Download Polycomb-group (Pc-G) Proteins Control Seed Development in

Journal of Integrative Plant Biology 2007, 49 (1): 52−59
. Invited Review .
Polycomb-group (Pc-G) Proteins Control Seed
Development in Arabidopsis thaliana L.
Xiao-Xue Wang and Li-Geng Ma*
(National Institute of Biological Sciences, Beijing 102206, China)
Abstract
Polycomb-group (Pc-G) proteins repress their target gene expression by assemble complexes in Drosophila and mammals. Three groups of Pc-G genes, controlling seed development, flower development and
vernalization response, have been identified in Arabidopsis (Arabidopsis thaliana L.). MEDEA (MEA), FERTILIZATION INDEPENDENT SEED2 (FIS2), and FERTILIZATION INDEPENDENT ENDOSPERM (FIE) are Pc-G genes
in Arabidopsis. Their functions in seed development have been extensively explored. The advanced findings of molecular mechanism on how MEA, FIS2 and FIE control seed development in Arabidopsis are
reviewed in this paper.
Key words: Arabidopsis; FIS1/MEA; FIS2; FIS3/FIE; Pc-G genes.
Wang XX, Ma LG (2007). Polycomb-group (Pc-G) proteins control seed development in Arabidopsis thaliana L. J Integr Plant
Biol 49(1), 52−59.
Available online at www.blackwell-synergy.com/links/toc/jipb, www.jipb.net
Polycomb-group (Pc-G) genes are highly conserved regulatory factors that are responsible for the maintenance of silent
states of genes. Pc-G genes were initially characterized in
Drosophila mutants that failed to maintain the transcriptional
repression of homeobox genes in the HOX cluster (Francis
and Kingston 2001). Pc-G proteins assemble into two distinct
complexes to exert their respective functions by modifying
chromatin structure. The first types of Pc-G complexes described in Drosophila, called the E(z)/ESC complex or the
Polycomb Repressive Complex 2 (PRC2), contains four PcG
proteins: Enhancer of zeste [E(z)], extra sex combs (ESC),
suppressor of Zeste 12 (Su(z)12) and the histone binding protein NURF-55. E(z) methylates lysine 27 of histone H3 (H3K27)
(Francis et al. 2001; Czermin et al. 2002; Cao and Zhang 2004),
creating an epigenetic mark that leads to the recruitment of the
second type of Pc-G complex, named PRC1, via binding of the
Received 19 Jul. 2006
Accepted 13 Oct. 2006
Publication of this paper is supported by the National Natural Science
Foundation of China (30624808) and Science Publication Foundation of the
Chinese Academy of Sciences.
* Author for correspondence. Tel: +86 (0)10 8072 7510; Fax: +86 (0)10 8072
7511; E-mail: <[email protected]>.
© 2007 Institute of Botany, the Chinese Academy of Sciences
doi: 10.1111/j.1672-9072.2007.00415.x
chromodomain of one of its components, the Polycomb (PC)
protein. PC is a core component of PRC1, together with
Polyhomeotic (PH), Posterior sex combs (PSC), and dRing (Shao
et al. 1999). PRC1 can mediate silencing of target genes, by
interfering with SWI/SNF chromatin remodeling machinery,
blocking transcriptional initiation, or recruiting additional silencing activity (Shao et al. 1999; Francis and Kingston 2001; Müller
et al. 2002; Czermin et al. 2002; King et al. 2002; Dellino et al.
2004; Lavigne et al. 2004; Plath et al. 2004).
The plant Pc-G genes were identified genetically from
screens for mutations affecting seed formation, flower development and vernalization response. Several Pc-G proteins have
been identified as developmental regulators in plants. Experimental data indicates the presence of PRC2, ESC-E(z)-like complexes in plants, no evidence for the existence of PRC1,
however, has been reported. To date, three PRC2 complexes
have been well characterized.
The MEA-FIE complex has specific functions during gametophyte and early seed development, including suppression of
seed development in the absence of fertilization and repression of PHERES1 (PHE1) (Ohad et al. 1996; Chaudhury et al.
1997; Grossniklaus et al. 1998; Kiyosue et al. 1999; Ohad et al.
1999; Köhler et al. 2003). A second PRC2 complex, the CURLY
LEAF (CLF) complex, most likely represses transcription of floral homeotic genes, such as the MADS-box gene AGAMOUS
(AG). The CLF complex probably consists of MSI1, the E(z)
Pc-G in Seed Development 53
homolog CLF, FIE, and the Su(z)12 homolog EMBRYONIC
FLOWER2 (EMF2) (Goodrich et al. 1997; Kinoshita et al. 2001;
Yoshida et al. 2001; Hennig et al. 2003; Chanvivattana et al.
2004; Katz et al. 2004; Schönrock et al. 2006). The CLF
complex represses the expression of MADS-box gene AGL19.
AGL19 is a potent floral activator. AGL19 chromatin is strongly
enriched in trimethylation of Lys 27 on histone H3 (H3K27me3),
which is mediated by the Pc-G proteins CLF and MSI1 in the
absence of cold. Prolonged cold relieves AGL19 from the CLF
complex repression. Elevated AGL19 levels activate LFY and
AP1 and eventually cause flowering. The third potential PRC2like complex is the VERNALIZATION (VRN) complex. The existence of the VRN complex was hypothesized because the Su
(z)12 homolog VRN2 is required for maintaining repression of
the MADS-box gene FLOWERING LOCUS C (FLC) after vernalization and for vernalization-induced H3 methylation at the
FLC locus (Chandler et al. 1996; Gendall et al. 2001; Bastow et
al. 2004; Chanvivattana et al. 2004; Sung and Amasino 2004).
In this review, we will focus on the recent advances on the
molecular repression mechanism of the three Pc-G proteins,
MEA/FIS1, FIS2 and FIE/FIS3, in Arabidopsis seed development.
mea, fis2 and fie are Mutations That Allow
Endosperm Development Without Fertilization
The two products of fertilization, which are the embryo and
endosperm, display distinct patterns of development. Fertilization of the egg cell by a sperm cell gives rise to a diploid embryo
(Goldberg et al. 1994). Fertilization of the central cell by the
second sperm cell generates the triploid endosperm. Distinguishing to embryogenesis, fertilized triploid central cell nucleus,
also termed primary endosperm nucleus, undergoes a series
of mitotic divisions to produce a syncytium of nuclei that surround the embryo and fill the expanding central cell (Mansfield
and Briarty 1990a,b; Webb and Gunning 1991; Berger 1999;
Brown et al. 1999). The endosperm nurtures the developing
embryo and is ultimately absorbed by embryo development.
To understand how fertilization initiates reproductive
development, three mutants, fis1/mea, fis2 and fis3/fie, have
been isolated (Ohad et al. 1996; Chaudhury et al. 1997;
Grossniklaus et al. 1998; Kiyosue et al. 1999; Ohad et al. 1999).
The fis-class mutations (fis1/mea, fis2 and fis3/fie) allow for
the replication of the central cell nucleus without fertilization. In
the fis mutants, a number of steps in seed development occur
without pollination, including the autonomous development of
diploid endosperm, a low frequency development of globular,
embryo-like structures, and the partial development of ovules
into seeds, indistinguishable from developing sexual seeds in
size and external morphology. Most fis-class seeds do not
develop beyond the endosperm cellularization stage before
atrophying. These results indicate that a substantial activation
of genes involved in seed development is induced in plants
carrying the mutated alleles at the FIS loci. All of the three genes
have been isolated (Ohad et al. 1996; Chaudhury et al. 1997;
Grossniklaus et al. 1998; Kiyosue et al. 1999; Ohad et al. 1999).
It is known that FIS1/MEA and FIS3/FIE are Arabidopsis
homologs of the Drosophila Pc-G genes E(z) and ESC, respectively (Grossniklaus et al. 1998; Kiyosue et al. 1999; Ohad
et al. 1999). FIS2 is a homolog of the recently identified Drosophila Pc-G gene Su (z)12 (Luo et al. 1999; Birve et al. 2001).
As mentioned, the function of Pc-G protein complexes is to
repress their targets gene expression in Drosophila. Thus, the
possible mechanisms for how FIS genes regulate replication
of the central cell nucleus in response to fertilization is that FIS
proteins prevent the central cell from initiating endosperm
development, and fertilization results in the inactivation of FIS
proteins or delivers other factors to trigger the endosperm
development. The mutations at FIS loci result in the production
of inactive FIS proteins, so that fertilization is no longer required for initiation of endosperm development. The hypothesis
is confirmed in the following experiments.
MEA and FIE Proteins Form a Complex to
Control Seed Development
MEA and FIE are orthologs of the polycomb genes E(z) and
Esc in Drosophila. In the Drososphila these gene products
interact as part of a protein complex that is associated with the
changes in chromatin architecture and repression of gene expression (Furuyama et al. 2003; Tie et al. 2003). Mutants of the
FIS class (presently including fis1/mea, fis2, and fis3/fie) disrupt normal endosperm and embryo development. The common
phenotype suggests that FIS1/MEA, FIS2 and FIS3/FIE may function in the same complex. Thus physical interaction between
the Arabidopsis MEA and FIE proteins has been tested by using yeast two-hybrid assay (Luo et al. 2000; Spillane et al.
2000). The results showed us that MEA polypeptides can interact physically with the FIE protein. The FIS2 protein, however,
does not physically interact with either the MEA or FIE protein
(Luo et al. 2000; Spillane et al. 2000). This lack of evidence
could mean that another protein may be needed in the complex
to facilitate the interaction of FIS2 with MEA and FIE. The question remains as to what is the target(s) of MEA-FIE Pc-G complex in Arabidopsis.
Expression of a MADS-box Gene PHERES1 is
Regulated by MEA-FIE Pc-G Complex to
Control Seed Development
The Pc-G proteins, MEA, FIE and FIS2 regulate seed development in Arabidopsis by repressing embryo and endosperm
54
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2007
proliferation without fertilization. All three of these FIS-class
proteins are likely subunits of a multiprotein Pc-G complex, but
the direct targets for MEA-FIE complex remain poorly defined.
PHE1 was identified as a possible target of MEA-FIE complex
by using the microarray approach to uncover genes whose
expressions were upregulated in mea and fie mutant (Köhler et
al. 2003; Schubert and Goodrich 2003; Köhler et al. 2005).
To characterize the expression pattern of PHE1, the expression of PHE1 in flowers before fertilization, open pollinated flowers (0−1 DAP), seeds containing embryos at the early globular
stage (2−3 DAP), and seeds containing embryos at the late globular stage (3−4 DAP) were analyzed. No PHE1 expression is
detectable before pollination; however, it becomes detectable in
seeds containing preglobular-stage embryos in wild-type plants.
In contrast, PHE1 expression in all three fis-class mutants initiated earlier than in wild-type plants, starting directly after
pollination, because of the removal of the repression of MEA-FIE
Pc-G complex. It remains upregulated in the fis mutants, consistent with the proposed function of the FIS genes as transcriptional repressors. Reduced expression levels of PHE1 in mea
mutant seeds can suppress mea seed abortion, indicating a key
role of PHE1 repression in seed development. Confirmation that
PHE1 is a direct target of MEA-FIE Pc-G complex came from
chromatin immunoprecipitation (ChIP) experiments using antibodies against MEA and FIE Pc-G proteins, which showed that
MEA and FIE bind to the PHE1 promoter. Their results showed
us that PHE1 expression is commonly upregulated in mea, fie,
and fis2 mutants, even though the extent of upregulation can
differ among the fis-class mutants. These findings support the
hypothesis that the FIS proteins are part of a common protein
complex repressing common target genes (Grossniklaus et al.
1998; Luo et al. 2000; Spillane et al. 2000; Yadegari et al. 2000).
Results from Makarevich et al. (2006) reveal the existence of
common target genes of different Pc-G complexes in
Arabidopsis (Makarevich et al. 2006). They show that the plant
Pc-G target gene PHE1 is regulated by histone trimethylation
on H3K27 residues (H3K27me3) mediated by at least two different Pc-G complexes MEA-FIE complex and the CLF/
SWINGER (SWN) complex in plants, which contain SET domain
proteins MEA or CURLY LEAF/SWINGER.
PHE1 gene encodes MADS-box transcription factor, regulated by MEA-FIE Pc-G complex to control normal seed development in Arabidopsis. In contrast, Pc-G complexes in Drosophila and mammals maintain the repressive state of homeobox
gene expression, such as HOX genes in Drosophila, suggesting the evolutionary diversity in plant and animal kingdoms.
development is dependent on extrazygotic influences. The classical view is that both endosperm and the sporophyte play an
important role in the nutrition of the embryo. This is probably
correct, although somatic- and microspore-derived embryogenesis is possible under artificial conditions in tissue culture. A
more interesting possibility, that extrazygotic cells directly control the expression of certain genes in the embryo, is relatively
unexplored (Ray 1998). The finding of molecular mechanisms of
MEA imprinting provides sound events for this hypothesis.
MEA is the first-identified imprinted gene in Arabidopsis. The
maternal allele of MEA is expressed and the paternal allele is
repressed in endosperm. In genetic analysis only the maternal
wild-type MEA allele, and not the paternal MEA allele, is required for proper embryo and endosperm development
(Chaudhury et al. 1997; Grossniklaus et al. 1998; Kiyosue et al.
1999; Kinoshita et al. 1999).
The uncovering of the MEA imprinting mechanism is triggered
by the isolation of the DEMETER (DME) gene, which encodes
a large protein with the DNA glycosylase and a nuclear localization domain. Choi et al. (2002) isolated a mutant, named
demeter (dme), that causes parent-of-origin effects on seed
viability. Seed viability depends solely on the maternal DME
allele. DME, primarily expressed in the central cell, is required
for the maternal allele expression of MEA in the central cell and
the endosperm. These results suggest DME is required for the
maternal expression of the imprinted MEA gene in the central
cell; a process that is essential for subsequent embryo and
endosperm viability (Choi et al. 2002; Lohe and Chaudhury 2002;
Dickinson and Scott 2002).
Seed abortion caused by DME mutation is suppressed by
maternal inherited MET1 if a wild-type maternal MEA allele is
present (Xiao et al. 2003). Maternal mutant dme or mea alleles
result in seed abortion. Seeds with maternal dme and met1
alleles, however, survive, indicating that met1 is the suppressor of dme. DME activates whereas MET1 suppresses maternal MEA::GFP allele expression in the central cell (Xiao et al.
2003), convincing us of the antagonistic interaction between
DME and MET1 gene products. MET1 is responsible for de
novo and maintenance of DNA methylation to keep MEA silenced
in the central cell. DME could antagonize MET1 by specifically
removing 5-methylcytosine from MEA, allowing the maternal
MEA allele to be expressed and form a complex before
fertilization. The maternal allele of MEA is expressed, but the
paternal allele is repressed in the endosperm after fertilization
(Choi et al. 2004, Gehring et al. 2004). The suppressed mechanism of MEA paternal allele is the next question to be addressed.
Antagonistic Interaction Between DME and
MET1 to Control MEDEA Imprinting
MEA-FIE Complex Maintains MEA Paternalallele Silencing
An open question in plant biology is the extent to which embryo
A major breakthrough on the role of Pc-G proteins in imprinting
Pc-G in Seed Development 55
sheds light on the molecular mechanism of imprinting in both
plants and animals. Gehring et al. (2006) found that paternal
MEA allele expression is not subject to the same controls as
the maternal MEA allele. MEA methylation is maintained by MET1.
Whenever DME activity removes methylation from its promoter,
MEA protein is produced and integrated into MEA-FIE complex
in the central cell. After fertilization, the MEA-FIE complex
targets the paternal allele of MEA to maintain its silent state.
It is the first time it has been found that Polycomb group
proteins that are expressed from the maternal genome, including MEA, silence the paternal MEA allele. This showed a novel
example of self-imprinting. Integration of the findings draws a
nice picture of the molecular mechanism of imprinting in plant
seed development (Figure 1) and enlarges our views on the
Figure 1. Model for MEA imprinting and endosperm development mechanism.
MEA methylation in either male or female gametophyte is maintained by MET1. In the central cell, expression of MEA is demethylated and
activated by the activity of DME. MEA protein is produced and integrated into Pc-G complex, which is termed MEA-FIE Pc-G complex.
Repression of PHE1 by MEA-FIE Pc-G complex blocks cell proliferation, which is essential for normal seed development. After fertilization,
maternal MEA continues to be expressed in the endosperm. MEA-FIE Pc-G complexes target the paternal allele to maintain its silent state.
The signal from male or other tissue triggers the disintegration of MEA-FIE Pc-G complex and activates the expression of PHE1 to promote
endosperm development. Black circles, methyl groups.
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2007
Figure 2. Comparison of imprinting in plants and mammals.
(A) In plants, embryo and endosperm are two products derived from the fertilized egg and central cell. Imprinting is only confined to
endosperm in plants. Silent methylation state is maintained in micro- or megaspore mother cell during flower development. Egg, central
cell, and sperm are the products of female and male gametogenesis, respectively, in Arabidopsis. The activity of DME, a DNA glycosylase,
activates the maternal diploid alleles by demethylation in central cell before fertilization. After fertilization, the paternal allele is repressed
in endosperm by the self-imprinting mechanism known for MEA imprinting or the mechanism unknown. Imprinting in planta endosperm is
one-way control because the endosperm vanishes after nurturing the developing embryo.
(B) In mammals, the repression of the paternal allele in sperm is established after meiosis through methylation or another mechanism.
Inactivated paternal allele is present in both the embryo and placenta (the similar organ to endosperm in plants). The imprinted state is
maintained throughout the somatic organ development. The repressed methylation state is removed just before the regeneration of
germline for the next generation. Black box, imprinted gene in plants; Empty box, imprinted gene in mammals; Black circles, methyl groups.
Pc-G in Seed Development 57
differential mechanisms for genomic imprinting in plants and
animals. It should be pointed out that there is an argument regarding the autoregulation of MEA imprinted expression. Data
from Baroux et al. (2006) indicates that autorepression of the
maternal MEA allele is direct and independent of the MEA-FIE
complex, which is similar to the E(Z)-ESC complex of animals
(Baroux et al. 2006).
MEA is Necessary for PHE1 Repression
Much more interestingly, PHE1 is another imprinted gene in
Arabidopsis. PHE1 is mainly paternally expressed but maternally repressed. The maternal repression of PHE1 is disrupted
in seeds lacking maternal MEA activity, indicating the role of PcG proteins in the control of PHE1 imprinting, which is one of the
imprinting mechanisms existing in mammals. The mouse
Polycomb group protein EED, a homolog of FIE, is required to
maintain silencing of some imprinted autosomal gene (Delaval
and Feil 2004). The evidence of PHE1 imprinting is an example
of a gene imprinted oppositely to MEA, such that the maternal
allele is largely silent and the paternal allele is expressed in the
endosperm. MEA-FIE Pc-G complex likely assemble at the maternal PHE1 allele in the central cell before fertilization (Köhler
et al. 2005). The SET domain of MEA is essential for the allele
specific expression of PHE1 by repressing the maternal PHE1
allele (Makarevich et al. 2006). The SET domain of MEA mediates
the PHE1 repression by setting histone trimethylation on H3K27
residues, which is a different mechanism to MEA imprinting.
DNA Methylation is Responsible for Silencing
of FIS2 Paternal Allele
FIS2 is another gene, which is subject to parental genomic
imprinting (Jullien et al. 2006a,b). FIS2 is a maternally expressed
imprinted gene. Unlike MEA, FIS2 and MEA imprinting follows
distinct molecular mechanisms. DNA methylation mediated by
MET1 activity is responsible for silencing of FIS2 paternal allele.
A CpG domain upstream of FIS2 that is targeted by MET1 is one
of the three DNA methyltransferases responsible for both de
novo DNA methylation and maintenance of the DNA methylated
state is associated with the control of FIS2 imprinting. MET1 dependent silencing of FIS2 is required during the vegetative
phase, male gametogenesis, and endosperm development; when
it maintains silencing of the paternal allele. Similarly, FIS2 is
activated during female gametogenesis by DME, leading to the
expression of maternal alleles in the endosperm after fertilization.
In the endosperm, the paternal allele remains silenced through
the continuous action of MET1.
DNA methylation, histone methylation and self-regulated imprinting mediated by histone methylation show us the diversity
of imprinting mechanisms in plants. In addition, the mechanisms
of imprinting in plants and animals are different (Surani et al.
1984; Reik et al. 2001; Reik and Walter 2001; Surani 2001; Scott
and Spielman 2004; Kinoshita et al. 2004; Arnaud and Feil 2006).
The placenta in mammals and the endosperm in plants function
as the extra-embryonic tissues to nurture the embryo and to
connect the embryo to the maternal tissue. The plant endosperm
and the mammalian placenta are both subjected to imprinting,
resulting in expression of maternal copies of genes and the
repression of the paternal alleles of genes, most notably those
playing an essential role in growth and development (Figure 2).
In plants, imprinted-gene expression seems to be confined to
the endosperm, which is one of the two double fertilization
products (Figure 2A). In contrast, imprinting in mammals occurs both in the embryo and the placenta. In both plants and
animals, however, DNA methylation is essential for imprinting.
In mammals, DNA methylation marks are present at the key
regions that control imprinting (Figure 2B). These marks are
established in germ lines by de novo DNA methyltransferase.
After fertilization, they are maintained throughout development
in all the somatic lineages. The imprinting needs to be erased
and reset before passing to the next generation to allow the
establishment of novel imprints. Unlike the situation in mammals,
endosperm-specific imprinting in plants is conferred through
the specific demethylation in the female gametophyte, where
DME is believed to be the main player. The imprinted status in
plants is confined to the endosperm, which does not contribute
to the next generation (Figure 2A). Thus the erasure of imprinting status is omitted in plants.
Growing evidence suggests that Pc-G proteins participate in
a wide range of developmental processes in both plant and
animal kingdoms. Decoding molecular mechanisms of plant PcG repression will not only contribute to the understanding of
the molecular mechanism during plant development, but will
also enlarge our view on the epigenetic control of both plant
and animal development.
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Schönrock N, Bouveret R, Leroy O, Borghi L, Köhler C, Gruissem
(Handling editor: Yong-Biao Xue)