[62] reported that reduction of the OsMADS4 expression level
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2.3 Transcriptome analysis of anther development
Currently, around 41000 genes have been estimated in
rice genome and whole-genome microarrays have recently been generated[13]. Microarrays have become the
essential approach for high-throughput analysis of
global gene expression and for genome-wide mapping of
functional genes. Recently more and more available microarray data for understanding the biological processes
of rice anther development have also been released[93–101]. Transcriptional profiling of rice anther
using a 10 k cDNA microarray revealed the transcriptome in anther is quite distinct from other tissues, with
2155 genes showing expressional changes are observed
in the anther[97]. An anther usually consists of 4 sporophytic cell layers enclosing gametophytic microspores,
laser microdissection (LM) has been recently used for
separating microspore/pollen and the sporophytic
tapetum specific cell types from sectioned anther specimens for microarray analysis. This combination tech-
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coding a YABBY domain protein in rice has been identified in carpel specification, floral meristem determinacy, and the antagonistic function with class B
genes[75,76]. DL is the ortholog of CRABS CLAW (CRC)
in Arabidopsis.
Phylogenetic analysis identified five SEP-like genes
in rice genome, i.e. OsMADS1, OsMADS5, OsMADS24
(allelic to OsMADS8), OsMADS34 (allelic to OsMADS19), and OsMADS45 (allelic to OsMADS7)[77–82].
Among these five SEP-like genes, only the function of
OsMADS1 has been revealed more clearly[81,83–88]. The
mutant of OsMADS1, lhs1, develops leafy lemma and
palea, a reduced stamen number, and conversion of
lodicules and stamens into leafy lemma- and palea-like
structures[83,86–89], suggesting that OsMADS1 functions
in floral organ specification and floral determinacy[86].
Moreover, stamen specification is controlled by rice
ABERRANT PANICLE ORGANIZATION 1, an ortholog
of Arabidopsis UNUSUAL FLORAL ORGAN (UFO),
encoding an F-box protein. In addition to the positively
controlling spikelet number, APO1 has the ability to
regulate floral organ identity by positively regulating
OsMADS3, but not class-B genes, and apo1 displays
conversion of stamens to lodicules[90,91]. Moreover, another mutant termed pistilloid-stamen (ps) displays partial transformation of stamens into pistils and pistilstamen chimeras suggesting the ps locus is critical for
stamen identity[92].
DEVELOPMENTAL GENETICS
caused similar defects to spw1. Previous data suggested
that OsMADS2 does not interact with SPW1[57,60], and
RNA interference (RNAi) of OsMADS2 results in the
partial transformation of lodicules into mrp-like structures, but no obvious change for stamen development[63–65]. However, Yao et al.[66] produced RNAi
transgenic lines to specifically reduce the expression of
OsMADS2 and OsMADS4 independently or simultaneously, and OsMADS2 RNAi lines display normal morphology of the floral organs except abnormal elongated
lodicules. By contrast, no abnormal floral organs are
caused by the OsMADS4 RNAi plants, which is consistent with the reported data by Yoshida et al[65], but inconsistent with the data of Kang et al.[62] and Yao et
al.[66]. Moreover, reduction of both OsMADS2 and
OsMADS4 causes the similar defects of the spw1 mutants, confirming the redundant functions of OsMADS2
and OsMADS4 in lodicule and stamen development.
Furthermore, Y2H assays proved that SPW1 interacts
with both OsMADS4 and OsMADS2[65,66]. These data
imply that OsMADS4 and OsMADS2 may act redundantly with SPW1 in specifying lodicule and stamen
identity in rice.
In Arabidopsis one typical class C gene AGAMOUS
(AG) has been identified for specifying stamen and carpel identity and for floral determinacy[67]. Whereas four
AG-like genes have been identified in rice genome, i.e.
OsMADS3[68], OsMADS58[61], OsMADS13[69] and
OsMADS21[60,70]. OsMADS3 and OsMADS58 have
restricted expressional signals in both stamen and carpel,
suggesting these two genes may have the similar function to class C genes[61,71,72]. Over-expression of OsMADS3 causes partial conversion of lodicules into stamens[73], and the osmads3 mutant displays complete
transformation of stamens to lodicules. However,
knockdown of OsMADS58 only resulted in the reduced
stamen number. Thus OsMADS3 and OsMADS58 may
have distinct roles in specifying the stamen identity[61],
with OsMADS3 playing a more important role in stamen
specification. Consistent with this, OsMADS3 transcripts
occur mainly in stamen, carpel, and ovule primordia,
with no expression in the differentiated organs. By contrast, OsMADS58 is expressed in stamen, carpel and
ovule primordia, also in these differentiated and mature
organs. OsMADS13 and OsMADS21 have been grouped
as D class genes because of their expression pattern and
their functional analyses[60,69,70,74]. More interestingly,
another C function gene DROOPING LEAF (DL) en-
nology is called LM- microarray, which has been proved
to be reliable for probing transcriptomes in microspore/
pollen and tapetum of rice anther[101]. 28141 anther-expressed genes have been identified in rice using Agilent
44K rice oligo microarray with about 42000 oligonucleotides, and they were grouped into 20 clusters[100].
Among these, 3468 anther-specific genes were detected
to be expressed in the anther during the five developmental stages of meiosis, tetrad, uninuclear microspore,
bicellular pollen, and tricellular pollen. During these
developmental stages various spatiotemporal expression
patterns among the microspores/pollen genes were observed, some genes were gradually up-regulated,
whereas some genes down-regulated, suggesting complex regulatory changes during anther developmental
events. Intriguingly, 10,810 (38.4%) genes were observed to be synchronously expressed in both microspore/pollen and tapetum, while some genes displayed
low synchronized expression profiles. Gene ontology
(GO) categories and gene annotations indicated that
these genes were related to important biological events
such as translation regulation, carbohydrate metabolism,
lipid metabolism, secondary metabolism, cell-cycle, cytoskeleton re-organization, etc.
Furthermore, a total of 164188 cis-elements grouped
into 256 cis-motifs within 140 representative microspore/pollen and tapetum-specific genes were identified[101]. Moreover, Tos17-insertion mutant lines of 17
microspore/pollen and tapetum-specific genes have been
identified in the Tos17 mutant panel database (http://tos.
nias.affrc.go.jp/). These global gene expression data in
microspore/pollen and tapetum will definitely facilitate
more biological studies using genetic, biochemical approaches to understand more molecular basis of anther
development in plants.
Considering the technical limitations of using DNA
microarrays to generate transcriptomes, such as includ-
Figure 4
2348
ing low numbers of gene transcripts and minimal quantification etc., Huang et al.[102] employed the advanced
sequencing-by-synthesis (SBS) technology to analyze
transcriptomes of rice anthers of 6 developmental stages
and mature pollen. Each SBS transcriptome obtained the
sequenced signatures (i.e, 20-mer tags of cDNA) ranging from 1.1 to 4.3 million, and the 7 SBS transcriptomes revealed a total 18,267 genes expressed in rice
anther, and about 25% had antisense transcripts, suggesting elegant control of gene expression during anther
development. In addition, a number of transcripts were
deduced to be specifically expressed in tapetum, some
genes encoding secretory proteins, and some genes encoding potential proteins related to lipid exine synthesis
during pollen wall development[102]. Obviously, this
SBS based comprehensive transcriptome analysis in the
rice anther offers data with high quality, more precise
quantity, which are valuable for plant reproductive
study.
2.4 Key regulators for anther development
Understanding the molecular mechanism of rice anther
and pollen development is crucial for future hybrid rice
breeding. We recently summarized the molecular regulatory networks controlling anther and pollen development in Arabidopsis and rice, including the genes regulating anther cell division and differentiation, meiosis,
pollen development and anther dehiscence[103]. Therefore here we briefly introduce some key regulators for
anther development in rice (Figure 4).
MSP1 (MULTIPLE SPOROCYTE1) plays a critical
role for normal anther cell differentiation especially
controlling early sporogenic development. MSP1 encodes a putative leucine-rich-repeat receptor kinase,
which is an ortholog of EXS/EMS1 in Arabidopsis. In
addition to the msp1-1, msp1-2, and msp1-3 mutants, we
identified another msp1 mutant called msp1-4 with 10
base pairs deletion between 758 and 767 bp in the MSP1
The process of pollen development and regulators in rice.
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vide cellular contents supporting pollen wall formation
and to allow the subsequent pollen release. However, the
molecular basis regulating tapetal PCD in plants remains
poorly understood. Studies on key transcription factors
during rice anther and pollen development are helpful to
elucidate the regulation and function of transcriptional
control. A key gene involved in rice the early stage of
tapetal development is Undeveloped Tapetum1 (Udt1),
which is a putative basic loop-helx-loop (bHLH) transcription factor, necessary for the differentiation and
development of tapetal cells. The Udt1 mutant had undifferentiated tapetum and delayed degenerated anther
layers with aborted microspores[96]. TDR (tapetum degeneration retardation), a newly found putative basic
helix-loop-helix (bHLH) protein in rice, is thought to be
a positive regulator of tapetal PCD[26]. In the tdr mutant,
delayed tapetal PCD and aborted microspore with abnormal pollen wall were observed, also the lipidic metabolism for anther cuticle and pollen exine synthesis
and the expression of 236 genes in the tdr anther were
altered[26,112]. In addition, there are some other genes that
have been shown to affect postmeiotic tapetum development and microspore development. For instance, the
Arabidopsis ABORTED MICROSPORE (AMS) gene,
the ortholog of TDR, also encoding a bHLH containing
protein plays a crucial role in tapetum and microspore
development[113]. In addition, the Arabidopsis MALE
STERILITY1 gene encodes a protein with a PHD finger
motif and is important for proper tapetal function and
－
normal microspore development[114 117]. OsGAMYB is
another transcription factor controlling rice pollen development, loss-of-function of OsGAMYB causes loss of
α-amylase expression in the endosperm in response to
the treatment of GA, and the mutant microspores could
not stick to the tapetal cells from the tetrad stage. The
microspore mother cells were observed to be abnormal,
and the mutant tapetal cells were aberrantly expanded[118,119].
One important role of the tapetum is supplying nutrients for pollen development such as providing enzymes
for callose dissolution and materials for pollen-wall
formation. The rice tapetum belongs to the secretory
type and it supplies lipid derived molecules for pollen
wall development through secreting bodies called Orbicules (Ubisch bodies), which are spheroid structures of
about 1 µm. RAFTIN is mainly expressed in tapetal
cells and accumulates in Ubisch bodies; knock down of
DEVELOPMENTAL GENETICS
open reading frame[104]. The defect of the msp1 mutants
revealed the role of MSP1 in restricting the number of
cells for further male and female sporogenesis, and loss
of function of MSP1 resulted in extra number of both
male and female sporocytes[104,105]. In addition, the msp1
mutants develop abnormal anther wall layers and have
no tapetal layer, and the microsporocyte was retarded
during meiotic prophase I, leading to complete male
sterility. More recently, OsTDL1A, a TPD1-like gene in
rice, has been proved to bind the leucine-rich-repeat
domain of MSP1 to limit sporocyte numbers, but this
function is limited in the ovule[106].
Like other flowering plants, the rice diploid parental
cells undergo meiosis to generate haploid microspores
essential for sexual reproduction. Several rice genes
have been identified in controlling meiosis such as
PAIR2 (HOMOLOGOUS PAIRING ABERRATION IN
RICE MEIOSIS2), PAIR1 and OsRad21-4. PAIR2 encodes a HORMA-domain protein, which is the homolog
of HOP1 in Saccharomyces cerevisiae and ASY1 in
Arabidopsis, and it controls chromosome synapsis at
meiosis I during male[107,108]. PAIR1 is a novel protein
putatively containing two coiled-coil motifs, two basic
regions and nuclear localization signal sequence, and it
controls chromosome pairing and cytokinesis during
both male and female gamete development[109]. The rice
OsRad21-4 encoding an orthologue of yeast Rec8 protein, is required for efficient meiosis and in Osrad21-4
knock-down lines abnormal homologous chromosome
pairing and uneven distribution of chromosomes during
meiosis were observed[110]. ARGONAUTE (AGO)
members have been proved to be crucial for RNAmediated silencing in plants, and rice genome has 18
copies of predicted AGO family members. Intriguingly,
one rice AGO gene MEIOSIS ARRESTED AT
LEPTOTENE1 (MEL1) was proved to control chromosome condensation during early meiotic stages, and
mel1 develops abnormal multinucleated, and vacuolated
pollen mother cells. Also abnormal development of female germ cells occurred[111], this indicated that RNAmediated gene silencing plays essential roles during
germ cell development in rice.
Tapetal cell differentiation and subsequent degradation by programmed cell death (PCD) coincides very
well with the program of anther postmeiotic development, and premature or delayed degradation of tapetum
may result in male sterility. The PCD is thought to pro-
OsRAFTIN1 produced abnormal microspore exine development, leading to male sterility[120].
As a sink tissue, the anther requires the supply of nutri- ents, in particular carbohydrates from source tissue
for pollen development and maturation. Disturbances in
sugar partitioning or metabolism in the anther usually
cause abnormal pollen development, and eventually
male sterility. UDP-glucose pyrophosphorylase (UGPase) is related to sucrose degradation by catalyzing
UDP-glucose generated by sucrose synthase to glucose1-phosphate for the metabolic demand of anther and
pollen development[121]. One rice UGPase gene, Ugp1,
has been proved to be critical for callose deposition from
the tetrad, leading to novel thermosensitive male sterile
lines[122].
Myosins are actin-based molecular motor proteins
which are involved in eukaryotic motility such as cytokinesis, muscular contraction, maintenance of cell shape,
vesicle transport[123,124]. OsmyoXIB (Oryza sativa myosin XI B), a rice myosin gene, was first demonstrated
in controlling pollen development by sensing changed
environmental factors[125]. A Ds insertion mutant of
this gene displayed abnormal pollen development
under short day length (SD) conditions due to the
OSMYOXIB-GUS fusion protein localizing only in the
anther epidermal layer, whereas, this protein is normally
distributed in the anther wall layers, connective tissues
and microspores during pollen development under long
day length (LD) conditions. RICE IMMATURE
POLLEN 1 (RIP1) is one putative protein homologous
to the proteins with five WD40 repeats, rip1 mutant developed delayed developed microspore from the vacuolated stage, leading to male sterility[126]. The synthesis of
very long chain fatty acids (VLCFAs) is required for
wax and ether lipids synthesis for the anther develop1
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ment in flowering plants. The rice WDA1 gene
(LOC_Os10g33250) encoding one putative enzyme with
higher similarity of CER1 in Arabidopsis is mainly expressed in the anther epidermal cell and involved in the
decarboxylation pathway in the production of VLCFAs
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anther development in rice.
3 Perspective
Molecular genetic and biochemical studies have successfully revealed a number of key regulators in flowering plants for the specification of stamen identity, anther
cell division and differentiation, control of male meiosis,
PCD of anther wall, lipid metabolism during pollen development and hormonal regulation of anther dehiscence.
The availability of whole genome sequences, more mutants, genome-scale expression profiling and advanced
sequencing capability will significantly speed up identifying more genes that are crucial for male reproduction
in rice. The tools of cell biology and biochemistry will
also be essential for the understanding of molecular and
biochemical mechanisms of the identified genes. In addition, comparative analysis of rice male reproductive
regulators with the identified genes in maize and Arabidopsis, as well as other organisms will reveal the conserved and divergent regulatory pathways controlling
male reproduction. More importantly, understanding of
these processes will be used in selective breeding, hybrid rice production. Therefore the future for systematically investigating rice male reproduction is very exciting.
We appreciate the assistance of Yuan Zheng, Zhang Lan, Li Lantian and
Zhang Dasheng for preparing the pictures of this paper.
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