Journal Of
of Experimental
20122012
Experimental Botany,
Botany, Vol.
Vol. 63,
63, No. 2,
13,pp.
pp.695–709,
4713–4722,
doi:10.1093/jxb/err313
doi:10.1093/jxb/ers145 Advance Access publication 4 November, 2011
This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH
FLOWERINGPAPER
NEWSLETTER REVIEW
Evolution,
function,
and
regulation
of genomic
imprinting
In
Posidonia
oceanica
cadmium
induces
changes
in DNA in
plant seed development
methylation
and chromatin patterning
Hua Jiang
andAdriana
ClaudiaChiappetta,
Köhler*
Maria
Greco,
Leonardo Bruno and Maria Beatrice Bitonti*
Plant Biology
and Forest
Genetics,
UppsalaofBioCenter,
Swedish University
Agricultural
and LinneandiCenter
Department of Ecology,
University
of Calabria,
Laboratory
Plant Cyto-physiology,
PonteofPietro
Bucci, Sciences
I-87036 Arcavacata
Rende,of
Plant Biology,
Cosenza,
Italy 750 07 Uppsala, Sweden
* To
To whom
whom correspondence
correspondence should
should be
be addressed:
addressed. E-mail:
E-mail: [email protected]
[email protected]
Received 29
May 2011;
Revised
8 July
Accepted
18 August
2011
28 February
2012;
Revised
252011;
April 2012;
Accepted
26 April
2012
Abstract
In
mammals,
cadmium
is widely
considered
as a non-genotoxic
carcinogen
actingalleles
through
methylation-dependent
Genomic
imprinting
is an
epigenetic
phenomenon
whereby genetically
identical
area differentially
expressed
epigenetic
Here, the effects
of Cdimprinting
treatmenthas
on independently
the DNA methylation
are examined
together
with
dependent mechanism.
on their parent-of-origin.
Genomic
evolvedpatten
in flowering
plants and
mammals.
its
effect
on chromatin
reconfiguration
in Posidonia
oceanica. DNA
methylation
level and
were analysed
in
In both
organism
classes,
imprinting occurs
in embryo-nourishing
tissues,
the placenta
andpattern
the endosperm,
respecactively
growing
under short(6 h) and long(2 regulate
d or 4 d) the
termtransfer
and lowof(10
mM) andtohigh
mM) doses
of Cd,
tively, and
it has organs,
been proposed
that imprinted
genes
nutrients
the (50
developing
progeny.
through
a Methylation-Sensitive
Polymorphism
technique
and or
anrepeat
immunocytological
approach,
Many imprinted
genes are located Amplification
in the vicinity of
DNA-methylated
transposon
sequences, implying
that
respectively.
The expression
of one member
the CHROMOMETHYLASE
(CMT)
family, a DNA
methyltransferase,
transposon insertions
are associated
with theofevolution
of imprinted loci. The
antagonistic
action
of DNA methylawas
alsoPolycomb
assessedgroup-mediated
by qRT-PCR. Nuclear
chromatin ultrastructure
was
byoftransmission
electron
tion and
histone methylation
seems important
forinvestigated
the regulation
many imprinted
plant
microscopy.
Cd the
treatment
DNA hypermethylation,
as well
as an up-regulation
of will
CMT,
that de
genes, whereby
positioninduced
of suchaepigenetic
modifications can
determine
whether a gene
be indicating
mainly expressed
novo
methylation
did indeed
Moreover,
a high
dose
of Cd led to
a progressive
heterochromatinization
of
from either
the maternally
or occur.
paternally
inherited
alleles.
Furthermore,
long
non-coding RNAs
seem to play an as
interphase
nuclei and apoptotic
figures
wereof
also
observed
after
long-term
treatment.
The data
that Cd
yet underappreciated
role for the
regulation
imprinted
plant
genes.
Imprinted
expression
of ademonstrate
number of genes
is
perturbs
the
DNA methylation
status
through
the involvement
of a specific
Suchexpression
changes are
conserved
between
monocots and
dicots,
suggesting
that long-term
selectionmethyltransferase.
can maintain imprinted
at
linked
to nuclear chromatin reconfiguration likely to establish a new balance of expressed/repressed chromatin.
some loci.
Overall, the data show an epigenetic basis to the mechanism underlying Cd toxicity in plants.
Key words: Endosperm, evolution, DNA methylation, genomic imprinting, Polycomb group proteins, transposons
Key words: 5-Methylcytosine-antibody, cadmium-stress condition, chromatin reconfiguration, CHROMOMETHYLASE,
DNA-methylation, Methylation- Sensitive Amplification Polymorphism (MSAP), Posidonia oceanica (L.) Delile.
Introduction
Genomic imprinting is an epigenetic phenomenon leading to a
Introduction
change of gene expression dependent on whether the gene was
In
the Mediterranean
coastal
the (Reik
endemic
inherited
from the maternal
or the ecosystem,
paternal parent
and
seagrass
Posidonia
oceanica
(L.)
Delile
plays
a
relevant
role
Walter, 2001). The ‘imprint’ is placed during male or female
by
ensuring primary
production,
water oxygenation
and
gametogenesis
and determines
the differential
expression state
of
provides
niches
for
some
animals,
besides
counteracting
the alleles in post-fertilization tissues. This parent-of-origin specoastal
erosion
through
its widespread
meadows
(Ott,
1980;
cific change
in gene
expression
is not connected
with
a change
Piazzi
et
al.,
1999;
Alcoverro
et
al.,
2001).
There
is
in DNA sequence and does, therefore, represent one form of also
epiconsiderable
evidence
P. oceanica
are function
able to
genetic inheritance
wherethat
heritable
changes plants
in genome
absorb
accumulate
metals
from sediments
(Sanchiz
can occurand
without
a change in
DNA sequence
(Bird, 2007).
As it
et
al.,
1990;
Pergent-Martini,
1998;
Maserti
et
al.,
2005)
thus
is possible that the ‘imprint’ can either activate or repress expresinfluencing
metal
bioavailability
in
the
marine
ecosystem.
sion at a particular locus, to avoid confusion it is required to refer
For
this reason,
seagrass
is widely
considered
to be
to imprinted
genes this
as either
maternally
or paternally
expressed
aimprinted genes.
metal bioindicator species (Maserti et al., 1988; Pergent
et Genomic
al., 1995;
Lafabrieoccurs
et al.,
2007). Cd
is one
of most
imprinting
in flowering
plants
and mammals
widespread
heavy
metals
in
both
terrestrial
and
marine
and is considered to have evolved independently (convergently)
environments.
in both lineages (Feil and Berger, 2007; Köhler and Weinhofer,
2010; for a detailed history on genomic imprinting research see
Although
essential
plant imprinting
growth, inin terrestrial
Köhler
et al.,not
2012).
While for
genomic
mammals
plants,
Cd
is
readily
absorbed
by
roots
into
occurs both in the placenta and embryo as and
well translocated
as in adult tissues
aerial
organs
while,
in
acquatic
plants,
it
is
directly
taken
up
(Frost and Moore, 2010), imprinting in angiosperms occurs preby
leaves.
In
plants,
Cd
absorption
induces
complex
changes
dominantly in the endosperm and in the early embryo, but not in
at
thetissues
genetic,
biochemical
and
physiological
levels which
adult
(Bauer
and Fischer,
2011).
The seed endosperm
can
ultimately
account
for
its
toxicity
(Valle
and
Ulmer,
1972;
be considered a functional analogue of the mammalian placenta
Sanitz
di Toppi
and and
Gabrielli,
Benavides
et al.,
2005;
and serves
to support
nurture1999;
the growing
embryo
(Berger,
Weber
et
al.,
2006;
Liu
et
al.,
2008).
The
most
obvious
2003). It is a triploid tissue derived after fertilization of the
symptom
of Cd
toxicity
is a reduction
plant
growth
to
homodiploid
central
cell with
one spermincell,
whereas
thedue
other
an
inhibition
of
photosynthesis,
respiration,
and
nitrogen
sperm cell will fertilize the egg cell, resulting in the formation of
metabolism,
as (Berger,
well as 2003).
a reduction
and
mineral
a diploid embryo
Modelsin
forwater
genomic
imprinting
uptake
(Ouzonidou
et
al.,
1997;
Perfus-Barbeoch
et
al.,
2000;
in mammals involve the erasure of all imprints in the primorShukla
et
al.,
2003;
Sobkowiak
and
Deckert,
2003).
dial germ cells, followed by the resetting (or re-establishment)
genetic
level,theinmale
bothor animals
and plants,
of At
the the
imprint
in either
female gametes,
whichCd
is
can induce chromosomal aberrations, abnormalities in
© 2011
The Author
[2012]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
ª
The Author(s).
For Permissions,
please article
e-mail:distributed
[email protected]
This
is an Open Access
under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/bync/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
4714 | Genomic imprinting in plants
subsequently maintained post-fertilization in embryonic tissues
as an imprinted gene expression pattern (Feng et al., 2010). As
the endosperm is a terminal tissue which does not genetically
contribute to the next generation, for endosperm imprinted genes
there is no apparent cycle of erasure, resetting, and maintenance
required which would parallel that observed in mammals (Jullien
and Berger, 2009; Bauer and Fischer, 2011).
Genome-wide analysis of imprinting
in plants
Until very recently, fewer than 20 imprinted genes had been
reported in plants (Jullien and Berger, 2009), placing genomic
imprinting in plants as rather an oddity than a relevant phenomenon. The application of genome-wide RNA sequencing
strategies in genomic imprinting research changed that view
and revealed that there are about 100–300 genes regulated by
genomic imprinting in Arabidopsis thaliana, rice, and maize
(Table 1; Gehring et al., 2011; Hsieh et al., 2011; Luo et al.,
2011; McKeown et al., 2011; Waters et al., 2011; Wolff et al.,
2011; Zhang et al., 2011). Three recent studies of imprinting
in A. thaliana applied next generation sequencing to identify
imprinted genes (Hsieh et al., 2011; Wolff et al., 2011; Gehring
et al., 2011). Rather surprisingly though, the overlap of commonly identified imprinted genes was rather low (Köhler et al.,
2012). Apparently, a major challenge to imprinting studies in
plants is posed by the genetically chimeric nature of seed tissues. Seeds are composed of three tissues, namely a uniparentally derived maternal sporophytic seed coat which encases the
two biparentally-derived fertilization products (the embryo and
endosperm). While precise microdissection of the seed into
its three tissue components is a logical approach, followed by
allele-specific transcript level analysis, this can be technically
challenging for small seed species such as A. thaliana. Whereas
in one of the studies whole seeds were analysed and seed coatexpressed genes were removed by filtering using available
microarray expression data (Wolff et al., 2011), in two other
studies the endosperm was manually isolated prior to analysis
(Gehring et al., 2011; Hsieh et al., 2011). However, manual dissection did not eliminate seed coat contamination and extensive
data filtering was required to remove false positive candidates.
Using the same statistical pipeline to analyse these two different datasets (Gehring et al., 2011; Hsieh et al., 2011) tripled
the number of commonly identified imprinted genes (Gehring
et al., 2011), revealing that different statistical methods explain,
in large part, the low number of commonly identified imprinted
genes. However, different filtering strategies are unlikely to be
the only cause for the low overlap among these experiments,
since only a small number of predicted maternally expressed
genes (MEGs) and paternally expressed genes (PEGs) identified by Wolff et al. (2011) were also present in the unfiltered
dataset of Hsieh et al. (2011). This rather suggests that different accession combinations and different developmental
stages resulted in the identification of complementary datasets.
Whereas one experiment analysed early seeds [4 d after pollination (DAP)] derived from reciprocal crosses of Columbia
(Col) and Bur-0 accessions (Wolff et al., 2011), in two other
experiments endosperm was analysed derived from crosses of
Col and Landsberg erecta (Ler) accessions at 7 DAP (Gehring
et al., 2011; Hsieh et al., 2011; Table 1). Expression of many
MEGs and PEGs declines during the later stages of seed development (Wolff et al., 2011), suggesting that part of the data discrepancy can be explained by differences of the analysed seed
stages. In addition, imprinting is accession-dependent, with
some genes only being imprinted in defined accessions. One
possible explanation for this phenomenon is epigenetic natural variation, consistent with the fact that there is a high level
of polymorphic DNA methylation among different accessions
(Vaughn et al., 2007; Zhai et al., 2008; Zhang et al., 2008).
Therefore, the different accession combinations used in two of
the three experiments could also limit the number of commonly
identified imprinted genes.
Genome-wide analysis of imprinting in rice endosperm identified 262 imprinted loci, of which 177 were maternally and 85
paternally expressed (Table 1). About 80% of 67 randomly chosen
Table 1. Summary of genome-wide studies of genomic imprinting in plants MEGs and PEGs correspond to putatively maternally and
paternally expressed genes. ncMELs and ncPELs correspond to putatively non-coding maternally and paternally expressed loci. DAP,
days after pollination. na, not analysed.
Reference
Wolff et al., 2011
Hsieh et al., 2011
Gehring et al., 2011
Waters et al., 2011
Zhang et al., 2011
Luo et al., 2011
Plant species
Arabidopsis
Col, Bur
Arabidopsis
Col, Ler
Arabidopsis
Col, Ler
Maize
B73, Mo17
Maize
B73, Mo17
Rice
Nipponbare, 93-11
Timepoint
Endosperm
Embryo
MEGs
PEGs
ncMELs
ncPELs
MEGs
PEGs
4 DAP
39
27
na
na
na
na
7–8 DAP
116
10
na
na
0
0
6–7 DAP
165
43
na
na
18
0
14 DAP
54
46
na
na
29
9
10 DAP
111
68
25
13
na
na
5–6 DAP
93
72
84
13
1
0
Jiang and Köhler | 4715
loci could be experimentally validated, revealing that the applied
strategy identified imprinted loci at high confidence (Luo et al.,
2011). Previous studies in maize predicted that parentally biased
expression affects a large number of genes, ranging between
2–8% of all genes (Guo et al., 2003; Gutierrez-Marcos et al.,
2003). However, only about one-quarter of these genes were predicted to have parental-specific expression (Gutierrez-Marcos
et al., 2003). These predictions have been largely confirmed by
two recent genome-wide imprinting studies in maize that identified 100 and 179 imprinted genes, respectively, (Waters et al.,
2011; Zhang et al., 2011) with 55 genes being commonly identified in both studies. Similar to A. thaliana, imprinted expression of certain genes depends on developmental seed stages
(Danilevskaya et al., 2003; Gutierrez-Marcos et al., 2004; Zhang
et al., 2011), probably accounting for the different number of
identified imprinted genes in both studies that analysed 10 DAP
and 14 DAP endosperm, respectively (Zhang et al., 2011; Waters
et al., 2011). However, different filtering strategies were also
applied in both studies and a higher number of overlapping
genes might be identified by applying the same filtering strategy
to both datasets.
For more than ten genes, imprinting is conserved in at least
two species when comparing datasets obtained for maize and
rice, maize, and Arabidopsis (Waters et al., 2011; Zhang et al.,
2011), and Arabidopsis and rice (Köhler et al., 2012), with three
genes being commonly imprinted in all three species. Albeit
there have been fewer PEGs than MEGs identified in most studies, the three conserved imprinted genes show preferential paternal expression in all three species (At4G11400, Os10G30944,
GRMZM2G365731 encode for an ARID/BRIGHT DNA-binding
domain protein; At1G57800, Os04G22240, AC191534.3 encode
for VARIANT IN METHYLATION5; At1G48910, Os12g08780,
GRMZM2G091819 encode for YUCCA10), suggesting that
imprinted expression of these three genes confers a selective
advantage and has been maintained after the split of monocots
and dicots. Overall, the number of genes that are commonly
imprinted in at least two species is rather low; however, given
the rather low total number of imprinted genes the overlap is
highly significant. It is also likely that the number of conserved
imprinted genes will steadily increase, as only about one-third
to one-half of all genes has been analysed thus far. The analyses
have been limited by the number of available single nucleotide
polymorphisms (SNPs) between tested accessions or strains,
therefore, new analyses using different accession/strain combinations are likely to increase the number of imprinted genes.
Regulation of genomic imprinting in the
endosperm
To achieve parent-of-origin-specific gene expression, maternal
and paternal alleles have to acquire an epigenetic modification
(which constitutes the ‘imprint’). This modification is likely to
be established before maternal and paternal chromosomes are
united within the same nucleus, thus either during gametogenesis
or shortly after fertilization. The imprint has to be stably inherited over several mitotic divisions, but should be erased during gametogenesis, in order to allow appropriate parent-specific
imprints to be established in the gametes. As a consequence of
these imprints, the expression status of the alleles will change in
a parent-of-origin specific manner (Ferguson-Smith, 2011).
Regulation of imprinted genes by DNA
methylation
DNA methylation has been widely recognized as an epigenetic
mark distinguishing maternal and paternal alleles in mammals
(Ferguson-Smith, 2011) as well as in plants (Kinoshita et al.,
2004; Gehring et al., 2006; Gutierrez-Marcos et al., 2006; Jullien
et al., 2006b; Makarevich et al., 2008). Asymmetric DNA methylation of maternal and paternal alleles is achieved by DNA
demethylation in the central cell of the female gametophyte.
DNA demethylation relies on the 5-methylcytosine excising
activity of the DNA glycosylase DEMETER (DME) (Kinoshita
et al., 2004; Gehring et al., 2006) as well as on repression of the
maintenance methyltransferase MET1 in the central cell of the
female gametophyte and in the endosperm (Jullien et al., 2008;
Hsieh et al., 2011). DME is expressed in the central cell of the
female gametophyte (Choi et al., 2002) but not in sperm cells
(Schoft et al., 2011), leading to specific removal of DNA methylation marks on the maternally inherited genome. DNA hypomethylation in the endosperm is not confined to specific loci but
is a genome-wide phenomenon affecting mainly transposon and
repeat sequences, with virtually all CG sequences being methylated in the embryo having reduced methylation levels in the
endosperm (Gehring et al., 2009; Hsieh et al., 2009). Therefore,
imprinted gene expression can arise whenever transposon insertions or local sequence duplications occur close to gene regulatory sequences. DNA methylation will be recruited to silence
these potentially damaging DNA elements and will cause silencing of neighbouring genes. However, as a consequence of these
elements becoming hypomethylated in the central cell of the
female gametophyte, neighbouring genes will become active
when maternally inherited, but remain silenced when paternally
inherited. This mechanism implies that genomic imprinting in
plants is largely a consequence of differential DNA methylation established in the central cell. Genome-wide analyses of
imprinted genes in A. thaliana revealed indeed that a subset
of MEGs are imprinted by DNA methylation, and that activation
of the maternal MEG alleles requires DME-mediated DNA demethylation (Gehring et al., 2009; Hsieh et al., 2009; Wolff et al.,
2011). As a corollary, those MEGs are silenced by DNA methylation in vegetative tissues and specifically expressed in the
endosperm upon loss of DNA methylation (Hsieh et al., 2011;
Wolff et al., 2011).
Regulation of imprinted genes by
Polycomb group proteins
Differentially DNA-methylated regions are not restricted
to the vicinity of MEGs, but have as well been identified in
PEGs (Waters et al., 2011; Zhang et al., 2011), suggesting that
other repressive mechanisms account for silencing of maternally inherited PEGs alleles. One major repressive mechanism
4716 | Genomic imprinting in plants
involved in imprinted expression of a subset of genes relies
on Polycomb group (PcG) proteins. PcG proteins are evolutionary conserved master regulators of cell identity that act in
multimeric complexes repressing the transcription of target
genes (Schuettengruber and Cavalli, 2009). There are two main
PcG complexes, the Polycomb Repressive Complex 2 (PRC2)
that catalyses the trimethylation of histone H3 on lysine 27
(H3K27me3), and PRC1, which binds to this mark and catalyses ubiquitination of histone H2A at lysine 119 (Schuettengruber
and Cavalli, 2009). Plants contain multiple genes encoding
homologues of PRC2 subunits that have different roles during
vegetative and reproductive plant development (Hennig and
Derkacheva, 2009). The FERTILIZATION INDEPENDENT
SEED (FIS) PRC2 complex [comprised of the subunits MEDEA
(MEA), FERTILIZATION INDEPENDENT SEED2 (FIS2),
FERTILIZATION INDEPENDENT ENDOSPERM (FIE), and
MULTICOPY SUPPRESSOR OF IRA1 (MSI1)] is active in
the central cell of the female gametophyte and in the endosperm
and is essential for normal endosperm development (Hennig
and Derkacheva, 2009). DNA hypomethylation creates target
sites for repressive PcG proteins in the endosperm (Weinhofer
et al., 2010), suggesting that, at defined loci, repression of the
maternally inherited alleles is mediated by epigenetic imprints
established by PcG proteins. In agreement with this notion, many
PEGs are targeted by the FIS PRC2 complex in the endosperm
and deregulated upon loss of FIS PRC2 function (Hsieh et al.,
2011; Wolff et al., 2011). Also a subset of MEGs is regulated
by FIS PRC2. However, whereas for some MEGs imprinted
expression depends on FIS PRC2 function (Baroux et al., 2006;
Gehring et al., 2006; Jullien et al., 2006a; Hsieh et al., 2011),
many MEGs are targeted by the FIS PRC2 complex which does
not cause complete silencing but merely dampening of maternal
MEG allele expression (Fig. 1A, B). This obviously raises the
question why maternal alleles of PEGs are completely silenced
by the FIS PRC2 complex, whereas maternal MEG alleles remain
expressed although being targeted by FIS PRC2. Silencing of the
maternal alleles of the PEG PHERES1 (PHE1) from A. thaliana
depends on demethylation of a distantly located repeat region
Fig. 1. Models explaining different regulatory modes of maternally (A, B, C) and paternally (C, D, F) expressed imprinted genes.
(A) Differential methylation of maternal and paternal alleles is established in the gametes by DNA hypomethylation of transposable
elements located in the vicinity of genes. The FIS PRC2 complex binds to hypomethylated regions and modulates gene expression, but
does not cause complete silencing. Differential DNA methylation and repression of the paternal allele is maintained in the endosperm.
(B) Differential methylation of the maternal and paternal alleles is established in the gametes by DNA hypomethylation of transposable
elements which are distantly located relative to genes. The FIS PRC2 complex binds to hypomethylated regions as well as unmethylated
regions and modulates gene expression, but does not cause complete silencing. Repression of the paternal allele might be caused
by the co-occurrence of DNA methylation as well as FIS PRC2-mediated epigenetic modifications. (C) Long non-coding RNAs (lnc
RNAs) are specifically transcribed from the paternal allele, leading to the recruitment of FIS PRC2 and silencing of the paternal allele.
(D) Differential methylation of maternal and paternal alleles is established in the gametes by DNA hypomethylation of transposable
elements that flank genes in distant locations from the 5' and 3' ends of the genes. The FIS PRC2 complex binds to hypomethylated
regions and mediates silencing of maternal alleles by applying epigenetic modifications. Methylated transposable elements prevent FIS
PRC2 binding to the paternal allele, preventing paternal allele repression. (E) It is possible that distantly located FIS PRC2 complexes
interact with each other causing loop formation and enhancement of maternal allele silencing. (F) Long non-coding RNAs (lnc RNAs) are
specifically transcribed from the maternal alleles, leading to the recruitment of FIS PRC2 and silencing of the maternal alleles.
Jiang and Köhler | 4717
at the 3' end of the PHE1 locus as well as on binding of the
FIS PRC2 complex to the PHE1 promoter region, suggesting
long-range interactions between the repeat region and PcG proteins (Makarevich et al., 2008; Villar et al., 2009). Demethylation
of the repeat region might expose a FIS PRC2 binding site that
allows interaction of promoter and repeat bound PRC2 complexes
(Fig. 1D, E). Long-range interactions of PcG protein binding
sites occur frequently in Drosophila (Tolhuis et al., 2011) and
are essential for silencing of some fly loci (Cleard et al., 2006;
Lanzuolo et al., 2007), suggesting that similar mechanisms operate in plants and are essential for the efficient silencing of the
maternal PHE1 alleles. PHE1 seems not be an exceptional case,
as many PEG loci in A. thaliana become activated upon the loss
of FIS PRC2 function, whereas expression of the paternal alleles
at PEG loci depends on DNA methylation (Hsieh et al., 2011).
Based on these findings it seems likely that repression of maternal alleles at many PEG loci depends on FIS PRC2 function,
whereas binding of FIS PRC2 to the paternal alleles at PEG loci
is prevented by DNA methylation. DNA methylation has indeed
been detected in the vicinity of many PEG loci in A. thaliana
(Gehring et al., 2009; Wolff et al., 2011), however, the presence
of DMRs seems rather rare in maize (Waters et al., 2011; Zhang
et al., 2011), suggesting that genomic imprinting does not solely
rely on DNA methylation-dependent mechanisms.
Imprinted expression of non-coding RNAs
in the endosperm
Genome-wide imprinting analyses revealed that, in plants, similar to mammals, many imprinted transcripts are derived from
intergenic regions or introns (Royo and Cavaille, 2008; Luo
et al., 2011; Zhang et al., 2011). In maize and rice endosperm,
38–97 imprinted long non-coding RNAs (lnc RNAs) have been
identified, respectively (Luo et al., 2011; Zhang et al., 2011).
A detailed characterization of maize imprinted lncRNAs revealed
that all of them lacked the conserved structure of snoRNAs and
the typical hairpin structure of miRNAs. These RNAs have an
average length of about 500 bp, ranging from less than 100 bp
to more than 1.5 kb. Importantly, four of the identified maternally expressed imprinted lncRNAs in maize are transcribed
from within four PEGs, suggesting that they play a similar role
in imprinted gene expression as lncRNAs in mammals (Santoro
and Barlow, 2011). One possible scenario is that lncRNAs recruit
PRC2 complexes, causing allele-specific silencing (Fig. 1C, F).
In mammals, the importance of lncRNAs for the recruitment
of PcG proteins is well recognized (Beisel and Paro, 2011) and
imprinted expression of the Kcnq1 gene cluster depends on
the Kcnq1ot1 lncRNA that probably recruits PRC2 in cis (Wu
and Bernstein, 2008). There is also precedence in A. thaliana
for lncRNAs being required for PRC2 recruitment. Thus, the
lncRNA COLDAIR mediates vernalization-dependent epigenetic
repression of FLC by recruitment of a PRC2 (Heo and Sung,
2011). Whether and to what extent lncRNAs play a role for
imprinted gene expression remains to be investigated.
Aside from a limited number of imprinted lncRNAs, there have
been more than 100 000 different small interfering RNAs (siRNAs) of maternal origin detected in A. thaliana seeds. Formation
of maternal-specific siRNAs depends on the plant-specific RNA
polymerase, Pol IV that preferentially generates transcripts
from methylated or heterochromatic DNA. These transcripts are
converted to double stranded RNA by RDR2 (RNA-dependent
RNA Polymerase 2) and further processed into 24-nt-long siRNAs by DCL3 (DICER-LIKE 3). The 24-nt siRNAs bound by
AGO4 guide the de novo methyltransferase DRM2 (DOMAINS
REARRANGED METHYLTRANSFERSE 2) to cytosines in
all sequence contexts (Law and Jacobsen, 2010). Global hypomethylation caused by repression of MET1 and activity of DME
(Jullien et al., 2008; Gehring et al., 2009; Hsieh et al., 2009,
2011) is expected to cause a boost of 24-nt siRNAs mainly
directed against repeat sequences and transposable elements.
Such siRNAs could, in turn, generate a wave of de novo DNA
methylation, explaining strongly increased CHH levels in the
endosperm of A. thaliana compared with vegetative tissues
(Hsieh et al., 2009). Alternatively, it is also possible that siRNAs
might guide DNA demethylation, similar to a proposed mechanism whereby siRNAs interact with ROS3 (REPRESSOR OF
SILENCING 3) (Zheng et al., 2008), which acts in the DNA
demethylation pathway and probably guides the DME homologue ROS1 to target loci (Zheng et al., 2008). Contrary to these
expectations though, formation of maternal-specific siRNAs
seems not to depend on DNA demethylation in the endosperm
(Mosher et al., 2011), raising the question by which mechanism
maternal specific RNAs are formed. Also elimination of siRNAs
by mutations in NRPD1A does not affect endosperm or seed
development, raising the question about the possible functional
role of these RNAs.
Genomic imprinting in the embryo
In flowering plants, parent-of-origin specific gene expression has
long been considered a phenomenon restricted to the ephemeral
endosperm and, therefore, mechanisms required for the resetting
of epigenetic marks would not be required. With the identification
of the imprinted maize gene mee1 this dogma had to be revised
(Jahnke and Scholten, 2009). Mee1 is imprinted in both the
embryo and endosperm and parent-of origin-specific expression
correlates with differential allelic methylation. Maternal mee1
activation in the endosperm is associated with de-methylation
of maternal alleles. Mee1 is methylated in the egg cell, but the
maternal allele becomes rapidly de-methylated after fertilization,
establishing distinct methylation profiles on maternal and paternal mee1 alleles in the embryo. However, differential methylation
is only transient and re-methylation of the maternal allele occurs
subsequently during embryogenesis. Genome-wide studies of
genomic imprinting in different plant species revealed that mee1
is not an exceptional case, but that there is a substantial number
of genes being expressed by parent-of-origin-specific mechanisms in plant embryos (Luo et al., 2011; Waters et al., 2011;
Nodine and Bartel, 2012). In Arabidopsis thaliana early embryos
(about 2-3 DAP) more than 100 transcripts have been identified
that are specifically derived either from maternal or paternal
parents (Nodine and Bartel, 2012). In maize, 38 parent-specific
transcripts were identified that, however, are also imprinted in
the endosperm (Waters et al., 2011; Table 1). Similarly, one
4718 | Genomic imprinting in plants
Fig. 2. Allele-specific siRNAs might cause parent-of-origin
specific gene expression in the embryo. Maternal-specific siRNAs
generated from hypomethylated regions in the endosperm
might move to the embryo and guide ROS1-mediated DNA
demethylation of specific regions in the embryo. Allele-specificity
could be a consequence of sequence specific siRNAs recognizing
only the maternal allele.
imprinted gene identified in rice embryos is also imprinted in the
endosperm (Luo et al., 2011). It is therefore tempting to speculate that a similar mechanism causing localized hypomethylation
in the endosperm by siRNA-mediated recruiting of DME is also
responsible for the localized de-methylation of specific regions in
the embryo. If this process is dependent on maternally produced
siRNAs, allele-specific de-methylation could be a consequence
of strain-specific polymorphisms that give rise to siRNAs which
specifically only match to the maternally inherited allele in the
embryo (Fig. 2). Whether there are strain-specific differences
for those genes that have a parent-of-origin-specific expression
in the embryo remains to be investigated. Alternatively, it has
been suggested that transcripts of imprinted genes in the embryo
are derived from the endosperm. It is possible that they are a
consequence of remaining endosperm contamination, or that
transcripts move from the endosperm to the embryo (Gehring
et al., 2011; Waters et al., 2011). However, this possibility is difficult to reconcile with differential DNA methylation of maternal
and paternal alleles reported for the mee1 locus (Jahnke et al.,
2009). Therefore, to reach a final conclusion on the incidence
and mechanism of genomic imprinting in the embryo requires
further investigations. Nevertheless, parent-of-origin-specific
transcripts have not been detected in later stage embryos (about
6–7 DAP) (Gehring et al., 2011; Hsieh et al., 2011), suggesting
that imprinting in the embryo is not a long-lasting phenomenon.
In agreement with this view, allele-specific expression analysis
in 7-d-old seedlings did not detect any evidence for imprinting
effects (Zhang and Borevitz, 2009).
Clustering of imprinted genes
The majority of imprinted genes in mammals is located in clusters and is co-ordinately regulated by imprinting control regions
(ICRs) (Barlow, 2011). Whether there are imprinted gene clusters in plants similar to those in mammals is still controversial
and no common ICRs for different imprinted genes have been
identified yet (Gehring et al., 2011; Luo et al., 2011; Wolff et al.,
2011; Zhang et al., 2011). By applying similar standards to those
in animals, several putative imprinted genes in plants are located
in clusters; however, the extent of imprinted gene clusters in
plants remains small compared with mammals (Barlow, 2011).
Maize imprinted genes are located in clusters containing at least
two imprinted genes within a region of 1 Mb (Zhang et al., 2011).
One-third of putative maize-imprinted genes fall into 33 clusters
and, by applying similar criteria, there are 62 clusters in A. thaliana and 55 clusters in rice containing two imprinted genes within
54 kb and 182 kb, respectively. By applying more stringent criteria, about 10 gene clusters containing two to three genes were
identified in A. thaliana, with most of these clusters containing
either homologous MEGs or PEGs, or non-imprinted homologues of MEGs and PEGs (Gehring et al., 2011; Wolff et al.,
2011). These results implicate local sequence duplications as a
driving force for the formation of imprinted genes. In agreement
with this view, there is an increased frequency of A. thaliana
MEGs and PEGs having close homologues in comparison to the
genome-wide frequency (Wolff et al., 2011).
Function of imprinted genes in seed
development
Among those imprinted genes that are conserved between
monocots and dicots are many genes with functional roles in
chromatin modification, for example, histone-lysine methyltransferases targeting histone H3 on lysine 9, Argonaute proteins, the 5-methylcytosine binding protein VIM5, and the
chromatin remodelling factor PICKLE RELATED 2 (Gehring
et al., 2011; Hsieh et al., 2011; Luo et al., 2011; Waters et al.,
2011; Wolff et al., 2011; Zhang et al., 2011). The PcG repressive
pathway is also controlled by genomic imprinting in monocots
as well as in dicots, with the FIS PcG genes MEA and FIS2 being
imprinted in A. thaliana, MEZ1 being imprinted in maize (Haun
et al., 2007), and FIE1 being imprinted in rice as well as in maize
(Kinoshita et al., 1999; Vielle-Calzada et al., 1999; Luo et al.,
2000, 2009; Danilevskaya et al., 2003). Genes involved in the
regulation of hormone biosynthesis and signalling are strongly
overrepresented among imprinted genes in A. thaliana (Gehring
et al., 2011; Hsieh et al., 2011) and partially conserved in monocots (Luo et al., 2011; Waters et al., 2011; Zhang et al., 2011),
suggesting an as yet unappreciated control of hormone signalling in the endosperm by imprinted genes. Among the known
imprinted genes in A. thaliana there is an overrepresentation of
type I MADS-box transcription factors that directly or indirectly
interact with a negative regulator of endosperm cellularization,
AGAMOUS-LIKE 62 (AGL62) (Kang et al., 2008; Hsieh et al.,
2011; Wolff et al., 2011). The timing of endosperm cellularization is likely to determine final seed size (Scott et al., 1998;
Garcia et al., 2003), suggesting that imprinted type I MADS-box
transcription factors regulate seed size by regulating the activity
of AGL62. AGL transcription factors have not been identified
in genome-wide surveys of imprinted genes in rice (Luo et al.,
Jiang and Köhler | 4719
2011) or maize (Waters et al., 2011; Zhang et al., 2011), implying different control mechanisms underlying endosperm cellularization in monocots and dicots. Albeit theoretical predictions
implicated a predominant functional role of imprinted genes
in nutrient allocation control (see discussion below), thus far,
the evidence for such a functional role has been rather scarce
(Köhler et al., 2012). Recent results revealing that the maternally expressed imprinted gene Meg1 from maize is required for
the formation of endosperm nutrient transfer cells and for the
regulation of maternal nutrient uptake and partitioning (Costa
et al., 2012) are, therefore, a substantial advance for our understanding of imprinted genes and their functional role during seed
development.
Evolution of imprinted genes in plants
About one third of imprinted genes identified in A. thaliana
are flanked by transposable elements or repeat sequences that
undergo extensive demethylation in the endosperm, suggesting
that imprinting may have arisen as a by-product of a silencing
mechanism targeting invading foreign DNA (Gehring et al.,
2009, 2011; Wolff et al., 2011). Transposon insertions that
occur close to gene regulatory regions will recruit DNA methylation and will potentially cause silencing of the affected gene.
However, due to DME-mediated DNA de-methylation in the
endosperm, this gene will remain expressed in the endosperm
and can adopt an imprinted expression (Gehring et al., 2009;
Hsieh et al., 2009). As a consequence of DNA de-methylation,
small RNAs will be generated that could enforce the silencing of transposable elements in the embryo, suggesting that
genomic imprinting in the endosperm might be a side-effect
of a mechanism destined to silence invading foreign DNA in
the embryo (Hsieh et al., 2009). A similar hypothesis has been
put forward to explain the evolution of genomic imprinting in
mammals. According to the host defence hypothesis, genomic
imprinting in mammals evolved from existing mechanisms
destined to silence foreign DNA elements (Barlow, 1993;
Yoder et al., 1997) and substantial supportive evidence for this
hypothesis has been obtained (Suzuki et al., 2007; Pask et al.,
2009). However, in maize, only about one-fifth of the identified imprinted genes are flanked or contained intragenic DMRs
(Waters et al., 2011; Zhang et al., 2011), seemingly posing a
contradiction to the proposed role of transposable elements
in driving the evolution of genomic imprinting by recruiting
DNA methylation. Yet both methylation analyses in maize
are limited to a small portion of genome, rendering premature a conclusion about the role of DMRs in maize genomic
imprinting. Furthermore, it is currently not known at which
distance a DMR can impact on imprinted gene expression. For
the imprinted gene PHE1, a DMR located about 1.3 kb downstream of the stop codon is required for imprinting regulation
(Villar et al., 2009), revealing a regulatory impact of differentially methylated regions even when located at a substantial
distance from the imprinted gene. Hence, a general conclusion
about the requirement of transposons and DMRs for imprinted
gene expression requires thorough functional testing of these
elements for their impact on imprinted gene expression.
The ‘parental conflict’ (Haig and Westoby, 1989) or ‘kinship’
theory (Trivers and Bart, 1999) provides another explanation for
the evolution of genomic imprinting by proposing that imprinting arose as a consequence of an intragenomic conflict over the
distribution of resources from the mother to the offspring. As a
consequence, in an outbreeding species, paternally active genes
that maximize the transfer of nutrients to the developing embryo
have a selective advantage. Conversely, maternally active genes
will have a selective advantage if they protect the interests of the
mother against the demands of the embryo by suppressing growth.
Such maternally expressed and paternally expressed imprinted
genes could, therefore, be subject to antagonistic co-evolution
(Spillane et al., 2007; O’Connell et al., 2010). In agreement with
the predictions of the parental conflict theory, imprinting occurs
in placental mammals and flowering plants, both contributing
maternal resources to the progeny and many imprinted genes in
mammals affect both the demand and supply of nutrients across
the placenta (Reik et al., 2003; Feil and Berger, 2007). In flowering plants, imprinting predominantly occurs in the endosperm,
which (similar to the mammalian placenta) constitutes a separate
organ dedicated to nourish the developing embryo. Although our
knowledge of the functional roles of most imprinted plant genes
is still scarce, at least some of the known imprinted genes affect
endosperm growth (Chaudhury et al., 1997; Kiyosue et al., 1999,
1999; Vielle-Calzada et al., 1999; Tiwari et al., 2008; Costa
et al., 2012).
Not easily to reconcile with the kinship theory is the strong
overabundance of maternally expressed genes A. thaliana as
well as in rice (Gehring et al., 2011; Hsieh et al., 2011; Luo
et al., 2011; Wolff et al., 2011). It rather lends support to the
‘coadaptation imprinting hypothesis’, which proposes that
genomic imprinting is a consequence of natural selection for
increased offspring fitness, by enhancing the genetic integration of co-adapted offspring and maternal traits (Bateson, 1994;
Wolf and Hager, 2006). The coadaptation imprinting hypothesis
predicts maternal-specific expression at loci affecting traits that
are vital at the interface of the maternal–offspring interaction.
The requirement of the maternally expressed imprinted gene
Meg1 from maize for the formation of endosperm nutrient transfer cells adds substantial support for this theory (Costa et al.,
2012). Importantly, the coadaptation hypothesis also provides
a rationale for the maintenance of imprinted genes in mainly
self-fertilizing species such as A. thaliana and rice, where any
extent of genetic conflict is predicted to be low. Interestingly, in
the outcrossing species, maize, about twice as many PEGs than
MEGs have been identified (Zhang et al., 2011), suggesting that
PEGs evolve as a consequence of genetic conflict, whereas MEGs
are rather a consequence of coadaptation between mother and
offspring. However, the maintenance of genomic imprinting in
self-fertilizing species might also be an evolutionary remnant of
their recent outcrossing past, dating back only about 9000 years
in rice (Li et al., 2006; Londo et al., 2006) and 400000 years in
A. thaliana (Bechsgaard et al., 2004).
In summary, a combination of different hypotheses, including the ‘defense hypothesis’ as well as ‘kinship and coadaptation hypotheses’, provide a theoretical framework to explain the
evolutionary origin of genomic imprinting in plants; whereas
the first hypothesis explains how imprinting may originate,
4720 | Genomic imprinting in plants
the latter two explain how imprinting can be manifested and
maintained.
Future direction
Next generation sequencing technology considerably advanced
our understanding of genomic imprinting by expanding the list
of genes affected by this phenomenon in A. thaliana, rice, and
maize. Importantly, several of the identified genes are imprinted
in both monocots and dicots, which is suggestive of a selective advantage of imprinting for seed development. To identify
the biological functions of imprinted genes and to analyse the
consequences of the imprinted nature of their expression (e.g.
by inducing biallelic expression of these genes) will form key
research questions for the near future. Genome-wide studies
of imprinted genes underpin the importance of transposable
elements for imprinting evolution. However, the underlying
evolutionary and biological processes that maintain imprinted
gene expression remain to be fully resolved. Insights into this
important question are likely to be gained by genomic analysis of imprinted genes in outcrossing relatives of A. thaliana.
Furthermore, comparison of imprinted genes across different
species will allow the identification of conserved imprinting elements and will help to refine current ideas on the mechanisms
underlying imprinted gene expression. Modern sequencing technology has already tremendously expanded our understanding of
genomic imprinting in plants. Applying the available and emerging tools to other plant species will allow the generation and testing of new hypotheses on how males and females differentially
control offspring fate and seed size via the enigmatic epigenetic
phenomenon of genomic imprinting.
Acknowledgement
Beisel C, Paro R. 2011. Silencing chromatin: comparing modes and
mechanisms. Nature Reviews Genetics 12, 123–135.
Berger F. 2003. Endosperm: the crossroad of seed development.
Current Opinions in Plant Biology 6, 42–50.
Bird A. 2007. Perceptions of epigenetics. Nature 447, 396–398.
Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES,
Peacock WJ. 1997. Fertilization-independent seed development
in Arabidopsis thaliana. Proceedings of the National Academy of
Sciences, USA 94, 4223–4228.
Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ,
Goldberg RB, Jacobsen SE, Fischer RL. 2002. DEMETER, a DNA
glycosylase domain protein, is required for endosperm gene imprinting
and seed viability in Arabidopsis. Cell 110, 33–42.
Cleard F, Moshkin Y, Karch F, Maeda RK. 2006. Probing
long-distance regulatory interactions in the Drosophila melanogaster
bithorax complex using Dam identification. Nature Reviews Genetics
38, 931–935.
Costa LM, Yuan J, Rouster J, Paul W, Dickinson H,
Gutierrez-Marcos JF. 2012. Maternal control of nutrient allocation in
plant seeds by genomic imprinting. Current Biology 22, 160–165.
Danilevskaya ON, Hermon P, Hantke S, Muszynski MG,
Kollipara K, Ananiev EV. 2003. Duplicated fie genes in maize:
expression pattern and imprinting suggest distinct functions. The Plant
Cell 15, 425–438.
Feil R, Berger F. 2007. Convergent evolution of genomic imprinting in
plants and mammals. Trends in Genetics 23, 192–199.
Feng S, Jacobsen SE, Reik W. 2010. Epigenetic reprogramming in
plant and animal development. Science 330, 622–627.
Ferguson-Smith AC. 2011. Genomic imprinting: the emergence of
an epigenetic paradigm. Nature Reviews Genetics 12, 565–575.
Frost JM, Moore GE. 2010. The importance of imprinting in the
human placenta. PLoS Genetics 6, e1001015.
This research was supported by grant ERC-2011-StG_20101109
to CK.
Garcia D, Saingery V, Chambrier P, Mayer U, Jürgens G,
Berger F. 2003. Arabidopsis haiku mutants reveal new controls of
seed size by endosperm. Plant Physiology 131, 1661–1670.
References
Gehring M, Bubb KL, Henikoff S. 2009. Extensive demethylation
of repetitive elements during seed development underlies gene
imprinting. Science 324, 1447–1451.
Barlow DP. 1993. Methylation and imprinting: from host defense to
gene regulation? Science 260, 309–310.
Barlow DP. 2011. Genomic imprinting: a mammalian epigenetic
discovery model. Annual Revue of Genetics 45, 379–403.
Baroux C, Gagliardini V, Page DR, Grossniklaus U. 2006.
Dynamic regulatory interactions of Polycomb group genes:
MEDEA autoregulation is required for imprinted gene expression in
Arabidopsis. Genes and Develpment 20, 1081–1086.
Bateson P. 1994. The dynamics of parent–offspring relationships in
mammals. Trends in Ecology and Evolution 9, 399–403.
Bauer MJ, Fischer RL. 2011. Genome demethylation and imprinting
in the endosperm. Current Opinions in Plant Biology 14, 162–167.
Bechsgaard J, Bataillon T, Schierup MH. 2004. Uneven
segregation of sporophytic self-incompatibility alleles in Arabidopsis
lyrata. Journal of Evolutonary Biology 17, 554–561.
Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y,
Harada JJ, Goldberg RB, Fischer RL. 2006. DEMETER DNA
glycosylase establishes MEDEA Polycomb gene self-imprinting by
allele-specific demethylation. Cell 124, 495–506.
Gehring M, Missirian V, Henikoff S. 2011. Genomic analysis of
parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS
One 6, e23687.
Guo M, Rupe MA, Danilevskaya ON, Yang X, Hu Z. 2003.
Genome-wide mRNA profiling reveals heterochronic allelic variation
and a new imprinted gene in hybrid maize endosperm. The Plant
Journal 36, 30–44.
Gutierrez-Marcos JF, Pennington PD, Costa ML, Dickinson HG.
2003. Imprinting in the endosperm: a possible role in preventing wide
hybridization. Philosophical Transactions of the Royal Society London,
Biological Sciences 358, 1105–1111.
Jiang and Köhler | 4721
Gutierrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B,
O’Sullivan DM, Wormald M, Perez P, Dickinson HG. 2004.
Maternally expressed gene1 is a novel maize endosperm transfer
cell-specific gene with a maternal parent-of-origin pattern of
expression. The Plant Cell 16, 1288–1301.
Köhler C, Weinhofer I. 2010. Mechanisms and evolution of genomic
imprinting in plants. Heredity 105, 57–63.
Gutierrez-Marcos JF, Costa LM, Dal Pra M, Scholten S, Kranz E,
Perez P, Dickinson HG. 2006. Epigenetic asymmetry of imprinted
genes in plant gametes. Nature Reviews Genetics 38, 876–878.
Lanzuolo C, Roure V, Dekker J, Bantignies F, Orlando V. 2007.
Polycomb response elements mediate the formation of chromosome
higher-order structures in the bithorax complex. Nature Cell Biology 9,
1167–1174.
Haig D, Westoby M. 1989. Paren-specific gene expression and the
triploid endosperm. American Naturalist 134, 147–155.
Haun WJ, Laoueille-Duprat S, O’Connell MJ, Spillane C,
Grossniklaus U, Phillips AR, Kaeppler SM, Springer NM. 2007.
Genomic imprinting, methylation and molecular evolution of maize
Enhancer of zeste (Mez) homologs. The Plant Journal 49, 325–337.
Hennig L, Derkacheva M. 2009. Diversity of Polycomb group
complexes in plants: same rules, different players? Trends in Genetics
25, 414–423.
Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing
by a long intronic noncoding RNA. Science 331, 76–79.
Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L,
Fischer RL, Zilberman D. 2009. Genome-wide demethylation of
Arabidopsis endosperm. Science 324, 1451–1454.
Hsieh TF, Shin J, Uzawa R, et al. 2011. Regulation of imprinted
gene expression in Arabidopsis endosperm. Proceedings of the
National Academy of Sciences, USA 108, 1755–1762.
Jahnke S, Scholten S. 2009. Epigenetic resetting of a gene
imprinted in plant embryos. Current Biology 19, 1677–1681.
Jullien PE, Berger F. 2009. Gamete-specific epigenetic mechanisms
shape genomic imprinting. Current Opinions in Plant Biology 12,
637–642.
Jullien PE, Katz A, Oliva M, Ohad N, Berger F. 2006a. Polycomb
group complexes self-regulate imprinting of the Polycomb group gene
MEDEA in Arabidopsis. Current Biology 16, 486–492.
Jullien PE, Kinoshita T, Ohad N, Berger F. 2006b. Maintenance
of DNA methylation during the Arabidopsis life cycle is essential for
parental imprinting. The Plant Cell 18, 1360–1372.
Jullien PE, Mosquna A, Ingouff M, Sakata T, Ohad N, Berger F.
2008. Retinoblastoma and its binding partner MSI1 control imprinting
in Arabidopsis. PLoS Biology 6, e194.
Kang IH, Steffen JG, Portereiko MF, Lloyd A, Drews GN. 2008.
The AGL62 MADS domain protein regulates cellularization during
endosperm development in Arabidopsis. The Plant Cell 20, 635–647.
Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE,
Fischer RL, Kakutani T. 2004. One-way control of FWA imprinting
in Arabidopsis endosperm by DNA methylation. Science 303,
521–523.
Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, Fischer RL.
1999. Imprinting of the MEDEA Polycomb gene in the Arabidopsis
endosperm. The Plant Cell 11, 1945–1952.
Kiyosue T, Ohad N, Yadegari R, et al. 1999. Control of
fertilization-independent endosperm development by the MEDEA
Polycomb gene in Arabidopsis. Proceedings of the National Academy
of Sciences, USA 96, 4186–4191.
Köhler C, Wolff P, Spillane C. 2012. Epigenetic mechanisms
underlying genomic imprinting in plants. Annual Review of Plant
Biology 63, 18.1–18.22.
Law JA, Jacobsen SE. 2010. Establishing, maintaining and
modifying DNA methylation patterns in plants and animals. Nature
Reviews Genetics 11, 204–220.
Li C, Zhou A, Sang T. 2006. Genetic analysis of rice domestication
syndrome with the wild annual species, Oryza nivara. New Phytologist
170, 185–193.
Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA.
2006. Phylogeography of Asian wild rice, Oryza rufipogon, reveals
multiple independent domestications of cultivated rice, Oryza sativa.
Proceedings of the National Academy of Sciences, USA 103,
9578–9583.
Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A.
2000. Expression and parent-of-origin effects for FIS2, MEA, and
FIE in the endosperm and embryo of developing Arabidopsis
seeds. Proceedings of the National Academy of Sciences, USA 97,
10637–10642.
Luo M, Platten D, Chaudhury A, Peacock W, Dennis ES.
2009. Expression, imprinting, and evolution of rice homologs of the
Polycomb group genes. Molecular Plant 2, 711–723.
Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S,
Singh M, Koltunow A. 2011. A genome-wide survey of imprinted
genes in rice seeds reveals imprinting primarily occurs in the
endosperm. PLoS Genetics 7, e1002125.
Makarevich G, Villar CB, Erilova A, Köhler C. 2008. Mechanism
of PHERES1 imprinting in Arabidopsis. Journal of Cell Science 121,
906–912.
McKeown PC, Laouielle-Duprat S, Prins P, et al. 2011.
Identification of imprinted genes subject to parent-of-origin
specific expression in Arabidopsis thaliana seeds. BMC Plant
Biology 11, 113.
Mosher RA, Tan EH, Shin J, Fischer RL, Pikaard CS,
Baulcombe DC. 2011. An atypical epigenetic mechanism affects
uniparental expression of Pol IV-dependent siRNAs. PLoS One 6,
e25756.
Nodine MD, Bartel DP. 2012. Maternal and paternal genomes
contribute equally to the transcriptome of early plant embryos. Nature
482, 94–97.
O’Connell MJ, Loughran NB, Walsh TA, Donoghue MT,
Schmid KJ, Spillane C. 2010. A phylogenetic approach to test for
evidence of parental conflict or gene duplications associated with
protein-encoding imprinted orthologous genes in placental mammals.
Mammalian Genome 21, 486–498.
Pask AJ, Papenfuss AT, Ager EI, McColl KA, Speed TP,
Renfree MB. 2009. Analysis of the platypus genome suggests a
transposon origin for mammalian imprinting. Genome Biology 10, R1.
4722 | Genomic imprinting in plants
Reik W, Constancia M, Fowden A, Anderson N, Dean W,
Ferguson-Smith A, Tycko B, Sibley C. 2003. Regulation of supply
and demand for maternal nutrients in mammals by imprinted genes.
Journal of Physiology 547, 35–44.
Reik W, Walter J. 2001. Genomic imprinting: parental influence on
the genome. Nature Revue Genetics 2, 21–32.
Royo H, Cavaille J. 2008. Non-coding RNAs in imprinted gene
clusters. Biology of the Cell 100, 149–166.
Santoro F, Barlow DP. 2011. Developmental control of imprinted
expression by macro non-coding RNAs. Seminars of Cell
Developmental Biology 22, 328–335.
Schoft VK, Chumak N, Choi Y, et al. 2011. Function of the
DEMETER DNA glycosylase in the Arabidopsis thaliana male
gametophyte. Proceedings of the National Academy of Sciences, USA
108, 8042–8047.
Schuettengruber B, Cavalli G. 2009. Recruitment of Polycomb
group complexes and their role in the dynamic regulation of cell fate
choice. Development 136, 3531–3542.
Scott RJ, Spielman M, Bailey J, Dickinson HG. 1998.
Parent-of-origin effects on seed development in Arabidopsis thaliana.
Development 125, 3329–3341.
Spillane C, Schmid KJ, Laoueille-Duprat S, Pien S,
Escobar-Restrepo JM, Baroux C, Gagliardini V, Page DR,
Wolfe KH, Grossniklaus U. 2007. Positive Darwinian selection at
the imprinted MEDEA locus in plants. Nature 448, 349–352.
imprinting at the Arabidopsis medea locus requires zygotic DDM1
activity. Genes and Development 13, 2971–2982.
Villar CB, Erilova A, Makarevich G, Trösch R, Köhler C. 2009.
Control of PHERES1 imprinting in Arabidopsis by direct tandem
repeats. Molecular Plant 2, 654–660.
Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA,
Yeh CT, Xu W, Schnable PS, Vaughn MW, Gehring M,
Springer NM. 2011. Parent-of-origin effects on gene expression
and DNA methylation in the maize endosperm. The Plant Cell 23,
4221–4233.
Weinhofer I, Hehenberger E, Roszak P, Hennig L, Köhler C.
2010. H3K27me3 profiling of the endosperm implies exclusion of
polycomb group protein targeting by DNA methylation. PLoS Genetics
6, e1001152.
Wolf JB, Hager R. 2006. A maternal-offspring coadaptation theory
for the evolution of genomic imprinting. PLoS Biology 4, e380.
Wolff P, Weinhofer I, Seguin J, Roszak P, Beisel C,
Donoghue MT, Spillane C, Nordborg M, Rehmsmeier M, Köhler
C. 2011. High-resolution analysis of parent-of-origin allelic expression
in the Arabidopsis endosperm. PLoS Genetics 7, e1002126.
Wu HA, Bernstein E. 2008. Partners in imprinting: noncoding RNA
and Polycomb group proteins. Developmental Cell 15, 637–638.
Yoder JA, Walsh CP, Bestor TH. 1997. Cytosine methylation
and the ecology of intragenomic parasites. Trends in Genetics 13,
335–340.
Suzuki S, Ono R, Narita T, et al. 2007. Retrotransposon silencing
by DNA methylation can drive mammalian genomic imprinting. PLoS
Genetics 3, e55.
Zhai J, Liu J, Liu B, Li P, Meyers BC, Chen X, Cao X. 2008. Small
RNA-directed epigenetic natural variation in Arabidopsis thaliana.
PLoS Genetics 4, e1000056.
Tiwari S, Schulz R, Ikeda Y, et al. 2008. MATERNALLY EXPRESSED
PAB C-TERMINAL, a novel imprinted gene in Arabidopsis, encodes
the conserved C-terminal domain of polyadenylate binding proteins.
The Plant Cell 20, 2387–2398.
Zhang M, Zhao H, Xie S, et al. 2011. Extensive, clustered parental
imprinting of protein-coding and noncoding RNAs in developing maize
endosperm. Proceedings of the National Academy of Sciences, USA
108, 20042–20047.
Tolhuis B, Blom M, Kerkhoven RM, Pagie L, Teunissen H,
Nieuwland M, Simonis M, de Laat W, van Lohuizen M,
van Steensel B. 2011. Interactions among Polycomb domains are
guided by chromosome architecture. PLoS Genetics 7, e1001343.
Zhang X, Shiu SH, Cal A, Borevitz JO. 2008. Global analysis of
genetic, epigenetic and transcriptional polymorphisms in Arabidopsis
thaliana using whole genome tiling arrays. PLoS Genetics 4,
e1000032.
Trivers R, Burt A. 1999. Kinship and genomic imprinting. Results and
Problems in Cell Differentiation 25, 1–21.
Zhang X, Borevitz JO. 2009. Global analysis of allele-specific
expression in Arabidopsis thaliana. Genetics 182, 943–954.
Vaughn MW, Tanurdzic M, Lippman Z, et al. 2007. Epigenetic
natural variation in Arabidopsis thaliana. PLoS Biology 5, e174.
Zheng X, Pontes O, Zhu J, Miki D, Zhang F, Li WX, Iida K,
Kapoor A, Pikaard CS, Zhu JK. 2008. ROS3 is an RNA-binding
protein required for DNA demethylation in Arabidopsis. Nature 455,
1259–1262.
Vielle-Calzada JP, Thomas J, Spillane C, Coluccio A,
Hoeppner MA, Grossniklaus U. 1999. Maintenance of genomic