Update on Polycomb Group Complexes
Polycomb Group Complexes Mediate Developmental
Transitions in Plants1
Sarah Holec and Frédéric Berger*
Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604 (S.H., F.B.);
and Department of Biological Sciences, National University of Singapore, Singapore 117543 (F.B.)
The modulation of transcription by chromatin
modifications participates in the coordination of gene
networks regulating development. Chromatin marks
deposited by Polycomb group (PcG) complexes induce a repressive state of the transcription, which is
propagated through cell division. Here, we focus on
the implications of this epigenetic regulation in the
development of flowering plants like Arabidopsis. We
present the mechanism of chromatin modification by
PcG and its modulation by other factors. We discuss in
detail the mechanisms leading to flowering and illustrate how PcG controls major progressions through the
life cycle.
The life cycle of eukaryotes is marked by developmental phases characterized by specific spatial and
temporal regulation of genome expression. Dynamic
regulation of chromatin state is crucial to ensure
proper regulation of gene expression. The mechanisms
involved in this regulation comprise nuclear localization, DNA methylation, histone variant replacement,
and histone posttranslational modifications that recruit or release various chromatin remodeling factors and govern nucleosome occupancy on the DNA
(Margueron and Reinberg, 2010).
Among the regulators of chromatin state and transcription, Polycomb group (PcG) genes were first
discovered in Drosophila melanogaster as repressors of
the homeotic Hox genes involved in embryo segmentation (Lewis, 1978; Jürgens, 1985). Four PcG proteins
form the core Polycomb Repressive Complex2 (PRC2):
Enhancer of Zeste [E(z)], Suppressor of Zeste12 [Su(z)
12], Extra sex combs (Esc), and p55. When properly
assembled in a protein complex by p55 and Esc, E(z)
trimethylates histone H3 Lys-27 (H3K27me3) at target
loci (Nekrasov et al., 2005). This mark induces a
durable transcriptional silencing (Fig. 1). In the absence of PcG activity, the initial pattern of Hox genes
breaks down, causing embryo developmental arrest.
PcG proteins were likely present in the last common
ancestor of eukaryotes and are conserved from unicellular organisms to metazoans, and plants but were
lost in yeast (Shaver et al., 2010; Margueron and
Reinberg, 2011). Here, we summarize the nature of
1
This work was supported by the Temasek Life Sciences Laboratory.
* Corresponding author; e-mail [email protected].
www.plantphysiol.org/cgi/doi/10.1104/pp.111.186445
plant PcG complexes and their mode of action.
We describe how PcG complexes interact with other
chromatin-modifying complexes and influence gene
expression. Furthermore, we detail the specific role of
plant PcG complexes in developmental transitions that
require coordinated regulation of gene networks.
THE MOLECULAR ACTORS OF
PCG-MEDIATED REPRESSION
In Arabidopsis (Arabidopsis thaliana), PcG proteins
form a family of eight homologs of PRC2 components.
The homologs of E(z) are MEDEA, CURLY LEAF (CLF),
and SWINGER. Su(z)12 also has three homologs, EMBRYONIC FLOWER2 (EMF2), FERTILIZATION INDEPENDENT SEED2 (FIS2), and VERNALIZATION2
(VRN2). Esc and p55 have the single homologs FERTILIZATION INDEPENDENT ENDOSPERM (FIE)
and MULTICOPY SUPPRESSOR OF IRA1 (MSI1),
respectively (Fig. 2).
FIE and MSI1 are expressed in all cell types, but the
expression of other PRC2 homologs is more restricted,
and molecular and genetic evidences support the idea
of at least three forms of PRC2 in plants: FIS, VRN, and
EMF, as per the different Su(z)12 homologs (Spillane
et al., 2000; Yoshida et al., 2001; Köhler et al., 2003;
Chanvivattana et al., 2004; De Lucia et al., 2008). The FIS
complex, for instance, is active in the female gametophyte and developing seed endosperm (Köhler et al.,
2003; Guitton et al., 2004), whereas the EMF complex
acts in the embryo and during subsequent sporophytic
development (Goodrich et al., 1997; Yoshida et al.,
2001). The VRN complex activity is triggered upon
association with PHD proteins VERNALIZATION INSENSITIVE3 (VIN3), VERNALIZATION LIKE1 (VEL1;
also known as VIN3-LIKE2 [VIL2]), and VERNALIZATION5 (VRN5; also known as VIL1) and represses
targets of vernalization, the prolonged cold period
that allows annual plants to flower in spring (Fig. 2).
A comparable association of PRC2 with PHD proteins
was observed in animals (Nekrasov et al., 2007; Sarma
et al., 2008).
In Drosophila, stable transcriptional repression
by the PRC2 complex requires the activity of other
proteins complexes: PRC1, Pleiohomeotic Repressive
Complex, and a newly identified module named PRDUB (Zheng and Chen, 2011). PRC1, in animals, binds
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Holec and Berger
Figure 1. Action of Polycomb and Trithorax complexes. PRC2 complexes trimethylate the Lys-27
residue of H3K27me3 and induce a silenced state
of the chromatin at the target locus. This mark is
recognized by the PRC1 complex. In animals, this
complex then monoubiquitinates H2A and triggers a compaction of the chromatin into a heterochromatin state that stably represses expression.
The components of PRC1 complex are not fully
described in plants so far. PRC2 activity of repression is antagonized by the function of Trithorax
(TRX). Trithorax trimethylates the histone H3
Lys-4 residue (H3K4me3) and induces the expression of target loci. Although Trithorax function
has been found in plants, the complex has not
been identified yet.
to H3K27me3 marks and ubiquitinates H2A Lys-119.
As a consequence, chromatin is compacted in a stable
heterochromatin state, and transcription is durably
repressed (Sawarkar and Paro, 2010). In plants, homologs have been identified for the PRC1 components
BMI1 and RING1. Monoubiquitination of H2A Lys121 in Arabidopsis by AtBMI1A and AtBMI1B is
implicated in repression of embryonic and stem cell
regulators (Bratzel et al., 2010). AtBMI1C physically
interacts with AtRING1A/B and may be involved in
flowering regulation (Li et al., 2011). AtRING1A and
AtRING1B also associate with LIKE HETEROCHROMATIN PROTEIN1 (LHP1) to form a complex similar
to the animal PRC1 (Xu and Shen, 2008; Fig. 1). There
are no clear homologs of other members of PRC1
defined in animals. However, proteins with an activity
comparable to PRC1 have been identified in Arabidopsis. LHP1 binds H3K27me3 (Turck et al., 2007) and
shares a subset of PRC2 targets in a manner similar to
Pc, a PRC1 component in animals (Bracken et al.,
2006). With the exception of an impact on flowering
time (Mylne et al., 2006; Sung et al., 2006), the lhp1
phenotype is quite distinct from the phenotypes of
mutants affecting PRC2 (Gaudin et al., 2001; Takada
and Goto, 2003). Two other proteins, VRN1 and EMF1,
which bind and act together with LHP1 and AtBMI1A/B (Bratzel et al., 2010), have been proposed to
be involved in PRC1-like functions (Mylne et al., 2006;
Calonje et al., 2008). Hence, several proteins with an
activity similar to PRC1 components are specific to
plants. Because PRC1 homologs are not conserved
between animal species, it may not be surprising that
PRC1 function in plants is mediated by mechanisms
distinct from that described in mammals.
POLYCOMB AND TRITHORAX COMPLEXES ARE
ANTAGONIZING EACH OTHER
As opposed to PRC2, Drosophila Trithorax group
proteins cause trimethylation of H3 Lys-4 and positively regulate transcription. The Arabidopsis genome
encodes five ARABIDOPSIS TRITHORAX proteins
(ATX1 to ATX5), with a SET domain and a PHD domain,
and seven ARABIDOPSIS TRITHORAX-RELATED
proteins (ATXR1 to ATXR7; Tamada et al., 2009).
ATXR5 and ATXR6 do not appear to be directly related
to ATXR function defined as antagonists to PRC2
and rather cause H3K27 monomethylation associated
with constitutive heterochromatin (Jacob et al., 2009;
Roudier et al., 2011). ATX1 and ATXR7 are required for
the expression of homeotic genes involved in flower
organogenesis and the floral repressor FLOWERING
LOCUS C (FLC; Pien et al., 2008; Tamada et al., 2009).
Besides its H3K4 methylation activity, ATX1 influences
transcription by recruiting the TATA binding protein
and RNA Polymerase II at promoters (Ding et al.,
2011).
Although ULTRAPETALA1 (ULT1) has no homology
with animal Trithorax group components, it functions
as a Trithorax factor regulating in an opposed manner
to PRC2 a common set of loci silenced by CLF. However, ULT1 does not have a methlytransferase activity
but rather helps recruiting ATX members on the DNA
(Carles and Fletcher, 2009). Hence, it is possible that
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Epigenetic Control of Developmental Transitions
Figure 2. Components of complexes associated with PRC2, PRC1, or Trithorax functions in Arabidopsis. While PRC2 complexes
are well established, the other complexes are currently hypothetical.
ATX1, ATXR7, and ULT1 associate to form a Trithorax
complex that may contain other proteins (Fig. 1).
Similarly, the chromatin remodeling factors PICKLE
and PICKLE RELATED2 antagonize CLF for the regulation of root meristematic growth (Aichinger et al., 2011).
In conclusion, PRC2 is conserved in plants, but the
regulatory PRC1 and TRX activities also are mediated by
nonconserved protein complexes that evolved independently from their functional counterparts in metazoans.
ates. Then, FLC becomes expressed again during early
embryogenesis (Sheldon et al., 2008; Choi et al., 2009;
Kim et al., 2009). The mode of deposition and removal of
H3K27 methylation that accompanies the cycle of FLC
expression have been studied in much detail and provide a good study case. The cycle can be divided in four
steps: deposition, spreading, maintenance, and removal.
Deposition
THE INS AND OUTS OF H3K27ME3 MARK
ON CHROMATIN
As many other annual species, Arabidopsis flowers in
spring after an obligate period of cold in winter (vernalization). However, some natural accessions of Arabidopsis flower late in summer and do not require
vernalization. Such natural variations rely primarily
on the regulation of two factors, FRIGIDA and FLC
(Koornneef et al., 1994; Lee et al., 1994). FLC encodes a
MADS box transcription factor that represses flowering.
At the FLC locus, H3K27me3 marks accumulate during
vernalization, and FLC expression remains repressed
throughout the life cycle until seed development initi-
How PRC2 is recruited on specific targets to deposit
the H3K27me3 mark is still largely unknown. Some
DNA sequences of the Hox loci in Drosophila are
recognized by PRC2 complexes and are called Polycomb response elements (PREs). However, the degree
of conservation of these elements is low across animal
species, and no PRE has been found in plants to date.
Nonetheless, at the FLC locus, some cis-sequences in
the promoter and intron 1 are required for the establishment of repression (Sheldon et al., 2002). Some of
these sequences play a role in assisting the recruitment of the noncoding RNA COLDAIR (for COLD
ASSISTED INTRONIC NONCODING RNA) that is
required for establishing stable repressive chromatin
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Holec and Berger
by recruiting PRC2 (Heo and Sung, 2011). In addition,
COOLAIR (for COLD INDUCED LONG ANTISENSE
INTRAGENIC RNA) is an antisense transcript initiated after the polyadenylation site of FLC that is
induced by cold early in the vernalization process
and silences FLC (Swiezewski et al., 2009). The role of
long noncoding RNAs is reminiscent of the silencing
by the XIST noncoding RNA and PRC2 in mammals
(Margueron and Reinberg, 2011), and further analyses
may show a generalization of this mechanism (Spitale
et al., 2011). Hence, it is likely that PRE represents only
the sequence complementary to a specific element of
the long noncoding RNA that forms a complex with
PRC2, and if true, this hypothesis would explain the
lack of conservation of PREs.
It is also possible that other mechanisms participate
to PRC2 recruitment. In animals, the JumonjiC (JmjC)
domain protein Jarid2 anchors PRC2 but inhibits its
repressive action. It remains to be discovered whether
plant homologs of Jarid2 fulfills the same role (Zheng
and Chen, 2011). In addition, a combination of histone
modifications could also be read by PRC2 complexes
or associated proteins to specify a target.
Spreading
Analyses of transgenes carrying FLC and a fusion
protein have shown that PRC2 can spread from an
initial entry site to methylate histones at adjacent
sequences (Schubert et al., 2006). However, genomewide studies showed that H3K27me3 marks do not
extend over large regions in plants as it does in flies
and mammals but are restricted to discrete domains
(Turck et al., 2007; Zhang et al., 2007). The PHD
proteins VIN3, VRN5 (VIL1), and VEL1 (VIL2; Sung
et al., 2006) that enhance the VNR complex activity at
vernalization were shown to play a role in the spreading of H3K27me3 marks on FLC locus upon return of
warm temperature (De Lucia et al., 2008).
At the tissue level, spreading of H3K27me3 marks
takes place only in dividing cells (Finnegan and
Dennis, 2007). In root meristems, a pFLC-GUS reporter
is expressed in a salt and pepper pattern after a limited
period of vernalization. This is interpreted as two
populations of cells, one with FLC still expressed and
another with FLC expression suppressed. The gradual
reduction of FLC expression would result from an
increased proportion of cells with FLC expression
turned off, and a mathematical model has been proposed to back up this hypothesis. The model proposes
a switching mechanism involving the local nucleation
of opposing histone modifications (Angel et al., 2011).
(Hansen et al., 2008). It was hypothesized that the
spreading of H3K27me3 also plays a role in this mitotic
inheritability, as a critical number of modified nucleosomes at one locus may be necessary to ensure the
fidelity of the epigenetic information being passed along
mitosis (Schubert et al., 2006).
Possible additional mechanisms for this controlled
inheritance have been proposed in mammals where it
was shown that PcG proteins have the ability to stay
bound on replicating DNA. As noncoding RNAs have
been observed to play a role in PRC2 recruitment,
RNA could be the molecule passing along the information (Sawarkar and Paro, 2010).
In addition, H3K27me3 recognition by PRC1 induces chromatin compaction, thus enforcing a stable
repression and cellular memory of PRC2 marks. But in
the case of FLC, none of these mechanisms has been
identified and the maintenance of H3K27me3 at FLC
locus remains to be understood.
Removal
FLC expression resumes after flowering, during the
early stages of seed development in the embryo but
not in the endosperm (Sheldon et al., 2008; Choi et al.,
2009). This period coincides with the time when histones H3 transmitted by the gametes are actively
removed after fertilization and replaced by newly
synthesized histone H3 variants in the zygote but not
in the endosperm (Ingouff et al., 2010). Thus, resetting
the H3 proteins provides a potential global mechanism
to discard H3K27me3 as well as other marks carried by
the nucleosomes at the FLC locus (Fig. 3). This model is
supported by the association between histones and
FLC reactivation (Yun et al., 2011).
A second possible mechanism of removal of
H3K27m3 is biochemical demethylation by a bone
fide demethylase (Fig. 3). In animals, H3K27me3 is
removed by KDM6a and KDM6b, two Jumonji domaincontaining Lys demethylases. In Arabidopsis, RELATIVE OF EARLY FLOWERING6 (REF6), also known as
JUMONJI12 (JMJ12), demethylates H3K27me3 and
H3K27me2, whereas its metazoan counterparts, the
KDM4 proteins (homologous in the JmjN and JmjC
domains), are H3K9 and H3K36 demethylases (Lu
et al., 2011). However, other proteins might be required
for the demethylation of all H3K27me3 targets as there
are at least two close homologs of REF6 in Arabidopsis,
EARLY FLOWERING6 and JMJ13, that could act redundantly with REF6. The reactivation of FLC remains
to be understood at the mechanistic level.
Maintenance
PCG COMPLEXES PLAY A CENTRAL ROLE IN
DEVELOPMENTAL TRANSITIONS
The mark H3K27me3 is generally heritable through
cell division for a stable repression. The PRC2 complex
may directly bind to H3K27me3, most likely through the
WD40 domain of FIE (Xu et al., 2010), thus ensuring a
semiconservative mode of maintaining the PRC2 mark
The transition toward flowering represents one of the
many sharp transitions between different phases of development that mark the plant life cycle. All plant species
alternate a haploid life form (gametophyte) and a diploid
form (sporophyte). The gametophyte produces gametes,
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Epigenetic Control of Developmental Transitions
Figure 3. Possible mechanisms causing H3K27me3 removal. A, Dilution by successive cell divisions: At each DNA replication
cycle, the H3K27me3 mark is lost if not added actively on the newly formed DNA strand. B, Removal in a transcription factordependent manner. For flowering after vernalization, the transcription factor AG binds on the KNU locus, and H3K27me3 marks
are gradually removed in an AG-dependent manner. The precise mechanism of this removal is still unknown. C, Demethylation
by an H3K27me3 demethylase, such as REF6. D, Replacement of the H3 histone that bears the H3K27me3 mark by a variant H3
(H3v) that doesn’t carry the H3K27me3 mark.
which undergo fertilization resulting in a zygote. Zygotic
division initiates a sporophyte that produces meiotic
haploid spores. In flowering plants, the sporophytic life is
divided into further transitions, including, for example,
the differentiation of meristem cells into vegetative organs and the switch between an indeterminate vegetative
meristem to a determinate inflorescence meristem. Here,
we detail how PcG is involved in several phase developmental transitions (Fig. 4).
DEVELOPMENTAL TRANSITION DURING
SEXUAL REPRODUCTION
Gametophyte-to-Sporophyte Transition
In mosses, the gametophytic life is the predominant
vegetative phase, and the sporophyte is a short-lived
structure specialized in meiosis and spore production.
In the moss Physcomitrella patens, mutants were obtained for the homologs of FIE and CLF (Mosquna
et al., 2009; Okano et al., 2009). In the absence of PpFIE
and PpCLF, meristems overproliferate and are unable
to develop leafy gametophytes or reach the reproductive phase. Instead, gametophytes produce proliferating clumps of cells that express sporophytic markers,
showing that PRC2 prevents a precocious transition
from the gametophytic to the sporophytic stage. Similarly in Arabidopsis, mutants for the FIS complex
produce an overproliferating central cell in the gametophyte (Ohad et al., 1996; Chaudhury et al., 1997).
This phenotype was interpreted as a prevention of
fertilization or endosperm development by the FIS
complex. However, in the light of the impact of PRC2
on gametophytic-to-sporophytic transition in mosses,
it is more likely that in Arabidopsis, FIS prevents the
arrest of gametophytic life. Hence, the tissue prolifer-
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Holec and Berger
Figure 4. PcG complexes mediate
transitions from one stage of development to another. PRC2 complexes
have been found to play an essential
role in major transitions from one
phase to another of plant development.
The inner cycle marks the transition
between the gametophytic to the sporophytic phase. Orange arrows mark
PRC2-dependent transitions that take
place during the sporophytic development.
ating from the fis central cell would represent abnormal gametophytic tissue. This suggests an ancestral
role of PRC2 in the control of the transition between
the gametophytic and sporophytic life.
of late endosperm development (Weinhofer et al., 2010).
Hence, PRC2 controls the transition from syncytial to
differentiated cellular endosperm.
Embryo Maturation
Endosperm Maturation
Embryo development requires the function of the
second product of fertilization, the endosperm. Endosperm development is initiated by a series of syncytial
divisions leading to a large multinucleate cell. After a
specific number of synchronous nuclear divisions,
cytokinesis takes place and cellular endosperm is
formed (Berger and Chaudhury, 2009). Seed reserves
accumulate in the cellular endosperm and, depending
on the species, are either retained in the endosperm or
transferred to the embryo. The transition to cellular
endosperm is controlled by PRC2 activity. Endosperms deprived of FIS function hyperproliferate
and never cellularize. The retention of a syncytial
endosperm in fis mutants is confirmed by an abnormal
expression of molecular markers of syncytial endosperm and the absence of expression of genes normally expressed in wild-type cellular endosperm
(Ingouff et al., 2005). This conclusion is further
strengthened by the abundance of H3K27me3 on
genes involved in cell wall synthesis and other markers
When the strict requirement of the FIS complex for
gametophytic development and endosperm is overcome, it is possible to study the function of PRC2 during
plant embryogenesis (Kinoshita et al., 2001; Bouyer
et al., 2011). fie embryos never mature but keep proliferating and eventually produce tissues that resemble
calluses. PRC2 not only prevents the transition between
early seed to dry seed but also represses entire networks
of genes involved in the reproductive transition. Interestingly, fie mutant seedlings are initially indistinguishable from wild-type plants, suggesting that the initial
patterning does not rely on PRC2 but rather does the
maintenance of this pattern (Bouyer et al., 2011).
TRANSITIONS DURING POSTEMBRYONIC LIFE
Transition from Juvenile to Adult Stage
The shoot apical meristem continuously initiates
primordia that exit the stem cell self-renewal program
and engage toward leaf development (Fig. 4). The
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Epigenetic Control of Developmental Transitions
genome-wide distribution of H3K27me3 marks and
the transcriptome were compared between meristematic cells and leaves to gain insight into the function
of PRC2 in tissue-specific differentiation (Lafos et al.,
2011). During wild-type leaf development, H3K27me3
marks are removed at several hundreds of loci. A large
fraction of these loci encode transcription factors,
some of which are already identified as key regulators
of leaf development. Interestingly, many of the transcriptional networks identified are also targeted by
microRNAs, which also become derepressed during
differentiation. For instance, genes involved in the
entire pathway of the phytohormone auxin regulation
are targeted by H3K27me3, including microRNAs
repressing auxin response factors. The mechanism
leading to coordinated removal of the H3K27me3
mark remains unclear.
Vegetative-to-Reproductive Transition
The shoot apical meristem keeps producing leaf
primordia until the transition to flowering. Then, the
meristem becomes determinate and becomes an inflorescence meristem that, in turn, produces floral meristems (Fig. 4). We discussed above the predominant
role of PRC2 in the induction of flowering in response
to vernalization. This role also extends to the control of
meristem determinacy via other major targets of PRC2:
LEAFY (LFY) and the transcription factors AGAMOUS (AG) and KNUCKLES (KNU).
LFY is essential for the transition to an inflorescence
meristem. Its expression is repressed by PRC2 during
embryo development (Kinoshita et al., 2001). The
MADS box transcription factor AG and the zinc finger
domain transcriptional repressor KNU ensure a determinate number of organs is produced by the floral
meristem. Their expression is repressed by H3K27me3
in a highly regulated temporal manner (Sun et al.,
2009). AG expression is initiated first, and AG binds to
the upstream promoter of KNU, which is still repressed by H3K27me3. Gradually, the repressive
mark is removed in a cell cycle in an AG-dependent
manner, allowing the basic transcriptional machinery
to access the KNU locus and induce transcription. This
mechanism provides a delay that is key to ensure that
a proper cell number is produced by the floral meristem before the flower organ differentiation.
CONCLUSION
PcG complexes PRC2 are conserved. However, there
is limited conservation of the activities that read the
H3K27me3 marks they deposit. As shown in animals,
long noncoding RNAs certainly play a role in PRC2
targeting (Zhao et al., 2010), but it remains unclear
whether this is also the case in plants where very
few long noncoding RNAs have been isolated so far.
Several other mechanisms might recruit PRC2 and
explain PRC2 targeting.
Unlike in animals, PRC2 in plants does not appear to
play a major role in patterning but is essential in the
control of developmental phase transitions (Fig. 4).
This implies cycles of maintenance and reprogramming, and the nature of these mechanisms is still not
understood. Certain phases are long lasting (for example, the sporophytic phase in flowering plants) and
contain cascades of more specific transitions (for example, vegetative to inflorescence to floral meristem).
This implies that developmental transitions controlled
by PRC2 become gradually more refined, while they
do not necessarily rely on a cascade of repressive
marks. Understanding resetting mechanisms and how
plants maintain certain marks specific for long-lasting
developmental status while other PRC2 marks are
remodeled during a transition contained within this
period are major challenges of this research field.
ACKNOWLEDGMENTS
We thank Laurent Pieuchot for help with the figures.
Received August 31, 2011; accepted November 11, 2011; published November
15, 2011.
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