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Female Gametophyte
Development in
Flowering Plants
Wei-Cai Yang,1 Dong-Qiao Shi,1
and Yan-Hong Chen2
1
Key Laboratory of Molecular and Developmental Biology, Institute of Genetics and
Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
email: [email protected], [email protected]
2
College of Life Sciences, Nantong University, Zhongxiu Campus, Nantong 226007,
China; email: [email protected]
Annu. Rev. Plant Biol. 2010. 61:89–108
Key Words
First published online as a Review in Advance on
February 24, 2010
embryo sac, synergid cell, egg cell, central cell, cell fate, ovule
The Annual Review of Plant Biology is online at
plant.annualreviews.org
This article’s doi:
10.1146/annurev-arplant-042809-112203
c 2010 by Annual Reviews.
Copyright All rights reserved
1543-5008/10/0602-0089$20.00
Abstract
The multicellular female gametophyte, a unique feature of higher
plants, provides us with an excellent experimental system to address
fundamental questions in biology. During the past few years, we have
gained significant insight into the mechanisms that control embryo sac
polarity, gametophytic cell specification, and recognition between male
and female gametophytic cells. An auxin gradient has been shown for the
first time to function in the female gametophyte to regulate gametic cell
fate, and key genes that control gametic cell fate have also been identified. This review provides an overview of these exciting discoveries
with a focus on molecular and genetic data.
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Contents
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
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INTRODUCTION . . . . . . . . . . . . . . . . . . 90
OVULE DEVELOPMENT . . . . . . . . . . 90
THE TRANSITION FROM
SOMATIC TO GERMLINE
FATE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
SPECIFICATION OF THE
FUNCTIONAL MEGASPORE . . . 93
PROGRESSION OF THE
GAMETOPHYTIC MITOTIC
CYCLE . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
The Initiation of Female
Gametogenesis . . . . . . . . . . . . . . . . . 94
Control of the Gametophytic
Cell Cycle . . . . . . . . . . . . . . . . . . . . . . 94
CELLULARIZATION OF THE
EMBRYO SAC . . . . . . . . . . . . . . . . . . . . 96
EMBRYO SAC POLARITY AND
GAMETOPHYTIC CELL
SPECIFICATION . . . . . . . . . . . . . . . . . 96
THE FUNCTIONAL FEMALE
GERM UNIT . . . . . . . . . . . . . . . . . . . . . 99
The Egg Cell . . . . . . . . . . . . . . . . . . . . . . 99
The Synergid Cell . . . . . . . . . . . . . . . . . 99
The Central Cell . . . . . . . . . . . . . . . . . . 101
CONCLUSIONS . . . . . . . . . . . . . . . . . . . . 102
INTRODUCTION
A female gametophyte is a multicellular
haploid structure that develops into an embryo
and endosperm after fertilization. In the
past decade, gametophyte development in
plants has emerged as an excellent system
to address fundamental questions in biology,
such as cell specification, cell-cell interaction,
and the developmental role of basic cellular
machinery. Significant progress has been made
to define the genetic components that govern
gametogenesis. This review focuses on recent
advances in defining genetic control of female
gametophyte development.
OVULE DEVELOPMENT
An ovule is a female organ within the carpel of
a flower that harbors the female gametophyte.
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Ovule development starts as a protrusion (primordium) on the edges of the septum of the gynecium. As the ovule primordium elongates, a
finger-like structure (nucellus) is formed. Then,
a hypodermal cell at the tip of the nucellus starts
to differentiate and forms an archesporial cell,
which produces the germline. The archesporial
cell enters meiotic development to differentiate
a megasporocyte, which becomes distinct by its
large size and nuclear morphology (Figure 1a).
The megasporocyte then undergoes meiosis
to give rise to four haploid megaspores. In
most flowering plants, which include the model
species Arabidopsis and rice, micropylar megaspores undergo programmed cell death, and the
chalazal-most megaspore becomes functional
and ultimately forms the female gametophyte,
the embryo sac (Figure 1b). Concurrently, epidermal cells at the proximal third of the nucellus divide parallel to the long axis and form two
primodia, which become the inner and outer integuments, respectively (Figure 1a). These enclose the functional megaspore, which becomes
the embryo sac, forming a narrow opening at
the micropyle where the pollen tube enters after pollination.
While nonfunctional megaspores undergo
cell death, the functional megaspore increases
in size and undergoes a nuclear division without cytokinesis to produce a two-nucleate embryo sac (Figure 1c). The two daughter nuclei,
now separated to the poles by the formation
of a central vacuole (Figure 1d), proceed to
a second karyokinesis to form a four-nucleate
embryo sac with nuclei in a 2n+2n configuration (Figure 1e). As the vacuole increases in
size, the third karyokinesis takes place, which
results in the formation of a huge coenocytic
cell with eight nuclei that adopt a 4n+4n
configuration—the eight-nucleate embryo sac
(Figure 1f ). Thereafter, two polar nuclei, one
from each pole, migrate to the micropylar cytoplasm of the embryo sac and finally fuse to form
a diploid central nucleus. As polar nuclei migrate, cell walls are formed simultaneously, dividing the embryo sac into seven cells with four
cell types: three antipodal cells at the chalazal
end, a diploid central cell, two synergids, and
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an egg cell at the micropylar end (Figure 1g).
Antipodal cells degenerate shortly before fertilization in Arabidopsis (Figure 1h) or undergo
further mitosis as seen in maize. Antipodal cells
are likely dispensable for fertilization. Therefore, the central cell, the egg, and two synergid
cells form a female germ unit—a functional unit
that is able to attract a pollen tube, interact with
the tube to trigger sperm release, and complete
double fertilization. As mentioned above, ovule
development involves both sporophytic and gametophytic processes, and is an excellent system
to study the basic developmental mechanisms
that control germline formation, cell growth
and division, and gametic cell fate specification.
The archesporial cell first becomes morphologically distinguishable from its surrounding
nucellar cells by its larger size and pronounced
nucleus, and it is called a megasporocyte when
a
b
it
ot
10µm
THE TRANSITION FROM
SOMATIC TO GERMLINE FATE
c
In angiosperms, the initial cells of the germline,
called archesporial cells, are formed de novo
from the hypodermal L2 cell layer of the ovule
primordium. Generally, in females, a single hypodermal L2 cell at the tip of the nucellus differentiates into the germline cell that enters the
meiotic pathway, which ultimately gives rise to
gametic cells: the egg and the central cell.
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
10µm
d
it
fc
ot
10µm
e
10µm
f
Figure 1
Development of the female gametophyte in
Arabidopsis. Confocal optical section showing
(a) nucleus with MMC ( green) and primordia of
inner (it) and outer (ot) integuments;
(b) one-nucleate embryo sac ( green) and
degenerating megaspores ( yellow) close to the
micropyle; (c) an early two-nucleate embryo sac
( green); (d ) a late two-nucleate embryo sac ( green),
inner (it) and outer (ot) integuments, and funiculus
(fc); (e) a four-nucleate embryo sac ( green); ( f ) an
early eight-nucleate embryo sac ( green), with
antipodal nuclei (pink), polar nuclei (blue), egg
nucleus (red ), and synergid nuclei ( yellow); ( g) a late
eight-nucleate embryo sac ( green), with antipodal
nuclei (pink), polar nuclei (blue), egg nucleus (red ),
and synergid nuclei ( yellow); (h) a mature four-celled
embryo sac ( green), with the secondary nucleus
(blue), egg nucleus (red ), and synergid nuclei
( yellow). Scalebar: 10 μm. Confocal images were
modified with PhotoShop to highlight the
megaspore mother cell, embryo sac, and nuclei.
10µm
g
10µm
h
10µm
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its nucleus enters the prophase of meiosis.
How the transition from a somatic cell fate
to a germline fate is controlled remains unknown. However, several putative components
that control this transition have been identified through genetic approaches. In Arabidopsis,
the SPOROCYTELESS gene (SPL/NOZZLE)
has been implicated in controlling germline
cell fate. In spl mutants, archesporial cells are
formed in both anther and ovule primodia, but
they fail to develop further, which results in a
complete lack of germline in male and female
organs (63, 75). This indicates that SPL plays an
essential role in germline formation. A recent
study revealed that the floral homeotic regulator AGAMOUS (AG) can activate the SPL
gene by binding to the CArG-box in its 3 region (24). SPL expression activated by AG induces the ectopic formation of microspores on
petaloid floral organs, which indicates ectopic
formation of the male germline. This finding
not only showed that SPL is a direct downstream target of AG but also demonstrated that
SPL is sufficient to trigger male germline specification in Arabidopsis. Whether SPL is also
sufficient for female germline specification remains unknown. SPL encodes a novel nuclear
protein with limited homology to MADS-box
transcription factors (63, 75). Therefore, how
SPL regulates its downstream genes in germline
specification is of great interest. Recently, researchers suggested that SPL may be involved in
auxin homeostasis by repressing YUCCA genes
in lateral organ development (32). It would be
interesting to investigate whether auxin is also
involved in germline formation.
Several genes that control the number
of cells entering germline fate have also
been identified. Mutation in MULTIPLE
ARCHESPORIAL CELLS 1 (MAC1) results
in an excessive number of archesporial cells
in maize (64). Similarly, in rice, the multiple
sporocyte 1 (msp1) mutants have increased numbers of both male and female sporocytes (45).
These excess sporocytes likely result from excessive archesporial cells, which suggests that
MSP1 is required for archesporial cell fate.
The MSP1 gene is expressed in nucellar cells
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that surround germline cells but not in the developing germline cells. This supports a role
for MSP1 in determining germline cell fate
by preventing the surrounding cells from becoming germline cells, similar to MAC1 in
maize (64). MSP1 encodes a leucine-rich repeat containing receptor-like kinase (LRRRLK). This implies that signaling between
the archesporial cell and its neighboring cells
is controlled by a ligand-receptor signaling
cascade, and this plays a critical role in female germline development. These findings
imply that a lateral inhibition mechanism may
act in controlling the number of germline
cells.
Because MSP1 is a membrane receptor kinase, it likely exerts its effects by binding to a
ligand. Recently, a putative ligand OsTDL1A
was shown to bind the extracellular domain
of MSP1 by yeast two-hybrid and BiFC experiments (78). Similar to MSP1, TDL1A is
expressed exclusively in nucellar cells but not
in germline cells. Furthermore, knockdown of
OsTDL1A expression phenocopies the msp1
phenotype in the nucellus. A similar mechanism, mediated by TPD1-EMS1/EXS1 signaling, controls male sporocyte fate (25, 36). These
data suggest that specification of germline cell
fate and number in plants involves a similar
ligand-receptor signaling system in both the
male and female.
In animals, germline fate is controlled by
a germline-specific PIWI-associated miRNA
(piRNA) system (33). Emerging data suggest
that miRNA also plays an important role in
germline development in plants. MEIOSIS
ARRESTED AT LEPTOTENE1 (MEL1), a
germline-specific member of ARGONAUTE
(AGO) genes family, is specifically expressed
in archesporial cells and sporogenous cells
(SCs), and disappears when SCs enter meiosis
in anther and ovule. Ovule development in
mel1 mutants is arrested at various stages from
pre-meiosis to tetrad. Chromosomes remain
uncondensed, and aberrant chromatin modification is detected in mel1 germline cells, which
suggests that MEL1 acts on chromatin structures, similar to those of the PIWI subfamily of
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AGOs in Drosophila. This implies that MEL1
is required for female germline development,
most likely by regulating cell division of
pre-meiotic germline cells, modification
of meiotic chromosomes, and progression of
meiosis; but it does not affect the initiation,
establishment, and early mitotic division of
germline cells (46).
Interestingly, the MEL1 expression domain
is larger than the germline cell in anther and
ovule primordia. Therefore, archespores may
be produced in excess of subsequent archesporial cells, and the fate of archesporial derivatives may be controlled by signals from SCs.
Therefore, MEL1 may suppress somatic gene
expression during germline development (46).
How does MEL1 function? MEL1 may modify
chromatin structure to repress the somatic gene
expression program in germline cells. Although
the role of MEL1 orthologs in germline formation has not been identified in other plants, this
demonstrates for the first time that, as in animals, the small RNA-mediated gene silencing
pathway mediated by MEL1 plays a key role in
plant germline formation (18).
SPECIFICATION OF THE
FUNCTIONAL MEGASPORE
The female megasporocyte undergoes meiotic
division to produce four haploid megaspores.
Of the four megaspores, one, two, or four may
participate in the formation of the final female
gametophyte depending on the plant species.
In the more advanced species, only one of the
four megaspores is functional, and the remaining three undergo programmed cell death. The
choice of functional megaspore is position dependent and also species dependent. In most
flowering plants, including Arabidopsis and rice,
the megaspore that is closer to the maternal tissue becomes the functional megaspore; distal
micropylar megaspores undergo programmed
cell death. Evolution seems to favor the more
defined monosporic type of gametogenesis, and
genetic mechanisms must have evolved to define such developmental control.
Observed in many species, polarity within
the megasporocyte is manifested by the polar distribution of organelles, the dynamic deposition of callose, and the microtubule cytoskeleton. So far, the role of this polarity on
megaspore development is unknown. The disruption of this polarity in megasporocytes was
observed in switch1 (swi1)/dyad ovules in Arabidopsis (42, 68). SWI1 encodes a novel protein
involved in chromatid cohesion establishment
and chromosome structure during meiosis (2,
38). Interestingly, dyad mutation causes defective meiosis that produces two unreduced
megaspores (diploid) (60). However, only the
chalazal megaspore, but not the micropylar
megaspore, expresses functional megasporespecific markers. This indicates that only the
chalazal megaspore is functional and suggests
a position-dependent mechanism. It also implies that a decision on cell fate has been made
at this stage of ovule development. In maize,
a similar mutation in ameiotic (am1) has been
identified in which meiosis is replaced by a mitotic division, as in swi1/dyad. Analysis of am1
allelic mutations indicates that the division of
the megasporocyte is completely blocked in
some alleles, or meiosis is initiated but not
completed in other alleles. However, all meiotic processes are impaired in am1. Together,
these data suggest that SWI and AM1 are essential for the switch between meiotic and mitotic division cycles and likely regulate the
transition through a novel leptotene–zygotene
checkpoint. AM1, which shares 30% identity with SWI1, is a plant-specific chromatinbinding protein with as yet unknown function
(54).
Surprisingly, the chalazal unreduced megaspore in dyad mutants occasionally proceeds to
form an unreduced embryo sac that can be fertilized to produce triploid seeds (60), which
may have implications for engineering hybrid
seed production in agriculture. This is likely
linked to the truncated SWI1 protein produced
in dyad. The functional dissection of SWI1 and
AM1 will shed light on how meiotic to mitotic
transition is regulated.
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PROGRESSION OF THE
GAMETOPHYTIC MITOTIC
CYCLE
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The functional megaspore undergoes rapid
growth, taking up the space left by the degenerating megaspores, and goes through three
consecutive rounds of karyokinesis to form an
eight-nucleate syncytial embryo sac. This sac
is cellularized simultaneously to form a sevencelled female gametophyte, composed of four
different cell types: egg, synergid, central, and
antipodal. In the past decade, genetic studies
have identified several mutations and genes that
control different stages of embryo sac development (50). Meanwhile, comparative expressionprofiling studies and cell-specific EST sequencing have revealed many genes that are expressed
in the female gametophyte (31, 70, 74, 76,
77). We discuss progress in each developmental stage and focus on recent important findings
below.
The Initiation of Female
Gametogenesis
Little is known about the genetic and molecular control of the initiation of female gametogenesis in flowering plants, although many
gametophytic mutations block embryo sac development at the one-nucleate stage. Mutations
in AGL23, a type I MADS-box gene, block the
first nuclear division of the functional megaspore (12). AGL23 expression is first detected
in the functional megaspore and persists in the
embryo sac. Together these data suggest that
AGL23-regulated transcription is required for
early female gametogenesis. However, AGL23
may not be required for the initiation or cell division of the functional megaspore, or cell cycle
progression during subsequent embryo sac development in Arabidopsis.
Using monoclonal antibodies against cell
wall components, female reproductive lineage
has been associated with distinct changes in
the distribution and types of arabinogalactan
protein (AGP) epitopes (11). Whether AGPs
function in cell surface signaling or recognition
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during gametogenesis remains to be clarified.
In AGP18 knockdown plants, the functional
megaspore fails to enlarge and divide. AGP18
is expressed in the female germline including
the functional megaspore, and it is weakly expressed in somatic nucellar cells. This suggests that a cell surface proteoglycan is required for functional megaspore development
in Arabidopsis (1).
Control of the Gametophytic
Cell Cycle
Many female gametophyte ( fem) mutations,
which were identified through a distorted
Mendelian segregation screen, display mitotic
arrest of the female gametophytic division cycle
(50). This indicates that progression of the mitotic cycle is critical for the formation of a functional gametophyte. Several mutants defective
in the progression of the mitotic division cycle
have been identified and molecular cloning of
these genes is starting to shed light on how cell
cycle progression is regulated during female gametogenesis in plants.
The
anaphase-promoting
complex/
cyclosome (APC/C) is a cell cycle–regulated,
multiple-subunit E3 ubiquitin-protein ligase
that controls important transitions during
mitotic progression and exit by sequentially
targeting for degradation many cell cycle
regulators, such as cyclins (55). The knockout
of APC/C components often impairs female
gametophyte development. Mutations in either
NOMEGA, which encodes APC6/CDC16,
or APC2, which interacts with APC11 and
APC8/CDC23, cause embryo sac arrest at the
two-nucleate stage (7, 29). This indicates that
the APC/C ubiquitin-mediated proteolysis
pathway plays a role in female gametophytic
cell cycle control. Similarly, mutations in
regulatory particle triple A ATPase (RPT ) of the
26S proteasome arrest embryo sac development at the one- or two-nucleate stage in the
rpt5a-4 rpt5b-1 double mutant, which indicates
a defect of the first or second mitosis of the
female gametophyte (17). Similarly, the double
mutation of two RING-finger E3 ligase genes
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RHF1a and RHF2a results in the interphase
arrest of the mitotic cell cycle in the female
gametophyte. RHF1a directly targets a cyclindependent kinase inhibitor ICK4/KRP6 for
proteasome-mediated degradation (34). This
suggests that the ubiquitin/26S proteasome
system helps control cell cycle progression
during female gametophyte development.
PRL encodes the DNA replication licensing
factor subunit MCM7 that is required in all
proliferating cells, including female germline
cells (69). Knockout of PRL function arrests
embryo sacs primarily at the one-nucleate stage.
Recently, we identified the slow walker1 (swa1)
mutation that causes slow progression of the
gametophytic division cycle and female sterility
owing to incomplete development of the female
gametophyte at anthesis (65). Delayed pollination tests showed that a small fraction of swa1
ovules are able to form functional female gametophytes; however, they missed the correct time
for fertilization because of the slow down of female gametophyte development when naturally
pollinated, which indicates that coordinated
development between the male and female gametophyte is critical for fertility in Arabidopsis.
SWA1 encodes a nucleolar WD40-containing
protein that is involved in the processing of
pre-18S rRNA in Arabidopsis, which suggests
that RNA biogenesis plays a role in the
progression of the gametophytic division cycle.
Mutations in the Arabidopsis retinoblastomarelated (RBR) gene, a key negative regulator
that controls G1/S transition by repressing E2F
transcription factors, result in arrested mitosis
and uncontrolled nuclear proliferation, which
gives rise to embryo sacs with supernumerary
nuclei that are irregular in size and partially enclosed by cell-wall-like structures (14). This indicates that cellularization and karyokinesis can
be uncoupled, and they are regulated independently. Consistently, premature cellularization
has been observed in hadad (hdd) ovules after
the first or second gametophytic division (41).
Although most proliferating rbr female gametophytes fail to express cell-specific markers, a
fraction of ovules in selfed rbr1–1/+ siliques
or rbr1–1/+ siliques that are pollinated with
wild-type pollen form abnormal embryos,
which implies that RBR is required for a complete differentiation of all gametophytic cells
(14, 26). This indicates that rbr mutant ovules
are able to cellularize and form functional egg
cells, which suggests that egg cell fate requires
the completion of a third nuclear division, but
not an arrest in the gametophytic cell cycle.
Therefore, RBR connects cell cycle control to
cellular differentiation processes.
In the indeterminate gametophyte1 (ig1) mutant of maize, female gametophytes have a
prolonged phase of free nuclear divisions before cellularization, which leads to a variety of
embryo sac abnormalities, including extra egg
cells, extra synergids, and extra central cells with
extra polar nuclei (16, 20). The rbr1 mutants of
Arabidopsis have a similar phenotype, with additional defects in pollen development. This suggests that IG1 restricts the proliferative phase
of female gametophyte development.
Together, these data suggest that timely mitotic progression of the division cycle is vital for gametogenesis. In addition to the conserved cell cycle machinery, other regulatory
mechanisms may play a role in gametophytic
cell fate in plants. One such mechanism is protein phosphorelay. The loss of CYTOKININ
INDEPENDENT1 (CKI1) function also results in the early degeneration of gametophytic
cells and excess nuclei (56). CKI1 encodes a
histidine kinase, which suggests that His/Asp
phosphorelay signaling plays a role in female
gametogenesis. At the onset of megagametogenesis, RNA interference depletes CHR11, a
member of the ATP-dependent SWI2/SNF2
family of chromatin-remodeling factors. This
depletion arrests uncellularized embryo sac development at the one-, two-, four-, or eightnucleate stages in Arabidopsis, which indicates
a role for chromatin-remodeling in karyokinesis during female gametogenesis (22). RBR
suppresses E2F-like protein activity by recruiting chromatin-remodeling factors of the
SWI2/SNF2 family. Together, CHR11 and
RBR regulate the E2F family proteins, and
thereby promote nuclear proliferation during
female gametogenesis. Furthermore, histone
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acetyltransferase HAM1 and HAM2 act redundantly during ovule development because ham1
ham2 double mutant embryo sacs arrest at the
one-nucleate stage with a huge nucleus (30),
which indicates that gene suppression and chromatin compaction requiring hypoacetylation of
histones in the functional megaspore block the
first karyokinesis during megagametogenesis.
CELLULARIZATION OF THE
EMBRYO SAC
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Cellularization of the syncytial embryo sac
is controlled temporally and spatially during
ovule development, and it is critical for gametophytic cell fate specification. Several genes have
been implicated in controlling this process. In
gemini pollen2 ( gem2), the cellularization of the
embryo sac is impaired: resulting in embryo
sacs that contain five nuclei at the micropylar
pole and three at the chalazal pole. Moreover,
no cell boundaries or only partial cellularizations are observed between nuclei. Most mature mutant embryo sacs contain one or two
extremely large nuclei, which might arise from
the fusion of free nuclei at the micropylar pole
(52). However, gem2 plants also display a variety of division defects in pollen development,
which include division asymmetry and incomplete cytokinesis. Together, these data suggest
that GEM2 plays a critical role in coordinating
karyokinesis and cytokinesis during gametogenesis. Interestingly, the partial cellularization of
gem2 ovules can develop further and form an
embryo sac with a large cell that possesses vacuolar characteristics of an egg cell, which suggests that egg cell fate can occur in a partially
cellularized embryo sac, and local cellularization may reinforce a gradient of cell fate determinants that are established in the coenocytic
embryo sac (52).
In addition, gem1/mor1 and two in one (tio)
mutants display similar or even more severe
ovule phenotypes as gem2. GEM1/MOR1 encodes a microtubule-associated protein (73),
and TIO encodes an essential phragmoplastassociated protein that is homologous to the
FUSED (Fu) Ser/Thr protein kinase of the
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hedgehog signaling complex in animals. Both
GEM1/MOR1 and TIO have a general effect
on cell plate formation in somatic and reproductive cells. The incomplete cell plate in tio
pollen is positioned correctly, which suggests
that TIO is not required for the positioning or
establishment of the cell plate but has a specific
role in cell plate expansion (47). In addition,
knockout of TUBG1 and 2 genes, which encode
γ-tubulin, results in uncellularized embryo sacs
with aberrant morphology, positioning, and
number of nuclei (53). In plant cells, the lateral
expansion of phragmoplast and cell plate is regulated by a kinesin-MAPKKK pathway during
cytokinesis; mutations in two kinesin-like proteins, AtNACK1 and AtNACK2, that bind and
activate the MAPKK kinase NPK1 result in the
mispositioning of nuclei and the formation of
nonfunctional gametophytes (72). Therefore,
they all play a role in positioning phragmoplast
and cell plate expansion, thereby controlling the
cellularization of the embryo sac. However, it
is not clear how the cell plate expansion phenotype is associated with the karyokinesis defect.
EMBRYO SAC POLARITY AND
GAMETOPHYTIC CELL
SPECIFICATION
The embryo sac is a polarized structure with
antipodal cells at the chalazal end and the egg
apparatus at the micropylar end. Gametophytic
cells within the embryo sac are also highly polarized. The nucleus of the egg cell is located
toward the chalazal end of the embryo sac,
whereas the nuclei of the synergid and central cells are located toward the micropylar end.
Therefore, the egg cell, and the central cell and
synergids have opposite polarity. The opposite
polarity of the central cell and egg brings their
nuclei into close proximity, which may facilitate their fusion with the sperm nuclei during
double fertilization. The final polarity of the
embryo sac is a result of coordinated nuclear
division and positioning, expansion of the central vacuole, and cellularization. This polarity
can be traced back to the four-nucleate stage,
when two pairs of nuclei, separated by a large
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central vacuole, migrate to opposite ends of the
syncytial embryo sac. At the chalazal pole, the
nuclei are positioned one above the other with
respect to the micropylar-chalazal axis. Meanwhile, the nuclei generally locate side by side
at the micropylar end. Comparatively large nucleoli distinguish the two polar nuclei in the
eight-nucleate stage. The migration and precise positioning of the nuclei and morphological differentiation of the polar nuclei suggest an
early distinction between the nuclei before cellularization. Polar expression of genes has also
been observed. For example, the DEMETER
(DME) gene, a key regulator of gene imprinting during endosperm development, is polarly
expressed in the micropylar domain of the embryo sac: first in the polar nuclei and synergid
nuclei before cellularization and then restricted
to the central cell after cellularization. FIS2, a
downstream gene of DME, is expressed only in
the polar nuclei but not in the future synergid
or egg, or antipodal nuclei (9). In rbr mutant
embryo sacs, FIS2 expression is lost or occasionally deregulated, which indicates the RBRcontrolled FIS2 polarity is nessessary for the
differentiation of the central cell in the embryo
sac (26). This polarity further suggests a role
for positional cues in gametic cell specification.
Compared to embryo sac polarity, the polarity within gametophytic cells is obviously established after cellularization of the eight-nucleate
embryo sac. The differentiation of egg and synergid cell fate also suggests that a lateral inhibition mechanism may exist for gametophytic
cell specification after cellularization (19).
Although the cellular and molecular basis
of gametophytic cell specification in the embryo sac is largely unknown, emerging evidence
supports the involvement of positional and lateral inhibition mechanisms in determining gametophytic cell fate. Several studies in maize
and Arabidopsis support the idea of a positional
mechanism. In the maize ig1 mutant, embryo
sacs undergo extra rounds of free nuclear divisions, which result in extra egg cells, extra central cells, and extra polar nuclei (17, 23). The final fate of the extra nuclei as either egg nuclei or
polar nuclei depends on their relative position
in the embryo sac. IG1 encodes a LATERAL
ORGAN BOUNDARIES (LOB) domain protein with high similarity to ASYMMETRIC
LEAVES2 (17), which controls leaf symmetry
in Arabidopsis. During female gametogenesis,
IG1 is expressed in functional, but not nonfunctional, megaspores; it is strong in antipodal cells
and the egg; and no signal is detected in the
synergids (16). Thus IG1 is asymmetrically expressed in the embryo sac, which supports the
existence of embryo sac polarity.
Recently, Sundaresan and colleagues discovered an asymmetric auxin gradient in the
syncytial embryo sac that plays a key role in
gametic cell specification (49). Using the synthetic DR5:GFP or DR5:GUS reporter that is
responsive to auxin, the auxin response can be
traced by monitoring reporter expression. During megasporogenesis, GFP or GUS expression
is detected at the distal tip of the nucellus and
increases in nucellar cells that surround the developing embryo sac at the early one-nucleate
stage. As the ovule develops, auxin level increases within the micropylar domain of the
embryo sac at the two- to eight-nucleate stages.
Interestingly, the auxin response distribution is
less polarized in the cellularized embryo sac,
because the reporter is expressed in all gametophytic cells. These data suggest a micropylarchalazal gradient of auxin in embryo sacs. Consistently, the disruption of auxin responses by
downregulating AUXIN RESPONSE FACTOR
(AFR) gene expression, or auxin synthesis by
ectopic expression of the auxin biosynthetic
YUCCA1 gene, impairs gametophytic cell identities at the micropylar domain. Specifically,
synergids adopt the fate of the egg cell in ARF
knockdown embryo sacs, and ectopic YUCCA1
expression results in the misspecification of all
gametophytic cells. However, no abnormalities
in embryo sac polarity or changes in central cell
and antipodal cell fates are observed. This suggests that such an auxin gradient is essential for
gametophytic cell specification but not for embryo sac polarity and central cell and antipodal cell fates. Furthermore, auxin polar transporters of the PIN family are not expressed
in the embryo sac, suggesting that the auxin
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gradient is correlated with location-specific
auxin biosynthesis and diffusion (49).
A fundamental question of female gametogenesis is, How is gametic cell fate determined?
As discussed above, embryo sac polarity and an
auxin gradient play a key role in gametophytic
cell fate. The manipulation of auxin responses
or synthesis results in the switching of gametic
and nongametic cell fates (49). To identify genes
that control egg cell fate, Gross-Hardt and colleagues (19) mutagenized an egg cell-specific
marker line and then screened for expression
changes of the egg cell-specific marker. They
identified three mutants, lachesis (lis), clotho (clo)
and atropos (ato), that showed deregulation of
the marker (19, 40). In lis embryo sacs, the expression of the egg–specific marker is expanded
to the synergids and central cell. Consistently
lis synergids display egg cell morphology defects and downregulate synergid-specific gene
expression. Pollen tube attraction is compromised, and reduced as well. These results indicate that the synergids have adopted an egg
cell fate in lis embryo sacs. Interestingly, the
ET884 synergid-specific marker is ectopically
expressed throughout lis embryo sacs. Similarly,
the central cell in lis embryo sacs also adopts
an egg cell fate. Polar nuclei rarely fuse and
cellularize separately to give rise to small uninucleate cells that are morphologically indistinguishable from the egg cell. Compromised
central cell fate is further suggested by the
downregulation of expression from the central cell-specific MEA promoter. Surprisingly,
the antipodal cells of lis embryo sacs adopt a
central cell fate as evidenced by their fusion,
and the downregulation of an antipodal-specific
marker, and the activation of a central cellspecific marker (19). A similar phenotype is also
found in the clo/gfa1 mutant (40). Unlike that
of the ig1 mutant in maize, the accessory cell
(synergid and antipodal cell) fates have been
mis-specified because no supernumerary nuclei
or cells are observed in lis or clo/gfa1 embryo
sacs. One idea that accounts for these phenotypes is that accessory cells are gradually recruited as gametic cells. This demonstrates a
central role for LIS and CLO/GFA1 in gametic
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cell fate specification during female gametophyte development. Furthermore, LIS nuclear
localization requires the CLO/GFA1 protein.
The findings above have several profound implications, as pointed out by Gross-Hardt and
colleagues (19). First, all gametophytic cells are
competent to adopt gametic cell fate, and LIS
is involved in a mechanism that represses gametic cell fate in accessory cells. Second, there
might be an intracellular signaling mechanism
that senses the number of nuclei in a given cell.
Third, there are two levels of cell fate regulation: one between the gametic cell and accessory cells, and the other between the egg cell
and central cell. Together, these genes might be
involved in an as yet unknown signaling pathway that operates in gametic cells and prevents
accessory cells from adopting a gametic cell fate.
Interestingly, LIS, CLO/GFA1, and ATO all
encode components of RNA splicing machinery. LIS is homologous to the yeast splicing
factor PRP4; CLO/GFA1 is a plant homolog
of yeast Snu114p, likely a component of the
U5 snRNP of the spliceosome, and is required
for the cell-specific expression of LIS gene (35,
40). This implies that LIS is downstream of
CLO/GFA1 in the pathway controlling gametic cell specification. In addition, LIS and
CLO/GFA1 are colocalized to nuclear speckles; this suggests they may form a complex as
well. ATO is homologus to SF3a60, a protein
that is implicated in prespliceosome formation.
These findings suggest that the RNA splicing
machinery plays an important role in gametic
cell specification in the female gametophyte, although the underlying mechanisms remain to
be elucidated.
The LIS gene is expressed strongly in reproductive tissues and remains high in gametic cells
but downregulated in accessory cells shortly after cellularization. Combined with its mutant
phenotype, this has led to a lateral inhibition
model in which, upon differentiation, gametic
cells generate an inhibitory signal that is transmitted to adjacent cells to prevent excess gametic cell formation (19). This model can explain the maintenance of only one egg cell in
the embryo sac after the initial specification of
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cell fate. However, once the egg cell is differentiated, a lateral inhibition mechanism may be
necessary to maintain cell fates because accessory cells can differentiate into gametic cells
later if this inhibitory mechanism is not present
(19).
EOSTRE, which encodes a BELL-like
homeodomain protein (BLH1), plays a role in
restricting synergid cell fate. In the eostre mutant, the female gametophyte is arrested at multiple stages that range from one-nucleate to
mature embryo sacs, and some mutant embryo
sacs collapse completely. The mutant embryo
sacs often display mispositioned nuclei during
the syncytial stage. Interestingly, a portion of
eostre embryo sacs displays abnormal cell specification, in which one of the two synergids exhibits polarity characteristic of the egg cell and
expresses an egg cell-specific marker. This indicates that one synergid has adopted an egg
cell fate, and therefore that there are two egg
cells in a single embryo sac, whereas the initial
central cell and the egg cell fate are not affected (51). Furthermore, the extra egg cell
can be fertilized after pollination, which indicates that it is fully functional. Molecular analysis showed that the eostre phenotype is caused
by the misexpression of the EOSTRE gene,
which is not expressed in the ovule in wild
type. BELL functions by forming a BELLKNAT heterodimer whose activity is regulated
by ovate family proteins (OFPs). Consistently,
the eostre phenotype can be reversed by a mutation in the class II knox gene KNAT3 and phenocopied by disruption of AtOFP5, a regulator
of BLH1-KNAT3 heterodimers (51). Together,
these data suggest a role for BLH-KNAT3
complex and AtOFP in gametic cell specification. Other BELL-like genes may substitute
the EOSTRE function to promote egg cell fate
in female gametophytes because the loss of
EOSTRE function has no effect on female gametophyte development. In addition, it would
be interesting to know whether the aberrant nuclear configuration observed in eostre syncytial
embryo sacs or the polarity change in one of
the synergid cells has any role in gametic cell
specification.
THE FUNCTIONAL FEMALE
GERM UNIT
The Egg Cell
Egg cell specification is a result of the interplay between the auxin gradient and the
LIS-mediated mechanism as discussed above.
Although many egg-specific transcripts have
been identified through single cell library and
EST analysis, key genes that control egg cell
function have not been identified. GAMETE
EXPRESSED3 (GEX3) is expressed specifically
in the egg cell of the female gametophyte and
in pollen, and encodes a plasma membranelocalized protein with unknown function that
has homologs in other plants. Both knockdown
and overexpression of GEX3 impair the female
control of micropylar pollen tube guidance (3).
Although the underlying mechanism is still unknown, this demonstrates a role for the egg cell
in the female control of pollen tube guidance,
in addition to fertilization.
The Synergid Cell
Synergid cells are key components of the female germ unit (FGU) and are located, side by
side with the egg cell, in the micropylar portion of the embryo sac. Typically, the synergid
cells display an opposite polarity compared to
the egg cell, they have no or discontinuous cell
wall at the chalazal end, and they are sealed by a
specialized cell wall-like structure—the filiform
apparatus at the micropylar opening. Often,
one of the two synergids undergoes cell death
upon arrival of the pollen tube. The synergids
likely play important roles in the attraction and
recognition of the pollen tube, sperm release,
and transportation. Therefore, genes that are
involved in those processes may be expressed in
synergids. However, the mechanisms by which
synergid cells develop their unique features are
poorly understood.
Mutations that affect synergid development
and function and genes that are specifically expressed in the synergids have been identified
(70). MYB98, which encodes a R2R3-type MYB
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transcription factor, is specifically expressed in
the synergids. Mutation in the MYB98 gene
specifically abolishes the formation of the filiform apparatus and has no effect on other aspects of ovule development (28). Thus, MYB98
is required specifically for the formation of
the filiform apparatus during synergid cell differentiation. Consistently, recent studies show
that MYB98 binds to a specific DNA sequence
(TAAC) and regulates a subset of genes that
encode secreted proteins targeted to the filiform apparatus (59). Most synergid-expressed
genes that are downregulated in myb98 encode small defensin-like cycteine-rich proteins
(CRPs) that are secreted into the filiform apparatus, which suggests that they play a role
in either the formation or the function of the
filiform apparatus (59). Many of these genes
are also weakly expressed in egg and/or central cells. Interestingly, myb98 female gametophytes that lack the filiform apparatus also lose
their ability to guide the pollen tube to the micropyle; therefore, MYB98 may also play a role
in the production of the guidance cue. Together,
these data strongly suggest that MYB98 acts
as a synergid-specific transcriptional regulator
to activate downstream genes that are required
for pollen tube guidance and filiform apparatus
formation.
To attract and recognize the pollen tube,
synergids need the ability to secrete pollen attracting signals and receive the pollen tube. Recent studies have provided strong evidence of
this. Using laser ablation, synergids, but not
any other gametophytic cells, were shown to
be required for pollen tube guidance in Torenia
fournieri (21). Also in T. fournieri, CRPs named
LUREs have been identified and are secreted
by synergids to attract pollen tubes in a semi–
in vivo assay (48). In Arabidopsis, CRPs are encoded by a large gene family and expressed in
the synergids and secreted into the filiform apparatus as discussed above. However, genetic
data that support their role as the guidance cue
are still lacking.
Synergid cells also play an essential role
for pollen tube reception. FERONIA (FER)
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(allelic to SIRENE, SRN) is a key gene that
controls the recognition between the synergids
and the pollen tube. In fer/srn ovules, the pollen
tube enters a synergid and overgrows within
the embryo sac (23, 61), which suggests that
FER/SRN plays a role in pollen tube reception
by the synergid. FER encodes a LRR-RLK that
accumulates specifically on the plasma membrane of the synergid cells (15). Therefore,
FER may be a synergid-specific membrane receptor which, upon binding to a signal from the
pollen tube, triggers a signaling cascade within
the synergids to prepare for fertilization and
also sends a signal to stop pollen tube growth
(15, 37). In support of this idea, additional
mutations are also reported in Arabidopsis. In
the lorelei (lre) mutant, pollen tubes that reach
embryo sacs often do not rupture but continue
to grow in the embryo sac, reminiscent of
the fer/srn phenotype. Moreover, lre embryo
sacs often attract additional pollen tubes.
LRE encodes a small plant-specific putative
glucosylphosphatidylinositol-anchored protein
and is expressed in synergid cells prior to fertilization (76). Pollen tubes of anxur1/anxur2
double mutants rupture before arriving at
the synergid cells (39). Both ANXUR1 and
2 genes encode receptor-like kinases that
are specifically expressed in pollen tubes. In
addition, mutations in ABERRANT PEROXISOME
MORPHOLOGY2/ABSTINENCE
BY MUTUAL CONSENT (APM2/AMC),
which is required for peroxisome transport,
impair pollen tube reception (5). This suggests
another signaling cascade, independent of the
FER/SRN-ANXUR kinase pathway that requires intact peroxisome function in both male
and female gametophytes, although the underlying mechanism remains to be elucidated.
Synergid cell death associated with fertilization is a common phenomenon, which has
been described in many plant species and invariably involves the collapse of vacuoles, a dramatic decrease in cell volume, and complete
disintegration of the plasma membrane and
most organelles. The underlying mechanisms
have not been revealed so far. In Arabidopsis,
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synergid cell death is initiated upon pollen tube
arrival but before pollen tube discharge, which
suggests that pollen tube-synergid contact triggers a signaling cascade that induces synergid
cell death (62). In gfa2 mutant ovules, the polar nuclei fail to fuse and the synergid persists after pollination. These ovules can attract
pollen tubes but are not fertilized. This indicates that synergid cell death associated with
fertilization did not occur, which suggests a
role for GFA2 in promoting synergid cell death
(10). The GFA2 gene encodes a mitochondrionlocated DnaJ domain–containing protein similar to yeast Mdj1p that functions as a chaperone in the mitochondrial matrix. Consistently,
GFA2 partially complements a yeast mdj1 mutant, which suggests a role for mitochondria
in synergid cell death in plants. How GFA2
acts in the mitochondria in promoting synergid cell death remains unknown. Interestingly, cell deaths of nonfunctional megaspores
and antipodal cells are not affected in gfa2 mutants; this suggests that cell death pathways
are different between synergids and antipodal
cells.
The Central Cell
Molecular mechanisms that control the specification and differentiation of the central cell
are poorly understood. Genetic evidence suggests that Type I MADS-box genes play an important role in central cell development. In the
diana (dia, agl61) mutant, polar nuclei of the
central cell are not fused, and central cell morphology is aberrant. The mutant embryo sac is
able to attract a pollen tube but fertilization of
the central cell does not occur (4, 71). Egg- and
synergid-specific markers, but not central cellspecific markers, are expressed in dia ovules,
which indicates that egg and synergid fates are
specified, and that central cell fate is impaired in
the mutant. DIA is expressed exclusively in the
late central cell, and the DIA protein is localized
in the polar nuclei and the central cell nucleus.
All these data suggest that DIA is required for
central cell differentiation and function. DIA
forms a heterodimer with AGL80, and its nuclear localization requires AGL80 because DIA
nuclear localization is lost in the agl80 mutant. AGL80 is also expressed in the polar nuclei and the secondary nucleus of the central
cell, and a mutation in the AGL80/FEM111
gene in Arabidopsis specifically affects central
cell maturation. Polar nucleoli and vacuole maturation fail and lead to endosperm development
arrests after fertilization. The egg, synergid,
and antipodal cells are correctly specified (57).
Therefore, both DIA and AGL80, most likely
forming a heterodimer, are required for polar nuclear fusion and central cell differentiation. Furthermore, AGL80, by interacting with
another Type I MADS-box protein AGL62,
also plays a critical role in endosperm development. AGL62 is expressed in the syncytial endosperm and is suppressed by the FIS Polycomb
complex just before endosperm cellularization.
Mutation in AGL62 causes precocious cellularization of the endosperm (13, 27). Together,
these Type I MADS-box transcription factors
are critical for central cell and endosperm development in Arabidopsis. It would be interesting to know the downstream genes controlled
by the DIA-AGL80 complex. Likely candidates
would be DD46 and DME, which are not expressed in agl80 mutant ovules (57). However,
there is no MADS-box binding site, the CArG
box [CC(A/T)6 GG] found in either gene, which
suggests that they may activate these downstream genes indirectly. Therefore, the DIAAGL80 complex may ultimately activate the
transcription of Polycomb group genes in the
central cell to repress endosperm development
prior to fertilization.
In magatama3 (maa3) mutant ovules, the polar nuclei fail to fuse at pollination and contain a
smaller nucleolus that lacks the vacuolar-like internal structure as compared to that of the wildtype. Consequently, central cell development is
arrested in the mutant, which ultimately results
in defective micropylar pollen tube guidance in
Arabidopsis (57). The MAA3 gene encodes a homolog of yeast SPLICING ENDONUCLEASE1 (SEN1) helicase involved in processing
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of a variety of RNA species in yeasts. Therefore, MAA3 may regulate the RNA metabolism
that is responsible for nucleolar organization
of the central cell and micropylar pollen tube
guidance.
The fusion of the polar nuclei is an important step in central cell development. Electron microscopy revealed that the fusion of
the polar nuclei begins with contact with endoplasmic reticulum (ER) membranes that are
continuous with the outer nuclear membranes
of the polar nuclei. First, the fusion with
the ER membranes gives rise to a continuous outer nuclear membrane that brings the
inner nuclear membranes into close contact,
which leads to its final fusion. So far, little is
known about the molecular basis of polar nuclear membrane fusion, although many mutations and genes have been identified (10, 50,
58). Interestingly, most of the genes whose
mutation blocks polar nuclear fusion encode
mitochondrial proteins. Similarly, mutation
in GLUCOSE 6-PHOSPHATE/PHOSPHATE
TRANSLOCATOR1 (GPT1) also blocks polar
nuclear fusion in the central cell (44). One possibility is that high respiratory activity is required for central cell development because the
central cell has such a large cytoplasm. Alternatively, an intracellular feedback mechanism
among the organellar and nuclear genomes may
coordinate central cell development. GFA2 has
been implicated in the membrane fusion. In
gfa2 mutants, the polar nuclei fail to fuse; their
outer nuclear membranes come into contact
but do not fuse (10). This suggests that GFA2,
either directly or indirectly, is required for
the membrane fusion of the polar nuclei in
Arabidopsis.
As the polar nuclei fuse, central cell specification and functional differentiation occur.
In glauce ( glc) mutant embryo sacs, gametophytic cells develop and are specified normally as manifested by the correct expression
of gametophytic cell-specific markers; however, the central cell cannot be fertilized (43).
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Genetic analysis suggests that GLC is epistatic
to MEA and plays an essential role in the maternal control of embryo and endosperm development, which suggests that it might play a
role in central cell competence for fertilization.
The molecular nature of GLC remains to be
revealed.
In addition to its role in fertilization, the
central cell also plays a role in pollen tube guidance. Pollen tube guidance is abolished in several mutants that disrupt central cell development. This includes maa1 and maa3 in which
the polar nuclei fail to fuse (66, 67), which indicates a defect in central cell development or/and
the maturation of the female gametophyte. In
contrast, in the central cell guidance (ccg) mutant, central cell development is not affected
because it does not display any morphological
abnormality and expresses a central cell-specific
marker (8). CCG is expressed in the central cell
of the mature embryo sac specifically and encodes a nuclear protein that might play a role
in regulating the expression of a subset of genes
that are necessary for pollen tube guidance in
the central cell.
CONCLUSIONS
Molecular mechanisms that control the
germline, gametic cell specification, and cellcell interactions in plant gametogenesis are
beginning to be revealed. Genes that control
these processes have been identified (Table 1).
The haploid female gametophyte provides
us with an exciting system to investigate
developmental roles of the RNA splicing
machinery; signaling pathways mediated by
membrane receptor kinases like MSP1, FER,
and ANUXR; and genetic control of cell fates.
Emerging combinatory approches that employ
genetics, single-cell based genomics, and
biochemistry will undoubtedly facilitate deciphering the genetic complexity and molecular
mechanisms that control female gametogenesis
in angiosperms.
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Table 1
26 March 2010
List of genes discussed in the text
Gene name
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Protein function
Biological function
Reference
SPOROCYTELESS
(SPL/NOZZLE)
Transcription regulator
Germline cell fate
24, 63, 75
AGAMOUS (AG)
MADS-box protein binds to CArG-box
DNA sequence
Activation of the SPL gene,
meristem determinacy and
floral organ identity
24
MULTIPLE ARCHESPORIAL
CELLS 1 (MAC1)
Not available
Germline cell number
64
MULTIPLE SPOROCYTE 1
(MSP1)
Leucine rich repeat–containing receptor
protein kinase
Numbers of male and female
sporocytes
45
OsTDL1A
Putative ligand of MSP1
Numbers of male and female
sporocytes
78
MEIOSIS ARRESTED AT
LEPTOTENE1 (MEL1)
A germline-specific member of
ARGONAUTE genes family
Germline development;
regulator of early meiosis
46
SWITCH1 (SWI1)/DYAD
Novel protein
Chromatid cohesion
establishment and chromosome
structure in meiosis
AMEIOTIC (AM1)
A plant-specific chromatin-binding
protein, with 30% identity with SWI1
Regulator of leptotene to
zygotene transition in meiosis
54
AGL23
Type I MADS-box family transcription
factor
Early female gametogenesis
12
ARABINOGALACTAN
PROTEIN 18 (AGP18)
A cell surface arabinogalactan proteoglycan
Functional megaspore
development
1
ANAPHASE-PROMOTING
COMPLEX/CYCLOSOME
(APC/C)
Multiple-subunit E3 ubiquitin-protein
ligase
Mitotic progression
NOMEGA/APC6/CDC16
A component of the Anaphase Promoting
Complex
Cell cycle control
7, 29
REGULATORY PARTICLE
TRIPLE A ATPASE (RPT)
A regulatory subunit of the 20S
proteosome; a member of the AAA
superfamily
Cell cycle control
17
RING-FINGER E3 LIGASE 1a
and 1b (RHF1a and RHF2a)
Ring-finger E3 ligase that targets a
cyclin-dependent kinase inhibitor
ICK4/KRP6 for proteosome-mediated
degradation
Cell cycle control
34
SLOW WALKER 1 (SWA1)
A nucleolar WD40-containing protein
controlling pre-18S rRNA processing
Cell cycle progression
65
RETINOBLASTOMA-RELATED
(RBR)
Negative regulator of G1/S transition
Cell cycle control
HADAD (HDD)
Not available
Cellularization of the embryo sac
INDETERMINATE
GAMETOPHYTE1 (IG1)
LATERAL ORGAN BOUNDARIES
(LOB) domain protein
Cell cycle control
CYTOKININ INDEPENDENT1
(CKI1)
Histidine kinase
Cytokinin signaling
56
CHROMATIN-REMODELING
FACTOR 11 (CHR11)
A member of the ATP-dependent
SWI2/SNF2 family of chromatinremodeling factors
Cell division control
22
GEMINI POLLEN2 (GEM2)
Not available
Cell division control
2, 38
7, 17, 29, 34
14, 26
41
16, 20
52
(Continued )
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(Continued )
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Gene name
Protein function
Biological function
Reference
GEM1/MOR1
A microtubule-associated protein
Cell plate formation
73
TWO IN ONE (TIO)
A phragmoplast-associated protein
Cell plate formation
47
AtNACK1 and AtNACK2
M-phase-specific kinesin-like protein
Phragmoplast and cell plate
expansion
72
DEMETER (DME)
DNA glycosylase
Gene imprinting during
endosperm development
9
FERTILIZATIONINDEPENDENT SEED2
(FIS2)
C2H2 zinc finger–containing polycomb
group protein
Suppressor of endosperm
development
26
LACHESIS (LIS)
RNA splicing factor
Gametic cell specification
19
CLOTHO (CLO)/GFA1
RNA processing
Gametic cell specification
35, 40
ATROPOS (ATO)
A component of prespliceosome and RNA
splicing machinery
Gametic cell specification
EOSTRE
A BELL-like homeodomain protein
Synergid cell fate
GAMETE EXPRESSED3 (GEX3)
A plasma membrane protein
Pollen tube guidance
3
MYB98
MYB family transcription factor
Filiform apparatus formation
and pollen tube guidance
59
FERONIA (FER) or SIRENE
(SRN)
Leucine rich repeat–containing receptor
protein kinase
Synergid-pollen tube interaction
LORELEI (LRE)
Putative
glucosylphosphatidylinositol-anchored
protein
Pollen tube attraction
76
ANXUR1 and 2
Pollen-specific receptor-like protein kinase
Pollen tube release
39
ABERRANT PEROXISOME
MORPHOLOGY2/
ABSTINENCE BY MUTUAL
CONSENT (APM2/AMC)
Src homology (SH3)-domain containing
peroxisomal membrane protein
Peroxisome transport and pollen
tube reception
5
GFA2
Mitochondrion-located DnaJ
domain–containing protein
Synergid cell death
10
DIANA (DIA, AGL61)
Type I MADS-box transcription factor,
forming a heterodimer with AGL80
Central cell differentiation and
function
4, 71
AGL80/ FEM111
Type I MADS-box transcription factor,
forming a heterodimer with DIA
Central cell differentiation and
function
57
AGL62
Type I MADS-box transcription factor
Central cell and endosperm
development
13, 27
MAGATAMA3 (MAA3)
RNA helicase involved in RNA splicing
Central cell maturation and
pollen tube guidance
57
GLUCOSE
6-PHOSPHATE/PHOSPHATE
TRANSLOCATOR1 (GPT1)
Transmembrane glucose 6–phosphate
translocator
Central cell development
44
GLAUCE (GLC)
Not available
Central cell function
43
CENTRAL CELL GUIDANCE
(CCG)
Putative transcription regulator
Pollen tube guidance
8
MAGATAMA 1 (MAA1)
Not available
Central cell development and
pollen tube guidance
66
104
Yang
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Shi
Chen
51
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DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
The authors acknowledge financial support from the National Science Foundation of China to
Y. W. C. (30830063) and D. Q. S. (3060032), and also from the Chinese Academy of Sciences to
W. C. Y. (KSCX2-YW-N-048).
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
by Universidad Veracruzana on 01/08/14. For personal use only.
LITERATURE CITED
1. Acosta-Garcı́a G, Vielle Calzada J-P. 2004. A classical arabinogalactan protein is essential for the initiation
of female gametogensis in Arabidopsis. Plant Cell 16:2614–28
2. Agashe B, Prasad CK, Siddiqi I. 2002. Identification and analysis of DYAD: a gene required for meiotic
chromosome organization and female meiotic progression in Arabidopsis. Development 129:3935–43
3. Alandete-Saez M, Ron M, McCormick S. 2008. GEX3, expressed in the male gametophyte and in the egg
cell of Arabidopsis thaliana, is essential for micropylar pollen tube guidance and plays a role during early
embryogenesis. Mol. Plant 1:586–98
4. Bemer M, Wolters-Arts M, Grossniklaus U, Angenent GC. 2008. The MADS domain protein DIANA acts
together with AGAMOUS-LIKE80 to specify the central cell in Arabidopsis ovules. Plant Cell 20:2088–101
5. Boisson-Dernier A, Frietsch S, Kim TH, Dizon MB, Schroeder JI. 2008. The Peroxin loss-of-function
mutation abstinence by mutual consent disrupts male-female gametophyte recognition. Curr. Biol. 18:63–68
6. Capron A, Gourgues M, Neiva LS, Faure JF, Berger F, et al. 2008. Maternal control of male-gamete
delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. Plant
Cell 20:3038–49
7. Capron A, Serralbo O, Fulop K, Frugier F, Parmentier Y, et al. 2003. The Arabidopsis anaphase-promoting
complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15:2370–82
8. Chen YH, Li HJ, Shi DQ, Yuan L, Liu J, et al. 2007. The central cell plays a critical role in pollen tube
guidance in Arabidopsis. Plant Cell 19:3563–77
9. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, et al. 2002. DEMETER, a DNA glycosylase
domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110:33–
42
10. Christensen CA, Gorsich SW, Brown RH, Jones LG, Brown J, et al. 2002. Mitochondrial GFA2 is required
for synergid cell death in Arabidopsis. Plant Cell 14:2215–32
11. Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG. 2007. Arabinogalactan proteins as molecular
markers in Arabidopsis thaliana sexual reproduction. J. Exp. Bot. 58:4027–35
12. Colombo M, Masiero S, Vanzulli S, Lardelli P, Kater MM, et al. 2008. AGL23, a type I MADS-box gene
that controls female gametophyte and embryo development in Arabidopsis. Plant J. 54:1037–48
13. De Folter S, Immink RGH, Kiefer M, Parenicova L, Henz SR, et al. 2005. Comprehensive interaction
map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–33
14. Ebel C, Mariconti L, Gruissem W. 2004. Plant retinoblastoma homologues control nuclear proliferation
in the female gametophyte. Nature 429:776–80
15. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, et al. 2007. The FERONIA
receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–60
16. Evans MMS. 2007. The INDETERMINATE GAMETOPHYTE1 gene of maize encodes a LOB domain
protein required for embryo sac and leaf development. Plant Cell 19:46–62
17. Gallois JL, Guyon-Debast A, Lécureuil A, Vezon D, Carpentier V, et al. 2009. The Arabidopsis proteasome
RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy.
Plant Cell 21:442–59
18. Grant-Downton R, Dickinson H. 2007. Germlines: Argonautes go full cycle. Curr. Biol. 17:R920
www.annualreviews.org • Female Gametogenesis
105
ARI
26 March 2010
21:40
19. Gross-Hardt R, Kägi C, Baumann N, Moore JM, Baskar R, et al. 2007. LACHESIS restricts gametic cell
fate in the female gametophyte of Arabidopsis. PLoS Biol. 5:494–500
20. Guo FL, Huang BQ, Han YZ, Zee SY. 2004. Fertilization in maize indeterminate gametophyte1 mutant.
Protoplasma 223:111–20
21. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima SY, et al. 2001. Pollen tube attraction by
the synergid cell. Science 293:1480–83
22. Huanca-Mamani W, Garcia-Aguilar M, León-Martı́nez G, Grossniklaus U, Vielle-Calzada JP. 2005.
CHR11, a chromatin-remodeling factor essential for nuclear proliferation during female gametogenesis
in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102:17231–36
23. Huck N, Moore JM, Federer M, Grossniklaus U. 2003. The Arabidopsis mutant feronia disrupts the female
gametophytic control of pollen tube reception. Development 130:2149–59
24. Ito T, Wellmer F, Yu H, Das P, Ito N, et al. 2004. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–60
25. Jia G, Liu X, Owen HA, Zhao D. 2008. Signaling of cell fate determination by the TPD1 small protein
and EMS1 receptor kinase. Proc. Natl. Acad. Sci. USA 105:2220–25
26. Johnston AJ, Matveeva E, Kirioukhova O, Grossniklaus U, Gruissem W. 2008. A dynamic reciprocal
RBR-PRC2 regulatory circuit controls Arabidopsis gametophyte development. Curr. Biol. 18:1680–86
27. Kang I-H, Steffen JG, Portereiko MF, Lloyd A, Drews GN. 2008. The AGL62 MADS domain protein
regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20:635–47
28. Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN. 2005. MYB98 is required
for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17:2981–92
29. Kwee HS, Sundaresan V. 2003. The NOMEGA gene required for female gametophyte development
encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis.
Plant J. 36:853–66
30. Latrasse D, Benhamed M, Henry Y, Domenichini S, Kim W, et al. 2008. The MYST histone acetyltransferases are essential for gametophyte development in Arabidopsis. BMC Plant Biol. 8:121
31. Le Q, Gutierrez-Marcos JF, Costa LM, Meyer S, Dickinson HG, et al. 2005. Construction and screening
of substracted cDNA libraries from limited populations of plant cells: a comparative analysis of gene
expression between maize egg cells and central cells. Plant J. 44:167–78
32. Li LC, Qin GJ, Tsuge T, Hou XH, Ding MY, et al. 2008. SPOROCYTELESS modulates YUCCA expression to regulate the development of lateral organs in Arabidopsis. New Phytol. 179:751–64
33. Lin H. 2007. piRNA in the germ line. Science 316:397
34. Liu J, Zhang Y, Qin G, Tsuge T, Sakaguchi N, et al. 2008. Targeted degradation of the cyclin-dependent
kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during
Arabidopsis gametogenesis. Plant Cell 20:1538–54
35. Liu M, Yuan L, Liu NY, Shi DQ, Liu J, et al. 2009. GAMETOPHYTIC FACTOR 1, involved in premRNA splicing, is essential for megagametogenesis and embryogenesis in Arabidopsis. J. Integr. Plant Biol.
51:261–71
36. Ma H. 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering
plants. Annu. Rev. Plant Biol. 56:393–434
37. McCormick S. 2007. Plant science. Reproductive dialog. Science 317:606–7
38. Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, et al. 2001. SWITCH1 (SWI1): a novel protein
required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes
Dev. 15:1859–71
39. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, et al. 2009. ANXUR1 and 2, sister genes
to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19:1327–31
40. Moll C, von Lyncker L, Zimmermann S, Kägi C, Baumann N, et al. 2008. CLO/GFA1 and ATO are
novel regulators of gametic cell fate in plants. Plant J. 56:913–21
41. Moore JM, Calzada JPV, Gagliano W, Grossniklaus U. 1998. Genetic characterization of hadad, a mutant
disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harbor Symp. Quant. Biol. 62:35–47
42. Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O, et al. 2000. switch (swi1), an Arabidopsis
thaliana mutant affected in the female meiotic switch. Sex. Plant Reprod. 12:209–18
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
by Universidad Veracruzana on 01/08/14. For personal use only.
ANRV410-PP61-05
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Yang
· ·
Shi
Chen
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
by Universidad Veracruzana on 01/08/14. For personal use only.
ANRV410-PP61-05
ARI
26 March 2010
21:40
43. Ngo QA, Moore JM, Baskar R, Grossniklaus U, Sundaresan V. 2007. Arabidopsis GLAUCE promotes fertilization-independent endosperm development and expression of paternally inherited alleles.
Development 134:4107–17
44. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, et al. 2005. The Arabidopsis plastidic glucose 6phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development.
Plant Cell 17:760–75
45. Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, et al. 2003. The MSP1 gene is necessary
to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall
formation in rice. Plant Cell 15:1728–39
46. Nonomura KI, Morohoshi A, Nakano M, Elguchi M, Mlyao A, et al. 2007. A germ cell-specific gene
of the ARGONAUTE family is essential for the progression of pre-meiotic mitosis and meiosis during
sporogenesis in rice. Plant Cell 19:2583–94
47. Oh SA, Johnson A, Smertenko A, Rahman D, Park SK, et al. 2005. A divergent cellular role for the
FUSED kinase family in the plant-specific cytokinetic phragmoplast. Curr. Biol. 15:2107–11
48. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, et al. 2009. Defensin-like polypeptide LUREs are
pollen tube attractants secreted from synergid cells. Nature 458:357–61
49. Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V. 2009. Auxin-dependent patterning and
gamete specification in the Arabidopsis female gametophyte. Science 324:1684–89
50. Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, et al. 2005. Genetic and molecular identification of
genes required for female gametophyte development and function in Arabidopsis. Development 132:603–14
51. Pagnussat GC, Yu HJ, Sundaresan V. 2007. Cell-fate switch of synergid to egg cell in Arabidopsis eostre
mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell
19:3578–92
52. Park SK, Rahman D, Oh SA, Twell D. 2004. Gemini pollen 2, a male and female gametophytic cytokinesis
defective mutation. Sex. Plant Reprod. 17:63–70
53. Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K, et al. 2006. γ-Tubulin is essential for
microtubule organization and development in Arabidopsis. Plant Cell 18:1412–25
54. Pawlowskia PW, Wang CJR, Golubovskaya IN, Szymaniaka JM, Shi L, et al. 2009. Maize AMEIOTIC1
is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc. Natl.
Acad. Sci. USA 106:3603–8
55. Perez-Perez JM, Serralbo O, Vanstraelen M, Gonzalez C, Criqui MC, et al. 2008. Specialization of
CDC27 function in the Arabidopsis thaliana anaphase-promoting complex (APC/C). Plant J. 53:78–89
56. Pischke MS, Jones LG, Otsuga D, Fernandez DE, Drews GN, et al. 2002. An Arabidopsis histidine kinase
is essential for megagametogenesis. Proc. Natl. Acad. Sci. USA 99:15800–5
57. Portereiko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, et al. 2006a. AGL80 is required for central
cell and endosperm development in Arabidopsis. Plant Cell 18:1862–72
58. Portereiko MF, Sandaklie-Nikolova L, Lloyd A, Dever CA, Otsuga D, et al. 2006b. NUCLEAR FUSION
DEFECTIVE1 encodes the Arabidopsis RPL21M protein and is required for karyogamy during female
gametophyte development and fertilization. Plant Physiol. 141:975–85
59. Punwani JA, Rabiger DS, Drews GN. 2007. MYB98 positively regulates a battery of synergid-expressed
genes encoding filiform apparatus–localized proteins. Plant Cell 19:2557–68
60. Ravi M, Marimuthu MPA, Siddiqi I. 2008. Gamete formation without meiosis in Arabidopsis. Nature
451:1121–24
61. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE. 2003. Female control of male gamete
delivery during fertilization in Arabidopsis thaliana. Curr. Biol. 13:432–36
62. Sandaklie-Nikolova L, Palanivelu R, King EJ, Copenhaver GP, Drews GN. 2007. Synergid cell death in
Arabidopsis is triggered following direct interaction with the pollen tube. Plant Physiol. 144:1753–62
63. Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, et al. 1999. Molecular analysis of
NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in
Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96:11664–69
64. Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya IN. 1996. The mac1 gene: controlling the commiment to the meiotic pathway in maize. Genetics 142:1009–20
www.annualreviews.org • Female Gametogenesis
107
ARI
26 March 2010
21:40
65. Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, et al. 2005. SLOW WALKER1, essential for gametogenesis
in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17:2340–54
66. Shimizu KK, Ito T, Ishiguro S, Okada K. 2008. MAA3 (MAGATAMA3) helicase gene is required for female
gametophyte development and pollen tube guidance in Arabidopsis thaliana. Plant Cell Physiol. 9:1478–83
67. Shimizu KK, Okada K. 2000. Attractive and repulsive interactions between female and male gametophytes
in Arabidopsis pollen tube guidance. Development 127:4511–18
68. Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V. 2000. The dyad gene is required for progression through
female meiosis in Arabidopsis. Development 127:197–207
69. Springer PS, Holding DR, Groover A, Yordan C, Martienssen RA. 2000. The essential MCM7 protein
PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally
for early Arabidopsis development. Development 127:1815–22
70. Steffen JG, Kang IH, Macfarlane J, Drews GN. 2007. Identification of genes expressed in the Arabidopsis
female gametophyte. Plant J. 51:281–92
71. Steffen JG, Kang IH, Portereiko MF, Lloyd A, Drews GN. 2008. AGL61 interacts with AGL80 and is
required for central cell development in Arabidopsis. Plant Physiol. 148:259–68
72. Tanaka H, Ishikawa M, Kitamura S, Takahashi Y, Soyano T, et al. 2004. The AtNACK1/HINKEL and
STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for
cytokinesis in Arabidopsis. Genes Cell 9:1199–211
73. Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, et al. 2002. MOR1/GEM1 has an essential role
in the plant-specific cytokinetic phragmoplast. Nat. Cell Biol. 4:711–14
74. Yang H, Kaur N, Kiriakopolos S, McCormick S. 2006. EST generation and analyses towards identifying
female gametophyte-specific genes in Zea mays. L. Planta 224:1004–14
75. Yang WC, Ye D, Xu J, Sundaresan V. 1999. The SPOROCYTELESS gene of Arabidopsis is required for
initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13:2108–17
76. Yu HJ, Hogan P, Sundaresan V. 2005. Analysis of the female gametophyte transcriptome of Arabidopsis
by comparative expression profiling. Plant Physiol. 139:1853–69
77. Weterings K, Russell SD. 2004. Experimental analysis of the fertilization process. Plant Cell
16(Suppl.):S107–18
78. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, et al. 2008. OsTDL1A binds to the LRR domain of
rice recaptor kinase MSP1 and is required to limit sporocyte numbers. Plant J. 54:375–87
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
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Contents
Volume 61, 2010
A Wandering Pathway in Plant Biology: From Wildflowers to
Phototropins to Bacterial Virulence
Winslow R. Briggs p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Structure and Function of Plant Photoreceptors
Andreas Möglich, Xiaojing Yang, Rebecca A. Ayers, and Keith Moffat p p p p p p p p p p p p p p p p p p p p p21
Auxin Biosynthesis and Its Role in Plant Development
Yunde Zhao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p49
Computational Morphodynamics: A Modeling Framework to
Understand Plant Growth
Vijay Chickarmane, Adrienne H.K. Roeder, Paul T. Tarr, Alexandre Cunha,
Cory Tobin, and Elliot M. Meyerowitz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p65
Female Gametophyte Development in Flowering Plants
Wei-Cai Yang, Dong-Qiao Shi, and Yan-Hong Chen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
Doomed Lovers: Mechanisms of Isolation and Incompatibility in Plants
Kirsten Bomblies p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 109
Chloroplast RNA Metabolism
David B. Stern, Michel Goldschmidt-Clermont, and Maureen R. Hanson p p p p p p p p p p p p p p 125
Protein Transport into Chloroplasts
Hsou-min Li and Chi-Chou Chiu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157
The Regulation of Gene Expression Required for C4 Photosynthesis
Julian M. Hibberd and Sarah Covshoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 181
Starch: Its Metabolism, Evolution, and Biotechnological Modification
in Plants
Samuel C. Zeeman, Jens Kossmann, and Alison M. Smith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Improving Photosynthetic Efficiency for Greater Yield
Xin-Guang Zhu, Stephen P. Long, and Donald R. Ort p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235
Hemicelluloses
Henrik Vibe Scheller and Peter Ulvskov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263
Diversification of P450 Genes During Land Plant Evolution
Masaharu Mizutani and Daisaku Ohta p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291
v
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Evolution in Action: Plants Resistant to Herbicides
Stephen B. Powles and Qin Yu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Insights from the Comparison of Plant Genome Sequences
Andrew H. Paterson, Michael Freeling, Haibao Tang, and Xiyin Wang p p p p p p p p p p p p p p p p 349
High-Throughput Characterization of Plant Gene Functions by Using
Gain-of-Function Technology
Youichi Kondou, Mieko Higuchi, and Minami Matsui p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 373
Histone Methylation in Higher Plants
Chunyan Liu, Falong Lu, Xia Cui, and Xiaofeng Cao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 395
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
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Genetic and Molecular Basis of Rice Yield
Yongzhong Xing and Qifa Zhang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 421
Genetic Engineering for Modern Agriculture: Challenges and
Perspectives
Ron Mittler and Eduardo Blumwald p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 443
Metabolomics for Functional Genomics, Systems Biology, and
Biotechnology
Kazuki Saito and Fumio Matsuda p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 463
Quantitation in Mass-Spectrometry-Based Proteomics
Waltraud X. Schulze and Björn Usadel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 491
Metal Hyperaccumulation in Plants
Ute Krämer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517
Arsenic as a Food Chain Contaminant: Mechanisms of Plant Uptake
and Metabolism and Mitigation Strategies
Fang-Jie Zhao, Steve P. McGrath, and Andrew A. Meharg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 535
Guard Cell Signal Transduction Network: Advances in Understanding
Abscisic Acid, CO2 , and Ca2+ Signaling
Tae-Houn Kim, Maik Böhmer, Honghong Hu, Noriyuki Nishimura,
and Julian I. Schroeder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561
The Language of Calcium Signaling
Antony N. Dodd, Jörg Kudla, and Dale Sanders p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 593
Mitogen-Activated Protein Kinase Signaling in Plants
Maria Cristina Suarez Rodriguez, Morten Petersen, and John Mundy p p p p p p p p p p p p p p p p p 621
Abscisic Acid: Emergence of a Core Signaling Network
Sean R. Cutler, Pedro L. Rodriguez, Ruth R. Finkelstein, and Suzanne R. Abrams p p p p 651
Brassinosteroid Signal Transduction from Receptor Kinases to
Transcription Factors
Tae-Wuk Kim and Zhi-Yong Wang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 681
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Contents
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15:25
Directional Gravity Sensing in Gravitropism
Miyo Terao Morita p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 705
Indexes
Cumulative Index of Contributing Authors, Volumes 51–61 p p p p p p p p p p p p p p p p p p p p p p p p p p p 721
Cumulative Index of Chapter Titles, Volumes 51–61 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 726
Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org
by Universidad Veracruzana on 01/08/14. For personal use only.
Errata
An online log of corrections to Annual Review of Plant Biology articles may be found at
http://plant.annualreviews.org
Contents
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