1 EMBO YIP Team, Unité Mixte de Recherche 5667, IFR128 BioSciences
Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 allée
d'Italie, F-69364 Lyon cedex 07, France
2 Institute of Plant Biology and Zürich-Basel Plant Science Center,
University of Zürich, Zollikerstrasse 107, CH-8008 Zürich,
Switzerland
* Author for correspondence (e-mail: frederic.berger{at}ens-lyon.fr)
Accepted 12 March 2004
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SUMMARY |
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Key words: Arabidopsis thaliana, Endosperm, Seed, FIS, Polycomb, MSI1
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Introduction |
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In Arabidopsis, the genes MEDEA (MEA) and
FERTILIZATION INDEPENDENT SEED 2 (FIS2) encode the Polycomb
group (PcG) protein homologues of Enhancer of zeste (E(Z)) and Suppressor of
zeste 12 (SU(Z)12) in Drosophila, respectively
(Grossniklaus et al., 1998;
Luo et al., 1999
). MEA
interacts in a PcG complex with the Arabidopsis homologue of Extra
Sex Combs (ESC), FERTILIZATION INDEPENDENT ENDOSPERM (FIE)
(Ohad et al., 1999
;
Luo et al., 2000
;
Spillane et al., 2000
;
Yadegari et al., 2000
) and
FIS2 is likely to be a third member of this PcG complex
(Berger and Gaudin, 2003
;
Köhler et al., 2003a
;
Reyes and Grossniklaus, 2003
).
The fis mutants were originally isolated for the capacity to initiate
seed development in absence of fertilisation
(Peacock et al., 1995
;
Ohad et al., 1996
;
Chaudhury et al., 1997
).
Autonomous seeds do not contain an embryo but only endosperm.
Another original feature shared by fis mutants is a gametophytic
maternal effect on seed abortion. The FIS class gene MEA was
originally identified in a screen for female gametophytic mutants affecting
embryo sac development and function or displaying maternal effects
(Grossniklaus et al., 1998).
Seeds derived from female gametophytes carrying a mutation in one of the
FIS genes abort irrespective of whether the paternal allele is mutant
or wild type (WT). Among other phenotypes, the fis class mutants for
FIE, MEA and FIS2 are all characterised by an abnormal
development of the endosperm posterior pole with a cyst and nodules larger
than in the WT and the ectopic location of nodules in the peripheral endosperm
(Sørensen et al.,
2001
). The endosperm of fis mutants shares other common
features such as the absence of cellularisation and overproliferation at late
stages (Kiyosue et al., 1999
;
Vinkenoog et al., 2000
;
Sørensen et al.,
2001
).
We have previously isolated the enhancer trap green fluorescent protein
(GFP) marker line KS117 that displays uniform GFP expression in the endosperm
until the embryo dermatogen stage and later becomes confined to the posterior
pole (Haseloff, 1999)
(http://www.plantsci.cam.ac.uk/Haseloff).
In contrast to the WT, KS117 GFP expression in a fis mutant
background is uniform throughout endosperm development and dramatically
over-expressed as early as the embryo octant stage
(Sørensen et al.,
2001
).
In this study, we took advantage of KS117 GFP reporter gene expression to
compare the dynamics of endosperm posterior pole formation in the WT and
fis mutants. We screened for altered KS117 GFP expression to identify
mutants that showed defects in endosperm patterning pertaining to the
posterior pole. We isolated two new members of the fis class,
medicis and borgia. MEDICIS encodes the WD40 domain protein
MSI1 that has recently been demonstrated to directly interact with the FIS
class protein FIE in the MEA/FIE PcG complex
(Köhler et al., 2003a).
Although medicis and borgia display autonomous endosperm
development as do other fis mutants, they show distinctive genetic
and phenotypic features.
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Materials and methods |
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Microscopy and image processing
Developing seeds were isolated from individual siliques at different stages
of development. Each population of seed was mounted in Hoyer's medium
(Boisnard-Lorig et al., 2001)
and fluorescence associated to the KS117 marker was readily observed with a
Leica MZFLIII stereomicroscope coupled to a DC300F digital camera (Leica
Microsystems, Heerburg, Germany). Images were processed with the FW4000
software (Leica). Endosperm size was measured using Image J (software
available at
rsb.info.nih.gov/ij/)
in WT and mutant populations of seeds. After clearing in Hoyer's medium, the
phenotype was determined microscopically using differential interference
contrast (DIC) optics (Optiphot, Nikon, Tokyo, Japan) coupled with an
AxioCam MRc digital camera (Carl Zeiss, Jena, Germany) and linked for each
seed to the associated genotype determined by the expression of KS117 GFP.
Images were processed with Axiovision software (Zeiss).
For confocal microscopy, seeds were stained with Feulgen as described
previously (Garcia et al.,
2003) and examined with a Zeiss LSM 510 microscope with a
x63 Plan-Apochromat oil immersion objective (n. a. 1.4). Serial optical
sections of 0.4 µm to 0.6 µm depth were recorded. Nucleoli were manually
segmented on each section with Image J, recorded as an individual stack of
images which was eventually subtracted from the original stack. Resulting
stacks were imported as separate channels in the Imaris software (Bitplane AG,
Zürich, Switzerland), pseudocoloured in white, red or yellow and
visualised as a 3D volume. All figures were composed with Adobe Photoshop 5.5
(Adobe Systems, San Jose, USA).
Time-lapse imaging of NCDs migration
Seeds from plants homozygous for the marker KS22
(Boisnard-Lorig et al., 2001)
were used for analysis of the WT and from plants heterozygous for
fis1/mea, fis2-3 and fie-10 and homozygous for KS117 for
analysis of KS117 reporter gene expression in fis mutant backgrounds.
Freshly isolated siliques were prepared as described previously in order to be
able to perform time-lapse analysis of NCDs migration
(Boisnard-Lorig et al., 2001
).
Seeds oriented in such a way that the endosperm posterior pole was included in
the confocal plane were selected for examination. Sections with
1024x1024 pixels were typically recorded every 10 minutes for at least
12 hours using a x20 (n. a. 0.4) Ph2 Achroplan objective (Carl Zeiss,
Jena, Germany) and a LSM510 Zeiss confocal laser scanning microscope. AVI
films were mounted using the software Metamorph.
Genetic screen
4000 M1 plants were grown from KS117/KS117 gamma-ray irradiated
seeds (200 gray at a rate of 27 gray/minute) and the main stem cut to allow
development of lateral sectors. One sector was chosen per plant and one
silique was slit open and seeds examined at the green embryo stage. The
presence of 10% semi-sterile mutation (absence of development of 50% of
seeds), 8% embryo lethal mutation (collapsed seeds) and 1.1% albino mutations
(seeds with a white embryo) was recorded. These percentages compared with
those obtained in EMS screens
(Jürgens et al., 1991)
allowed us to estimate the expected allelic frequency of the screen to be one
to two alleles per mutation. In parallel, we mounted a small population of
seeds isolated from one or two siliques in mounting medium on a microscope
slide. Mounting medium consisted of 0.3% plant agar (Duchefa, The Netherlands)
in Murashige and Skoog culture medium (Sigma, Saint-Quentin Fallavier,
France). Seeds were isolated at the embryonic heart stage when KS117
expression is confined to the posterior pole in the WT. We observed GFP
fluorescence patterns of the KS117 marker using a Leica MZFLIII
stereomicroscope equipped with a x1.6 planApo objective (Leica, Jena,
Germany) coupled to a DC300F digital camera (Leica Microsystems, Heerburg,
Germany). Images were processed with the FW4000 software (Leica). Four
backcrosses to WT KS117/KS117 were performed for each line.
Genetic mapping
F2 mapping populations were generated by crossing each mutant
line to WT Columbia. Putative alleles of mea, fis2, fie and
dme were identified through a low recombination rate with the
following markers, respectively: nT7i23 (for primer sequences, see the TAIR
database
(www.arabidopsis.org),
fis2sslp (5'-AATTGAGCCCTTTGACGTTTTGGTA-3' and
5'-CCTGCATTGTTTGGGAGTGATAGAA-3'), CER456484 [designed from Cereon
database
(www.arabidopsis.org/Cereon/index.html)
(Jander et al., 2002)],
5'-AACCCTAAAGCTAGAGTTTATAGC-3' and
5'-CCAAGCTCTAAGCCAATCAGAGAAG-3') and CER479331 (Cereon,
5'-GACGTCGAGCGTAGATAGCACGC-3' and
5'-CTGGTGGTCCTACGTTCCGATTCAAG-3'). Allelism to mea, fie
or dme was confirmed by direct sequencing of the gene in the mutant
line and comparison to the WT sequence. Allelism to fis2 was
confirmed by phenotypic complementation. The putative fis2 alleles
JF2034 and JF2206 were crossed as homozygotes with a line containing the 18H1
cosmid containing a wild-type copy of FIS2 linked to kanamycin
resistance (KanR) (Luo et al.,
1999
). F1 plants were heterozygous for the mutation and
hemizygous for 18H1. In F1 plants, half the mutant ovules carry a
WT copy of FIS2 provided by 18H1 cosmid. Thus, if complementation
takes place, only 25% of seeds are expected to display the mutant phenotype in
contrast to a selfed heterozygote fis2 mutant that produces 50%
mutant seeds. Four independent KanR F1 plants were
analysed for each line and showed 25% mutant seeds instead of the 50% observed
in heterozygous plants [JF2034x18H1 no. 1: 23.7% mutant seeds (s.d.
6.5); no. 2: 27.3% (4.5); no. 3: 25.2% (5.5); no. 4: 24.2% (4.6).
JF2206x18H1 no. 1: 24.7% (4.3); no. 2: 21.7% (3.2); no. 3: 24.4% (5.5);
no. 4: 22.5% (2.6)]. The locus associated with the bga mutation was
located between TAIR markers PLS7 and nga1126. MEDICIS was shown to
be located between MTI20.1/2 (Cereon,
5'-AACCGTTTTCCATATCTTATTCTC-3' and
5'-TCAAATCATACAACTACGAAAGTC-3') and K19M22.4/5 (Cereon,
5'-AGGTAATTGGGCCAGGAACTAAAT-3' and
5'-CCAAACGGGAGTAAATCATCTGGTG-3').
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Results |
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Endosperm posterior pole formation is maternally controlled by a group of at least six loci associated with gametophytic mutations
To identify new members of the FIS pathway, we screened a population of
developing M2 seeds of 4000 M1 plants for abnormal GFP
expression from the posterior endosperm marker KS117. We identified ten
putatively gametophytic mutants. As heterozygotes they produced 28-50% seeds
that over-expressed KS117 GFP and did not restrict its expression to the
posterior pole (Fig. 4A-G). At
the WT mature green embryo stage, mutant seeds are distinguished by a white
translucent colour with a small green embryo
(Fig. 4H-N). Eventually seed
integuments collapse and shrivel around the embryos that arrest development at
various stages after the heart stage. With the exception of JF0122, JF1762 and
JF2973, plants homozygous for the mutation could be recovered from all other
lines, showing that most of these mutations were not fully penetrant for seed
lethality.
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During the course of this work the mutant demeter (dme)
was isolated and reported to be defective in transcriptional activation of
MEA (Choi et al.,
2002). DME is located on chromosome 5, close to the
position we determined for JF1348, suggesting that JF1348 was allelic to
dme. We sequenced DME in this mutant and could confirm the
allelism (Fig. S1,
http://dev.biologists.org/supplemental/).
For two lines that could be mapped to chromosome 2 and 5, respectively,
JF1728 and JF2973, no tight linkage to any of the known FIS genes was
detected, suggesting that these two mutants affected unknown genes. We named
these two mutants borgia and medicis, respectively, as a
reference to the Italian families of the Renaissance period who were
particularly remarkable for a tradition of infanticide as was Medea in antique
Greece. The borgia mutation is located in proximity of FIS2
on chromosome 2 but bga location could be narrowed down to a region
that does not contain FIS2, confirming that we had identified a new
fis class locus on chromosome 2. We attribute the gene symbol
BGA to this locus. Map-based cloning of medicis narrowed
down the location of the mutation to a 280 kb interval that included the BACs
MTI20, K21L19, MCK7 and MQJ2 on chromosome 5. This portion of the
Arabidopsis genome contains the MSI1 gene which was a
candidate for the mutation. An orthologue of MSI1 in Drosophila, p55,
is part of the PcG complex formed by genes homologous to the FIS
genes MEA, FIS2 and FIE
(Tie et al., 2001). In the
course of this work, we learned that a T-DNA insertion in MSI1 was
associated with a loss-of-function that caused a phenotype similar to the
fis phenotype (Köhler et
al., 2003a
). Thus, we sequenced MSI1 in medicis
and identified a mutation leading to the production of a very short truncated
protein (Fig. S1,
http://dev.biologists.org/supplemental/).
We hereafter refer to the medicis mutation as msi1-2.
In summary, the ten gametophytic mutants recovered from our screen identified three new mea alleles (hereafter referred to as mea-5 to mea-7), two new fis2 alleles (hereafter referred to as fis2-6 and fis2-7), two new fie alleles (hereafter referred to as fie-10 and fie-11), and one allele each of dme (hereafter referred to as dme-4) and msi1 (hereafter referred to as msi1-2). Importantly, our screen reveals the mutation bga-1 in a new fis class locus on chromosome 2.
Effects of bga on seed development
Taking advantage of the differential KS117 GFP expression pattern between
WT and bga seeds, we established a precise description of mutant
seeds development. Mutant bga embryo development is similar to the WT
until early heart stage (Fig.
5A,D). From the WT mid heart stage, mutant embryo development
slows down (Fig. 5B,E) and
eventually arrests between the late heart and the late torpedo stages when the
WT embryos reach the mature green stage. Overall WT and mutant development of
endosperm are similar until the endosperm contains 200 nuclei. At this stage,
the WT endosperm cellularises, whereas the bga endosperm does not
(n=114, Fig. 5C,F).
Furthermore, an overgrowth of nodules and cyst is visible from this stage in
the mutant endosperm and is amplified later in development
(Fig. 6A,B). Seed size
measurements show that bga and WT endosperms are similar in size, as
it is the case for fie-11 at this point of seed development
(Table 2). Cellularisation is
followed in the WT by one cycle of pseudo-synchronous cell division leading to
an endosperm containing 400 nuclei. Only half of the mutant bga
syncytial endosperms undergo this division (n=39), and endosperm
nuclear proliferation is arrested in bga seeds after this stage.
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In conclusion, the bga mutation has a gametophytic maternal effect
on embryo and endosperm development. The embryo is first delayed from the
early heart stage and then arrested at late stages. Ectopic nodule formation
occurs in bga endosperm as in other fis mutants, but in
contrast to what was described previously for mea and for
fie (Kiyosue et al.,
1999; Vinkenoog et al.,
2000
), no overproliferation of endosperm nuclei was observed in
bga.
msi1 has both sporophytic and gametophytic effects on seed development
When msi1/MSI1 pistils are pollinated by WT plants,
siliques contain 52% seeds showing a fis phenotype, while reciprocal
crosses produce only seeds with a WT phenotype
(Table 1). These results show
that the msi1 fis-like phenotype is under gametophytic maternal
control. We were not able to obtain plants homozygous for msi1 as a
result of embryo lethality. Furthermore, transmission of the msi1
allele via the female gametes is null (n=232 F1 plants).
Paternal transmission is also reduced in the msi1 mutant, as only
36.2% F1 plants (n=232) from pollination of WT pistil by
msi1/MSI1 bear the mutant allele. Mature pollen grains from
msi1/MSI1 plants contain two gametes and present a normal morphology
(not shown) and the origin of reduced paternal transmission remains
unknown.
When msi1/MSI1 plants are self-pollinated only 30% of the
seeds have a fis phenotype and 22% of the seeds display a distinct
phenotype with severe embryo abnormalities. The distribution of the
fis and abnormal embryo phenotypes in self-pollinated plants is 2
WT:1 fis-like:1 abnormal embryo (n=157,
2=2.22 <
20.05[2]=5.991),
suggesting that the abnormal embryo phenotype is under sporophytic recessive
control.
KS117 GFP overexpression in mutant seeds allowed us to examine endosperm and embryo development in msi1/MSI1 self-pollinated plants. The sporophytic recessive phenotype in embryos is distinguished as early as the WT octant stage. Improper cell division patterns are observed in the embryo proper and in the suspensor (Fig. 7A,G), leading to the development of a highly abnormal embryo (Fig. 7B,H). Endosperm that surrounds the arrested embryo does not differentiate a posterior chalazal pole nor cellularise, and nucleoli are variable in size (Fig. 7C,I). In the WT, syncytial endosperm development consists of synchronous nuclear divisions. In the mutant endosperm, we observed a delay of one cycle of division at each developmental stage, in comparison to WT seeds.
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In conclusion, the msi1-2 mutation causes a severe gametophytic
maternal effect on endosperm and embryo development, and a distinct
sporophytic recessive embryo lethality. The pace and pattern of cell and
nuclei divisions are severely affected in msi1/msi1 embryo and
endosperm, as early as the octant stage in the WT embryo. The gametophytic
maternal effect causes the arrest of embryo development and affects several
features of endosperm development as other fis mutations. But, unlike
other mutations (Kiyosue et al.,
1999; Vinkenoog et al.,
2000
), the msi1 gametophytic maternal phenotype includes
a reduction of growth and proliferation of endosperm after the stage when WT
endosperm cellularises.
msi1 and bga mutations promote autonomous seed development
The mutants mea, fis2 and fie are able to initiate
endosperm development in the absence of fertilisation. Autonomous endosperm
development is accompanied by increase in pistil elongation, which was used as
a criterion to identify alleles representative of several fis class
loci (Fig. 8A-G). We observed
very little or no pistil elongation for dme-4 as reported for
dme-1 (Choi et al.,
2002). In contrast, pistil elongation was marked for the other
loci, with increasing strength in the following order, bga, mea, fis2,
fie and msi1. Endosperm development is characterised by an
increase in ovule size leading to a small developing seed that contains
autonomous endosperm (Ohad et al.,
1996
; Chaudhury et al.,
1997
). We quantified the penetrance of mutations at each locus by
counting the number of autonomous seeds relative to the total number of ovules
that are likely to carry the mutation
(Table 3,
Fig. 8H-N). The penetrance of
each mutation is correlated with the degree of pistil elongation. While no
autonomous seed development was observed in dme/DME, 25-92% of the
mutant ovules of other fis/FIS plants undergo some degree of seed
development in the absence of fertilisation. The allele msi1-2 has
the highest rate of autonomous seed development, with a penetrance of 92%,
suggesting that almost every ovule that inherits the msi1-2 mutation
undergoes autonomous seed development. We conclude that, unlike dme,
which does not promote autonomous seed development, bga and
msi1 represent true new members of the fis class of mutants.
As observed for alterations of endosperm development and penetrance of seed
abortion, bga has the weakest effects on autonomous seed development
while msi1 causes the strongest defect in this trait.
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Discussion |
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We had reported that fis mutations affect the organisation of the
posterior pole with overproliferation in nodules that could be located at
ectopic position (Sørensen et al.,
2001). We show in this study that fis mutations impair
the migrations of NCDs to the posterior pole. As NCDs do not migrate or
migrate at random, they eventually merge at a location distant from the
posterior pole and form nodules at ectopic positions. The tight regulation of
NCD migration, at least in part, is under the control of the MEA/FIE PcG
complex. It can be proposed that the MEA/FIE PcG complex regulates structural
features, such as the cytoskeleton, involved in endosperm polarity and NCD
migration. According to an alternative hypothesis, the absence of NCD
migration in the fis mutants could reflect a general delay of
endosperm development. However, such a hypothesis should involve a reduction
of growth and nuclear proliferation. This is not observed during fis
endosperm development. We therefore propose that the absence of NCD migration
in fis mutants reveals impairment of a specific mechanism rather than
a global developmental delay.
Maternal control of development of the endosperm posterior pole depends on the conserved MEA/FIE Polycomb Group complex
We identified ten gametophytic maternal mutants showing a fis
phenotype of the KS117 GFP expression pattern. Of these ten mutants, eight are
allelic to mea, fis2, fie or dme. Table S1
(http://dev.biologists.org/supplemental/)
compiles all the known and new mutant alleles for each of these loci. Genetic
mapping identified two other loci, bga and msi1, at
locations distinct from that of other known fis mutants. We have
identified one allele for each of these two loci.
The definition of the fis class of mutants was based on the common
ability of mea, fis2 and fie mutants to initiate autonomous
seed development. Whereas dme does not show this trait, the new
mutants bga and msi1 demonstrated autonomous endosperm
development. We also show that, as described for other fis mutants
(Kiyosue et al., 1999;
Vinkenoog et al., 2000
), the
development of seeds that maternally inherit bga or msi1 is
phenotypically normal until endosperm cellularisation. From this stage,
developmental defects, including perturbation of the posterior pole formation
and decrease in seed viability due to embryo arrest, are observed. Ectopic
nodules observed in msi1 and bga probably result from the
impaired migration of NCDs although we have not performed dynamic observations
in these backgrounds. Thus, the two new loci we identified on the basis of
their gametophytic maternal control on endosperm development share all the
typical characteristics of the fis phenotype with the exception of
endosperm overproliferation at late stages, and may constitute additional
members of the MEA/FIE PcG complex.
Members of the FIS class represent members of a conserved PcG complex
Our finding that medicis is mutated in the gene encoding MSI1
supports the recent demonstration of MSI1 as part of the MEA/FIE PcG protein
complex (Köhler et al.,
2003a). MEA, FIS2 and FIE are homologues of the
Drosophila PcG proteins E(Z), SU(Z)12 and ESC, respectively that
participate in a 600 kDa complex (Tie et
al., 2001
). This PcG complex has been analysed in detail and
contains p55, the homologue of MSI1. This strongly suggests a conservation of
the PcG E(Z)/ESC complex between plants and animals.
In this study we describe the new fis class mutant bga.
Penetrance in bga mutant is weak, suggesting that either our unique
allele bga-1 is a weak allele, or the BGA protein may form a specific
transient complex with the conserved MEA/FIE core complex. In
Drosophila the histone deacetylase RPD3 has been shown to be part of
the 600 kDa E(Z)/ESC complex in embryos
(Tie et al., 2001). However,
although the Arabidopsis genome contains ten members of the RPD3
family (Pandey et al., 2002
),
none of them is located in the vicinity of the bga locus.
Alternatively, bga might be defective in a regulator of expression or
imprinting of the FIS genes such as DME
(Choi et al., 2002
).
Interestingly, besides the embryo arrest provoked by the maternal loss of
function of MSI1, we observed in msi1-2 an embryonic
phenotype under a sporophytic recessive control. If the seed inherits paternal
and maternal msi1-2 alleles, the embryo pattern is disrupted by cell
divisions with a random orientation leading to an early arrest. Consistently
abnormally enlarged nucleoli are observed in endosperm suggesting an improper
control of nuclear division. MSI1 is known to be part of
Arabidopsis Chromatin Assembly Factor-1 (CAF-1), together with
FASCIATA1 and FASCIATA2 (Kaya et al.,
2001). In vitro assays show that CAF-1 has a replication-dependent
nucleosome assembly activity. Furthermore, Ach et al.
(Ach et al., 1997
) have shown
that the tomato homologue of MSI1, LeMSI1, interacts with Retinoblastoma
(Rb)-like RBB1 protein from Maize. Hennig et al.
(Hennig et al., 2003
) also
suggest that Arabidopsis MSI1 is able to interact with
Arabidopsis Rb-related RBR protein. As it is known in animals that Rb
is involved in G1 phase progression (reviewed by
Weinberg, 1995
), it is
possible that MSI1 represents a link that has already been suspected in
animals between chromatin remodelling by PcG and the control of the cell cycle
(Jacobs and van Lohuizen,
2002
).
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ACKNOWLEDGMENTS |
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Footnotes |
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REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ach, R. A., Taranto, P. and Gruissem, W.
(1997). A conserved family of WD-40 proteins binds to the
retinoblastoma protein in both plants and animals. Plant
Cell 9,1595
-1606.
Adams, S., Vinkenoog, R., Spielman, M., Dickinson, H. G. and
Scott, R. J. (2000). Parent-of-origin effects on seed
development in Arabidopsis thaliana require DNA methylation.
Development 127,2493
-2502.
Berger, F. and Gaudin, V. (2003). Chromatin dynamics and Arabidopsis development. Chromosome Res. 11,277 -304.[CrossRef][Medline]
Boisnard-Lorig, C., Colon-Carmona, A., Bauch, M., Hodge, S.,
Doerner, P., Bancharel, E., Dumas, C., Haseloff, J. and Berger, F.
(2001). Dynamic analyses of the expression of the HISTONE::YFP
fusion protein in Arabidopsis show that syncytial endosperm is
divided in mitotic domains. Plant Cell
13,495
-509.
Brown, R. C., Lemmon, B. E., Nguyen, H. and Olsen, O.-A. (1999). Development of endosperm in Arabidopsis thaliana.Sex Plant Reprod. 12,32 -42.[CrossRef]
Brown, R. C. and Lemmon, B. E. (2001). The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215,35 -49.[Medline]
Carter, G. C., Rodger, G., Murphy, B. J., Law, M., Krauss, O.,
Hollinshead, M. and Smith, G. L. (2003). Vaccinia virus cores
are transported on microtubules. J. Gen. Virol.
84,2443
-2458.
Castle, L. A., Errampalli, D., Atherton, T. L., Franzmann, L. H., Yoon, E. S. and Meinke, D. W. (1993). Genetic and molecular characterization of embryonic mutants identified following seed transformation in Arabidopsis. Mol. Gen. Genet. 241,504 -514.[Medline]
Chaudhury, A. M., Ming, L., Miller, C., Craig, S., Dennis, E. S.
and Peacock, W. J. (1997). Fertilization-independent seed
development in Arabidopsis thaliana. Proc. Natl. Acad. Sci.
USA 94,4223
-4228.
Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J. J., Goldberg, R. B., Jacobsen, S. E. and Fischer, R. L. (2002). DEMETER, a DNA Glycosylase Domain Protein, Is Required for Endosperm Gene Imprinting and Seed Viability in Arabidopsis. Cell 110, 33-42.[Medline]
Finnegan, E. J., Peacock, W. J. and Dennis, E. S.
(1996). Reduced DNA methylation in Arabidopsis thaliana
results in abnormal plant development. Proc. Natl. Acad. Sci.
USA 93,8449
-8454.
Floyd, S. K. and Friedman, W. E. (2000). Evolution of endosperm developmental patterns among basal flowering plants. Int. J. Plant Sci. 161Suppl. S, S57-S81.[CrossRef]
Garcia, D., Saingery, V., Chambrier, P., Mayer, U.,
Jürgens, G. and Berger, F. (2003). Arabidopsis
haiku mutants reveal new controls of seed size by endosperm. Plant
Physiol. 131,1661
-1670.
Grossniklaus, U., Vielle-Calzada, J. P., Hoeppner, M. A. and
Gagliano, W. B. (1998). Maternal control of embryogenesis by
MEDEA, a polycomb group gene in Arabidopsis.Science 280,446
-450.
Haseloff, J. (1999). GFP variants for multispectral imaging of living cells. Methods Cell Biol. 58,139 -151.[Medline]
Hebsgaard, S. M., Korning, P. G., Tolstrup, N., Engelbrecht, J.,
Rouze, P. and Brunak, S. (1996). Splice site prediction in
Arabidopsis thaliana pre-mRNA by combining local and global sequence
information. Nucleic Acids Res.
24,3439
-3452.
Hennig, L., Taranto, P., Walser, M., Schonrock, N. and Gruissem,
W. (2003). Arabidopsis MSI1 is required for
epigenetic maintenance of reproductive development.
Development 130,2555
-2565.
Jacobs, J. J. L. and van Lohuizen, M. (2002). Polycomb repression: from cellular memory to cellular proliferation and cancer. Biochim. Biophys. Acta 1602,151 -161.[CrossRef][Medline]
Jander, G., Norris, S. R., Rounsley, S. D., Bush, D. F., Levin,
I. M. and Last, R. L. (2002). Arabidopsis map-based
cloning in the post-genome era. Plant Physiol.
129,440
-450.
Jürgens, G., Mayer, U., Torres-Ruiz, R. A., Berleth, T. and Miséra, S. (1991). Genetic analysis of pattern formation in the Arabidopsis embryo. Development Suppl. 1,27 -38.
Kaya, H., Shibahara, K.-I., Taoka, K.-I., Iwabuchi, M., Stillman, B., Araki, T. (2001). FASCIATA genes for Chromatin Assembly Factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104,131 -142.[Medline]
Kiyosue, T., Ohad, N., Yadegari, R., Hannon, M., Dinneny, J.,
Wells, D., Katz, A., Margossian, L., Harada, J. J., Goldberg, R. B. and
Fischer, R. L. (1999). Control of fertilization-independent
endosperm development by the MEDEA polycomb gene in Arabidopsis.Proc. Natl. Acad. Sci. USA
96,4186
-4191.
Köhler, C., Hennig, L., Bouveret, R., Gheyselinck, J.,
Grossniklaus, U. and Gruissem, W. (2003a).
Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex
and required for seed development. EMBO J.
22,4804
-4814.
Köhler, C., Hennig, L., Spillane, C., Pien, S., Gruissem,
W. and Grossniklaus, U. (2003b). The Polycomb-group protein
MEDEA regulates seed development by controlling expression of the MADS-box
gene PHERES1. Genes Dev.
17,1540
-1553.
Luo, M., Bilodeau, P., Koltunow, A., Dennis, E. S., Peacock, W.
J. and Chaudhury, A. M. (1999). Genes controlling
fertilization-independent seed development in Arabidopsis thaliana.Proc. Natl. Acad. Sci. USA
96,296
-301.
Luo, M., Bilodeau, P., Dennis, E. S., Peacock, W. J. and
Chaudhury, A. (2000). Expression and parent-of-origin effects
for FIS2, MEA, and FIE in the endosperm and embryo of
developing Arabidopsis seeds. Proc. Natl. Acad. Sci.
USA 97,10637
-10642.
Mansfield, S. G. and Briarty, L. G. (1990). Development of the free-nuclear endosperm in Arabidopsis thaliana.Arabidopsis Inf. Serv. 27,53 -64.
Nguyen, H., Brown, R. C. and Lemmon, B. E. (2002). Cytoskeletal organization of the micropylar endosperm in Coronopus didymus L. (Brassicaceae). Protoplasma 219,210 -220.[CrossRef][Medline]
Ohad, N., Margossian, L., Hsu, Y. C., Williams, C., Repetti, P.
and Fischer, R. L. (1996). A mutation that allows endosperm
development without fertilization. Proc. Natl. Acad. Sci.
USA 93,5319
-5324.
Ohad, N., Yadegari, R., Margossian, L., Hannon, M., Michaeli,
D., Harada, J. J., Goldberg, R. B. and Fischer, R. L. (1999).
Mutations in FIE, a WD polycomb group gene, allow endosperm development
without fertilization. Plant Cell
11,407
-416.
Pandey, R., Muller, A., Napoli, C. A., Selinger, D. A., Pikaard,
C. S., Richards, E. J., Bender, J., Mount, D. W. and Jorgensen, R. A.
(2002). Analysis of histone acetyltransferase and histone
deacetylase families of Arabidopsis thaliana suggests functional
diversification of chromatin modification among multicellular eukaryotes.
Nucleic Acids Res. 30,5036
-5055.
Peacock, J., Ming, L., Craig, S., Dennis, E. and Chaudhury, A. (1995). A mutagenesis programme for apomixis genes in Arabidopsis. In Induced Mutations and Molecular Techniques for Crop Improvement, pp. 117-125. Vienna, Austria: IAEA.
Pollock, N., Koonce, M. P., de-Hostos, E. L. and Vale, R. D. (1998). In vitro microtubule-based organelle transport in wild-type Dictyostelium and cells overexpressing a truncated dynein heavy chain. Cell Motil. Cytoskeleton 40,304 -314.[CrossRef][Medline]
Raghavan, V. (2003). Some reflections on double fertilization, from its discovery to the present. New Phytol. 159,565 -583.[CrossRef]
Reyes, J. C. and Grossniklaus, U. (2003). Diverse functions of Polycomb group proteins during plant development. Semin. Cell Dev. Biol. 14, 77-84.[CrossRef][Medline]
Scott, R. J., Spielman, M., Bailey, J. and Dickinson, H. G.
(1998). Parent-of-origin effects on seed development in
Arabidopsis thaliana. Development
125,3329
-3341.
Sørensen, M. B., Chaudhury, A. M., Robert, H., Bancharel, E. and Berger, F. (2001). Polycomb group genes control pattern formation in plant seed. Curr. Biol. 11,277 -281.[CrossRef][Medline]
Sørensen, M. B., Mayer, U., Lukowitz, W., Robert, H., Chambrier, P., Jürgens, G., Somerville, C., Lepiniec, L. and Berger, F. (2002). Cellularisation in the endosperm of Arabidopsis thaliana is coupled to mitosis and shares multiple components with cytokinesis. Development 129,5567 -5576.[CrossRef][Medline]
Spillane, C., MacDougall, C., Stock, C., Köhler, C., Vielle-Calzada, J. P., Nunes, S. M., Grossniklaus, U. and Goodrich, J. (2000). Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes. Curr. Biol. 10,1535 -1538.[CrossRef][Medline]
Tie, F., Furuyama, T., Prasad-Sinha, J., Jane, E. and Harte, P.
J. (2001). The Drosophila Polycomb Group proteins ESC and
E(Z) are present in a complex containing the histone-binding protein p55 and
the histone deacetylase RPD3. Development
128,275
-286.
Vinkenoog, R., Spielman, M., Adams, S., Fischer, R. L.,
Dickinson, H. G. and Scott, R. J. (2000). Hypomethylation
promotes autonomous endosperm development and rescues postfertilization
lethality in fie mutants. Plant Cell
12,2271
-2282.
Walbot, V. (1994). Overview of key steps in aleurone development. In The Maize Handbook, pp.78 -80. New York: Springer-Verlag.
Weinberg, R. A. (1995). The retinoblastoma protein and cell cycle. Cell 81,323 -330.[Medline]
Yadegari, R., Kinoshita, T., Lotan, O., Cohen, G., Katz, A.,
Choi, Y., Nakashima, K., Harada, J. J., Goldberg, R. B., Fischer, R. L. and
Ohad, N. (2000). Mutations in the FIE and
MEA genes that encode interacting polycomb proteins cause
parent-of-origin effects on seed development by distinct mechanisms.
Plant Cell 12,2367
-2381.