Download Genetic and epigenetic processes in seed development Allan R

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Genetic and epigenetic processes in seed development
Allan R Lohe* and Abed Chaudhury†
Seed development has emerged as an important area of
research in plant development. Recent research has highlighted
the divergent reproductive strategies of the male and female
genomes and interaction between genetic and epigenetic
control mechanisms. Isolation of genes involved in embryo and
endosperm development is leading to an understanding of the
regulation of these processes at the molecular level. A thorough
grasp of these processes will not only illuminate an important
area of plant development but will also have an impact on
agronomy by helping to facilitate food production. An
understanding of seed development is also likely to clarify the
molecular mechanisms of apomixis, a fascinating process of
asexual seed production present in many plants.
Addresses
CSIRO Division of Plant Industry, PO Box 1600, Canberra,
ACT 2601, Australia
*e-mail: [email protected]
† e-mail: [email protected]
Current Opinion in Plant Biology 2002, 5:19–25
1369-5266/02/$ — see front matter
© 2002 Elsevier Science Ltd. All rights reserved.
Abbreviations
AMP1 ALTERED MERISTEM PROGRAMMING1
ESC
EXTRA SEX COMBS
E(Z)
ENHANCER OF ZESTE
FIE
FERTILIZATION INDEPENDENT ENDOSPERM
FIS
FERTILIZATION INDEPENDENT SEED
MET1
METHYL TRANSFERASE1
MOM1 MORPHEUS’ MOLECULE1
PcG
Polycomb group
TTN
TITAN
YFP
yellow fluorescent protein
Introduction
Seed development is central to the reproductive strategy
of angiosperms. It is triggered by the process of double
fertilization: the haploid egg is fertilized by one sperm cell
and a homodiploid central cell of the ovule is fertilized by
another sperm cell, leading to the formation of diploid
embryo and triploid endosperm. Synchronized development
of the embryo and the endosperm occurs inside the
maternal ovule tissues, which are surrounded by inner
and outer integuments. Thus, the interplay of different
genome dosages encompassing the haploid and diploid
generations participate in the ontogeny of seed.
Among angiosperms, seed development in monocots and
eudicots has important differences and similarities.
Although both types of seed are produced by double
fertilization, the relative development of embryo and
endosperm is different in the two groups. In eudicots, the
majority of the seed bulk is made up of embryo, whereas
in monocots (such as rice and wheat), endosperm tissue
constitutes the bulk of the grain.
Although conventional Mendelian genetics held that the
paternal and maternal genomes contribute equally to the
zygote resulting from sexual reproduction, that view has
been altered recently. Significant new results challenging
this view have come from work on seed development.
These results suggest that the paternal genome is
probably less important in defining the early stages of
seed development and that a number of genes show a
parent-of-origin effect in their mode of action. The events
of early seed development are modulated by epigenetic
processes, such as DNA methylation and chromatin
remodeling, that act on a large number of genes. The
complex interplay of maternal and paternal genomes,
involving genetic and epigenetic processes, makes seed
development an exciting area of study. This complexity is
also central to our understanding of an agronomically
challenging branch of seed development: apomixis, this is,
reproduction without fertilization.
Although most plants use paternal and maternal genomes
to produce a diploid organism sexually, in apomictic plants,
functional seeds are produced without a female haploid
reduction phase and without any contribution of the
paternal parent. The key processes that trigger gametophytic
apomixis are, first, an alteration of the female meiotic
program that produces an unreduced embryo sac; second,
the ability of the unreduced egg to develop parthenogenetically to produce a completely maternal diploid embryo;
and, sometimes third, autonomous development of the
endosperm to nourish the embryo. Thus, apomixis involves
important alterations in the reproductive strategies of
genes that control normal reproductive development.
Knowledge gained from recent exciting research in seed
development is likely to help the engineering of apomixis
in agronomically important crop plants.
Double fertilization
Double fertilization constitutes two important events that
initiate the process of seed development. Upon pollen
maturation, two sperm cells are delivered via the pollen
tube into the embryo sac. It has been suggested that sperm
cells are taken to the embryo sac with the help of a
cytoskeletal system [1]. One of the sperm cells then fuses
with the egg cell and the other with the central cell, thereby
initiating embryo and endosperm development (Figure 1).
Whether an individual sperm cell is programmed to fertilize
either the egg cell or the central cell is an issue that has not
yet been resolved.
Recent work suggests that sperm cell dimorphism exists
in several species [2]. Similarly, a lot of new information
regarding the early events of fertilization has been
obtained from studies with isolated sperm cells and
female gametes. The first detectable cellular event that
20
Growth and development
Figure 1
A developing seed with embryo at the heart
stage. clz, chalazal end of the embryo sac;
em, embryo; en, endosperm; f, funiculus;
mi, micropylar end of the embryo sac;
s, suspensor.
en
em
clz
s
mi
f
Current Opinion in Plant Biology
takes place after gamete fusion is an increase in the
concentration of cytosolic Ca2+, caused by an influx of
cytosolic Ca2+. It is not clear, however, if this Ca2+ elevation
is sufficient to trigger egg activation and the initiation
of fertilization [3].
Embryo development
Once the egg is fertilized, the unicellular zygote makes a
progressive transition to become the embryo. The main
body of the embryo that is elaborated includes the apical
meristem, hypocotyl, cotyledons, root and shoot meristems,
and a radial pattern including the epidermis and layers of
conductive and vasculature tissues [4].
Mutational dissection has illuminated some of the early
events of embryogenesis. Many genes affecting embryogenesis have been isolated, including LEAFY COTYLEDON2
(LEC2) [5], GNOM [6], SHOOT MERISTEMLESS (STM)
[7], MONOPTEROS [8] and FACKEL [9]. LEC2 is likely
to be a transcriptional regulator that provides the correct
cellular environment for the initiation of embryo development. The first division of the embryo following
fertilization is asymmetric and produces an apical and a
basal cell. The smaller apical cell produces the bulk of the
embryo and the larger basal cell forms part of the root and
the suspensor. Among the pattern-formation mutants, only
those that have mutations in GNOM/EMB30 have defective
apical–basal polarity; the first division in these mutants
appears to be symmetrical. GNOM encodes a guanine
nucleotide exchange factor (GEF) that acts on an ADP
ribosylation factor (ARF)-type G protein [6]. In contrast
with mutations in GNOM/EMB30, a mutation in the FACKEL
gene specifically reduces the hypocotyl, causing an
embryo in which the roots seem to be attached to the
cotyledons. The FACKEL gene product is a sterol reductase
that is involved in lipid biosynthesis [9]. Another
mutant, schlepperless, defines the gene that codes for a
Chaperonin 60 alpha; the mutant phenotype indicates a
role for this gene during proper seed development [10].
During the transition from the globular to the heart stage
of embryo development, the cotyledon fate and number
are elaborated giving rise to two cotyledons in the dicot
embryo. In plants with mutations in the ALTERED
MERISTEM PROGRAMMING1 (AMP1) gene, the cotyledon number is variable with up to 30% of the seedlings
containing non-dicot seedlings. The mutant was found to
have an elevated level of cytokinin and a number of other
phenotypes, including partially de-etiolated growth,
precocious flowering and an elevated level of cyclin D3. The
AMP1 gene has recently been cloned [11•]. By homology,
the gene is a putative glutamate carboxypeptidase. This
result suggests that the product of the AMP1 gene modulates
the level of a signaling molecule that acts to regulate a
number of aspects of plant development. That signaling
molecule could be an as yet unidentified small signal
peptide. The altered cotyledon number and occasional
formation of multiple embryos in the seeds of amp1
mutants suggest that AMP1 plays a critical role during
pattern formation in plant embryogenesis.
Genetic and epigenetic processes in seed development Lohe and Chaudhury
Development of the endosperm
Proper development of the endosperm is essential for
growth of the embryo and the production of viable seed.
The endosperm derives from a single precursor cell, the
homodiploid central cell, which is the product of the
fusion of the two haploid polar nuclei. After fertilization,
the central cell nucleus continues to divide without
cytokinesis, forming a syncytium. The diploid embryo and
the triploid endosperm nuclei develop in unison, with
each appearing to be dependent on the other for correct
developmental progression. Unlike the embryo, which
progresses through several morphologically distinct stages
as it develops from a fertilized egg cell, the endosperm
nuclei form a syncytium without readily identifiable features.
With the exception of nuclei at the chalazal (posterior)
pole, cellularization of the endosperm has occurred by the
time the embryo reaches the heart stage [12].
Endosperm polarity
The embryo sac forms within the ovule and is the product
of the meiosis of the megaspore mother cell, from which
a single cell of four survives. This cell undergoes three
mitotic divisions to form a seven-celled, eight-nucleus
embryo sac (the central cell contains two polar nuclei)
(see [13] for review). The positions of the haploid nuclei
within the embryo sac are highly ordered, possibly to
facilitate the double fertilization event and subsequent
development. These positions may also provide the initial
cues for the development of endosperm polarity.
The cellularized endosperm has a substructure consisting
of different types of tissue. Analysis of a histone 2B::YFP
(yellow fluorescent protein) gene fusion during early seed
development showed that the syncytium is organized into
three distinct mitotic domains along the anterior–posterior
axis [14•]. The domains are characterized by synchronously
dividing nuclei whose mitotic activity is independent of
the mitotic activity in other domains. From the intensity
of labeling, it was suggested that nuclei in the chalazal
domain undergo endoreduplication, in contrast to the
other nuclei in the endosperm. Mutations in any of the
three FERTILIZATION INDEPENDENT SEED (FIS) genes
(see next section) disrupt endosperm polarization as well
as proliferation of endosperm nuclei [15•].
Mutational analyses are being supplemented with molecular
genetics to assist in the identification of genes that are
active in the endosperm and therefore in seed germination.
Screening of more than 10 000 Arabidopsis transgenic lines
carrying a β-glucuronidase (GUS) gene trap identified a
line in which GUS expression was restricted to the
micropylar end of the germinating seed [16]. A T-DNA
insertion into the TITAN (TTN) gene alters mitosis and cell
cycle control during endosperm development. Some ttn
alleles form giant polyploid nuclei with enlarged nucleoli.
TITAN is related to ADP ribosylation factors and is a
member of the RAS family of small GTP-binding proteins,
which regulate many eukaryote cell functions [17].
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A common emerging theme in plant development is that
hypothetical ancestral representatives of gene families with
a broad expression pattern may be co-opted for specialized
functions. These genes may include representatives of
multigene families, such as the MADS-box family, some of
which are expressed in the endosperm and in the
developing male and female gametophytes [18]. Similarly,
in maize, a member of the RbAp (retinoblastoma-associated
protein) sub-family of WD-repeat proteins is abundant
during endosperm formation and is also expressed in the
shoot apical meristem and leaf primordia of the embryo [19].
Gametophytic maternal-effect mutations
Mutations that affect endosperm proliferation have been
isolated in screens that looked for seed development
without pollination. Three mutations belonging to the
FIS class are female gametophyte mutations that result in
the spontaneous initiation of endosperm development in
the absence of fertilization. Each of the FIS genes (i.e.
FIS1/MEDEA, FIS2 and FIS3/FERTILIZATION INDEPENDENT ENDOSPERM [FIE]) controls at least three
functions in the developing endosperm: repression of genes
required for the initiation of endosperm development,
organization of the endosperm anterior–posterior axis, and
the number of divisions of the endosperm nuclei [15•]. In
addition, embryos inheriting a maternal copy of fis1 or fis2
rarely develop past the heart stage, and there is no embryo
development in fis3 mutants. As a result, seeds carrying a
maternal copy of a fis mutation shrivel and are rarely
viable. The fis mutants mimic at least some of the apomictic
processes, such as autonomous endosperm development,
but the mutations are not sufficient for progression to full
apomictic seed development.
The FIS genes have several interesting properties in
common. They all encode proteins that belong to the Polycomb
group (PcG) of general transcriptional repressors, which were
originally described in Drosophila. A multiplicity of PcG
complexes exists in Drosophila, and each complex contains
about 30 proteins that maintain a repressed transcriptional state
throughout the lifetime of the organism [20•]. FIS1/MEDEA
has sequence similarity with the protein encoded by the
Drosophila gene ENHANCER OF ZESTE (E[Z]) and
FIS3/FIE with that encoded by EXTRA SEX COMBS (ESC)
(see [21] for review). Although it was originally proposed
that FIS2 may correspond functionally to the Drosophila
protein HUNCHBACK [22,23], FIS2 shares sequence similarity
with the Drosophila protein SU(Z)12 [21]. In the yeast
two-hybrid assay, the Drosophila E(Z) and ESC proteins
interact physically [24,25]. It has recently been shown
that FIS1/MEDEA and FIS3/FIE also interact physically, but
FIS2 does not interact with either FIS1/MEDEA or FIS3/FIE
[26,27••,28]. The Drosophila E(Z) and ESC proteins are
members of a multiprotein PcG complex that is distinct from
other complexes containing PcG proteins [29]. PcG complexes
have not yet been identified in plants, and it has not yet
been determined whether FIS1/MEDEA and FIS3/FIE are
also restricted to a subset of PcG complexes in Arabidopsis.
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Growth and development
Figure 2
Current Opinion in Plant Biology
Scanning electron microscope image of a silique containing seeds
resulting from the crossing of a FIS3/fis3 heterozygote with pollen
carrying a METHYL TRANSFERASE1 (MET1) antisense construct.
The picture shows rescued large seeds carrying maternal fis3 and
small seeds carrying maternal FIS3.
The FIS genes share two additional properties. First, there
is no phenotypic effect on seed development when fis
mutations are introduced to the zygote paternally, in contrast
to the shrunken seed phenotype caused by the maternal
inheritance of fis mutations. A possible reason for this is that
the paternal genome is repressed in early seed development
(see section on ‘Epigenetic effects in endosperm
development’ below). Second, each of the FIS genes is
expressed in the developing endosperm.
The finding that genes in Arabidopsis encode proteins that
are homologous to the PcG class of transcriptional repressors
suggests that global control of gene repression evolved
before the separation of lines leading to plants and animals.
Elucidating the function of PcG proteins is continuing
to be an important topic in Drosophila research, and may
help us to understand the functions of Arabidopsis PcG
proteins such as FIS. Recently, two Arabidopsis homologs
of the trithorax-group (trxG) of transcriptional activators
have been discovered [30], suggesting that the similarities
in global transcriptional activation are conserved between
plants and animals.
Epigenetic effects in endosperm development
Before fertilization, the egg and central cell (i.e. the
endosperm precursor) can express only maternal genes
because they originate from female tissue. After fertilization,
the zygote and endosperm contain both maternal and
paternal genomes. Gene expression in both embryo and
endosperm is largely, if not entirely, maternal in origin until
three to four days after fertilization. The activity of 20
paternal genes was first detected only after that time [31••].
The reasons for the delayed activation of the paternal
genome, and the molecular mechanisms that govern
that delay, are unknown. It seems unlikely that suppression of the male genome is necessary for correct gene
dosage because in apomicts the unreduced embryo sac has
two maternal genomes and develops normally. The
transient silencing of the male genome has similarities
to whole-genome imprinting by inactivation of the male
genome in mealybugs [32]. Acetylation levels of histone H4
in the chromatin of mealybugs have been implicated in
the control of the differential activity of the male and
female genomes [32].
Evidence is emerging, however, that not all genes from
the paternal genome are inactive in early embryo and
endosperm development. Springer et al. [33] found that
the PROLIFERA gene is expressed early in development
in both the embryo and endosperm. Similarly, paternally
inherited FIS1/MEDEA is expressed in the embryo but
not in the endosperm [34]. Further work is needed to
establish whether the transitory inactivation of the paternal
genome includes all genes whose maternal counterparts
are expressed before about 80 hours of development.
The three FIS genes are active in the central cell before
fertilization and so are expressed maternally. FIS::GUS
fusions that are inherited paternally are not expressed in
the early endosperm [27••], supporting evidence that the
male genome is not activated until later in development
[31••]. These results could explain why a wildtype FIS
gene introduced via pollen does not rescue a maternal fis
mutation. Interestingly, the absence of paternal rescue of
fis1, fis2 and fis3 mutations can be overridden when
methylation is disturbed, either by a mutation in DECREASE
IN DNA METHYLATION1 (DDM1), a gene that encodes a
SWI2/SNF2-like chromatin remodeling factor [35,36], or
with a DNA METHYL TRANSFERASE1 (MET1) antisense
construct (Figure 2; [27••,28,37,38,39•]). These mutations
decrease methylation over most of the genome, although
the MET1 antisense construct does increase methylation in
some regions [40,41]. Rescue of fis1 and fis2 mutations
most likely results from the early activation of one or more
genes in the paternal genome. The paternal genes that
rescue fis ovules are not the wildtype FIS alleles because
rescue also occurs in the presence of a paternally inherited
fis mutation [27••,42].
Parent-of-origin effects such as these suggest the occurrence
of genomic imprinting [43]. Usually, such effects are
manifested early in development, and they can occur in
both plants and animals. Epigenetic mechanisms such as
DNA methylation or chromatin remodeling may be
responsible for imprinting because the effects can be
modified by genes that affect methylation (e.g. MET1)
[37], histone deacetylation (e.g. HISTONE DEACETYLASE
COMPLEX [HDAC]) [44–46] or chromatin remodeling (e.g.
DDM1 and MORPHEUS’ MOLECULE1 [MOM1]) [35,36,47••];
(see [48] for a recent review).
Genetic and epigenetic processes in seed development Lohe and Chaudhury
Epigenetic regulation may also play an important role in
silencing some genes in polyploids. Arabidopsis suecica is an
allotetraploid derived from A. thaliana and Cardaminopsis
arenosa. At least ten genes are silenced by hypermethylation
in A. suecica, and it has been suggested that epigenetic
regulation may be advantageous in the evolution of polyploid
species [49•]. In F1 hybrids between diploid species of wheat
and in the derived allotetraploids, alterations to cytosine
methylation occurred in about 13% of the loci examined [50].
Apomixis
Several thousand plant species can reproduce asexually to
generate seeds that are clones of the female parent. The
apomictic process begins in the ovule with a modified
meiotic division that results in an unreduced embryo sac
and an egg cell with an unreduced chromosome number.
Development of the egg into an embryo begins spontaneously (i.e. by parthenogenesis), even though fertilization
has not occurred. Alternatively, another unreduced cell can
take on the role of the egg cell, either in the embryo sac
(diplospory) or a sporophytic cell (apospory). Depending
on the type of apomixis, fertilization of the central cell can
occur normally and development of a triploid endosperm is
initiated (pseudogamy, the most common type of apomixis).
Alternatively, spontaneous endosperm development can
occur without fertilization and independently of embryo
development (see [51,52]). Apomixis would be a particularly
useful trait to introduce into crop plants, primarily because
of its ability to propagate seeds clonally.
The genes that repress embryo and endosperm development
until fertilization are of interest in understanding how
apomictic systems function at the molecular level. Sexually
reproducing Arabidopsis thaliana has been studied intensively
to identify genes that, when mutated, allow seed production
without fertilization. Although it has not been possible to
generate an apomictic mutant of Arabidopsis to date, mutations
in each of the three FIS genes described above result in
endosperm proliferation in the absence of fertilization.
Spontaneous endosperm development is a characteristic
of some modes of apomictic reproduction. Even if
fertilized, however, a fis mutant embryo fails to develop,
and upon maturity, the seeds of these mutants shrivel and
are usually inviable.
Normal seed development also requires the coordinated
growth of the silique tissues surrounding the ovule. An
enhancer insertion has been isolated that hyperactivates
the cytochrome P450 gene CYP78A9, resulting in large and
seedless fruit in the absence of pollination [53]. Another
gene that is essential for development of the silique is
FRUIT WITHOUT FERTILIZATION (FWF) [54]. Mutation
of this gene results in enhanced cell division, expansion of
the silique mesocarp layer and increased lateral vascular
bundle development in the absence of fertilization. These
genes are of interest in understanding the molecular
events of apomixis because, in apomicts, both silique and
seed development occur spontaneously without fertilization.
23
Identification of the genes controlling the decision
between the sexual and apomictic pathways is difficult
because most apomicts are polyploid and recombinants are
difficult to obtain and analyze. Recent studies have indicated
that apomixis may be the product of one or a small number
of genetic factors that are closely linked. The three essential
components of apomixis in Hieracium (i.e. apospory, and
autonomous embryo and endosperm development) segregate
as a single dominant Mendelian factor [55]. It is unclear
whether the factor is a single gene or a co-adapted gene
complex that is maintained by an absence of crossing over.
From crosses between sexual and apomictic dandelions
(Taraxacum) and analysis of the progeny, it was concluded
that diplospory and parthenogenesis (two ‘elements of
apomixis’) can be uncoupled [56]. Similarly, in Erigeron
annuus, factors controlling diplospory and parthenogenesis
are unlinked and inherited independently [57]. The authors
of this work on Erigeron annuus further concluded that the
parthenogenetic locus is likely to be a gametophyte recessive
lethal, and that the region responsible for diplospory
appears to be inherited on a univalent chromosome.
Conclusions
Proper development of an ovule into a mature seed depends
on the coordinated expression of many genes over a short
period of time. Discovering the identities of these genes
and elucidating their roles will require a combination of
genetics, and molecular and cell biology. The most
exciting recent development has been the complete
sequencing of the Arabidopsis genome [58], which will
facilitate enormously the identification of seed development
genes and the genetic pathways that they control.
Sometimes the homologies of an unknown Arabidopsis
gene with a known gene in well-studied organism can
provide clues to its function. For example, each of three
FIS genes that suppress endosperm proliferation in the
absence of fertilization has a clear homolog in the Drosophila
PcG class of genes. The PcG proteins function as global
repressors of gene activity by altering chromatin structure.
Chromatin remodeling genes, in addition to the PcG FIS
class, play a key role in seed development. These genes
include histone deacetylases, genes in the SWI2/SNF2
class and methyl transferase genes (see [59]). Recently, a
new plant genome research project entitled ‘Functional
genomics of plant chromatin genes’ has been initiated to
identify, mutate, and functionally analyze the several
hundred plant chromatin genes in maize and Arabidopsis
that contribute to chromatin-level control of gene
expression [60•]. Epigenetic effects are also involved in
early embryo and seed development. Study of epigenetic
effects, best carried out in Arabidopsis and maize, may lead
to new insights into the genetic mechanisms that control
seed development.
Acknowledgements
We thank Aneta Ivanova for the photograph of the embryo in Figure 1.
The financial support of the Graingene organization to ARL is gratefully
acknowledged.
24
Growth and development
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60. Chromatin at the University of Arizona.
•
http://www.chromdb.org/
Details of the Arabidopsis and maize genes involved in many different
aspects of chromatin structure and function are listed at this website. The
evolutionary relationships of these genes with other genes are also presented.