seminars in CELL & DEVELOPMENTAL BIOLOGY, Vol. 12, 2001: pp. 387–394
doi:10.1006/scdb.2001.0268, available online at http://www.idealibrary.com on
Cell fate specification in the cereal endosperm
Philip W. Becraft
In double fertilization, two different cells of the
megagametophyte are fertilized. One pollen sperm
fertilizes the egg cell to form the zygote and the other
sperm nucleus fuses with the two polar nuclei in
the central cell to yield the triploid endosperm. The
evolutionary origin of the endosperm is an interesting
problem with two competing century-old hypotheses
to explain its derivation (reviewed by Friedman 1 ).
One suggests that the endosperm is derived from
an altruistic second embryo produced by double
fertilization, while the alternative hypothesis proposes
that the endosperm is derived from an extension
of megagametophyte development. This issue is
pertinent to understanding endosperm development
because the developmental program is built on
the genetic platform inherited from the ancestral
predecessor of the endosperm. Thus, understanding
evolution will help us understand development and
vice versa.
The endosperm is a transitory tissue in many
species, particularly dicots such as Arabidopsis where
the cotyledons represent the major site of food
storage. In cereals, the endosperm is persistent,
contains several specialized cell types and is a
prominent feature of the mature seed. Despite the
very different fates of the endosperm in species
such as Arabidopsis and maize, early endosperm
development shows remarkable conservation.
The cereal endosperm contains three major cell
types. The bulk of the endosperm is composed
of the starchy endosperm or internal endosperm
cells, which accumulate starch and storage proteins.
Adjacent to the pedicel is a transfer layer, specialized
for nutrient uptake and transport from the maternal
tissues to the developing endosperm. An epidermal
layer, called the aleurone, covers the endosperm
and during seed germination, secretes hydrolytic
enzymes to digest the storage products in the starchy
endosperm.
Understanding how the identity of these different
cell types is specified during development has a
number of potential practical applications. For
While superficially simple, endosperm development is a
complex, dynamic process. Cereal endosperms contain
three major cell types: starchy endosperm, transfer cells
and aleurone. The localized accumulation of the END1
transcript in the syncitial endosperm suggests that signals
from the maternal placental tissue specify transfer cell
type early. Aleurone fate is plastic and requires the
continual input of positional cues to maintain cell identity.
Starchy endosperm appears to be the default cell type.
Mutant patterns suggest that a regulatory hierarchy
integrates endosperm development. Requirements for gametic
imprinting, maternal : paternal genome ratios and putative
chromatin modeling factors indicate the importance of
genomic control.
Key words: aleurone / development / endosperm / positional cues / transfer cells
c 2001 Academic Press
Introduction
The endosperm is well recognized for its importance
as food and feed, yet the many fascinating features of
endosperm biology are often overlooked. The
perception of endosperm as uninteresting is
perhaps in part because of its familiarity as a
foodstuff and part because of the ‘dead end’, often
transitory, nature of the endosperm. However, these
impressions belie the dynamism and many unique
features of endosperm development. Positional
cues, cell cycle modifications, genomic imprinting
and programmed cell death figure prominently in
endosperm development.
From the Zoology and Genetics Department and Agronomy Department,
Iowa State University, Ames, IA 50011, USA.
E-mail: becraft@iastate.edu
c
2001
Academic Press
1084–9521 / 01 / 050387+ 08 / $35.00 / 0
387
P. W. Becraft
into tube-like alveoli that remain open at their inner
face. The next cell division occurs periclinally and is
accompanied by cytokinesis to yield a fully cellular
peripheral layer and an alveolar internal layer.
This process repeats until the entire volume of the
endosperm is cellularized. With minor differences,
this early development is remarkably conserved in
plants as divergent as Arabidopsis, with a transitory
endosperm, and cereals.
Shortly after cellularization, the Arabidopsis
endosperm begins degenerating as the growing
embryo crushes surrounding cells. Only an epidermal
layer of endosperm, reminiscent of the cereal
aleurone, remains in the mature seed. 5 The function
of this cell layer is unknown. In cereals, the persistent
endosperm grows to a substantial size. Cell division
initially occurs throughout the cellular endosperm
and then becomes restricted to a cambial zone at the
periphery. More interior cells continue to grow by cell
enlargement as they accumulate starch and protein
bodies. This growth is accompanied by an increase in
genomic DNA content through endoreduplication.
As growth continues, programmed cell death (PCD)
initiates and progresses throughout the starchy
endosperm until only the aleurone cells remain
alive in the mature endosperm (reviewed by Young 7 ).
Castor bean contains a living endosperm that remains
attached to the cotyledons and serves as a storage
site for lipids. This endosperm undergoes PCD after
germination, 8 similar to the aleurone of cereals. 9
example, manipulating the transfer layer might
allow enhanced solute uptake efficiency, leading to
increased yield. The aleurone is relatively lipid rich
and so altering aleurone development could allow
seed composition to be manipulated. In addition,
the aleurone layer is rich in phytic acid, which is
detrimental in uncooked corn products because
of its ability to bind dietary Ca2+ and Zn2+ . It is
also a leading source of phosphorus in livestock
wastes, posing a serious water pollution problem.
Finally, the aleurone is the major source of amylase
in the malting process and is therefore of great
interest to the malt beverage industry. This paper will
highlight recent advances in our understanding of
how cell fates are decided during cereal endosperm
development.
Overview of endosperm development
There are three main types of endosperm
development, nuclear, cellular and helobial. Only
nuclear endosperm development will be considered
here as it occurs in most familiar plants including
cereals and Arabidopsis. Following fertilization of
the central cell, the primary endosperm nucleus
enters a period of free nuclear division. Although
the early endosperm is syncitial, the daughter nuclei
of early divisions migrate to relatively invariant
positions. Clonal analysis in maize showed that
following the first division, daughter nuclei occupy
lateral positions and give rise to the left and right
halves of the endosperm. 2 Products of subsequent
divisions give rise to predictable quarters and
eighths and so forth. These results demonstrate that
positional information is present within the early
syncitial endosperm, possibly preexisting within the
megagametophyte.
After a period of free nuclear division, the nuclei
occupy the peripheral cytoplasm surrounding a large
central vacuole and cytoskeletal arrays define nucleocytoplasmic domains (NCDs). 3–5 In cereals, syncitial
divisions appear synchronous 3 while in Arabidopsis
there appear to be mitotic domains. 6 Cellularization
ensues through a process of free cell wall formation
whereby unusual microtubule structures called
adventitious phragmoplasts form at the boundaries
between NCDs. The phragmoplasts direct membrane
vesicles containing cell wall constituents to the
growing points of the cell walls. Beginning at the
periphery and growing centripetally, cell walls grow
between non-daughter nuclei, separating the nuclei
Cell fate acquisition in cereal endosperm
As mentioned, the cereal endosperm has three major
cell types. In addition, there are regions or subtypes of cells within the starchy endosperm that are
histologically distinct or show specialized patterns of
gene expression. The organization of these cells in
the maize endosperm is illustrated in Figure 1.
Transfer layer
The transfer layer, also called ‘modified aleurone’,
is the first cell type to become histologically
differentiated during endosperm development,
becoming visible at approximately 6 days after
pollination (DAP) in maize. 10 These cells develop
extensive inward cell wall projections that increase
the area of plasma membrane by approximately 20fold [Figure 1(c); see Thompson in Reference 11 for
review]. Molecular evidence suggests that positional
388
Cell fate specification in the cereal endosperm
is also unknown. BETL1 was originally proposed
to have a structural function because of its tight
association with the cell wall but the small cysteinerich BETL1 and BETL3 peptides also show similarity
with defensins, suggesting possible antimicrobial
functions. However, SCR, the pollen determinant
of sporophytic self-incompatibility in Brassica, and
likely ligand for the S receptor kinase (SRK), shows
a similarity to defensins. 15 Thus it is also possible
that the BETL1 and 3 peptides function as signaling
molecules. BETL2 has recently been shown to be a
member of a small family of related peptides that
possess antifungal activity. 16 These peptides are
called BAP1-3 (basal layer antifungal proteins) and
BETL2 has been renamed BAP2.
Interestingly, a proper 2 : 1 maternal to paternal
genomic ratio is critical for transfer cell differentiation in maize. 17 The basal cells of tetraploid (2m : 2p)
endosperms fail to initiate cell wall ingrowths. In
addition, they show cytoplasmic disorganization and
abnormal inclusions in the cell wall matrix. Defects
in other parts of the endosperm, including necrosis
and failure of aleurone cell differentiation were
considered potential secondary effects of impaired
nutrient uptake. These effects of paternal genomic
excess suggest that a regulatory factor, critical for
transfer cell fate or differentiation, is differentially
imprinted in the pollen and the egg.
Consistent with the role of the basal transfer cells
in solute uptake, a cell wall acid invertase gene,
INCW1, is specifically expressed in these cells. 18
In fact, sugar sensing, and possibly flux, appear
to influence the development of maternal and
endosperm tissues. Endosperms mutant in mn1,
which codes for INCW2, cause degeneration of the
maternal placental tissues. 19,20 Since hydrolysis of
sucrose to hexose is a key step in sugar import to the
endosperm, the placental defects might result from
reduced flux. The reduced grain filling1 (rgf1) mutant
has a similar phenotype to mn1 but has apparently
normal sugar levels, suggesting the lesion may be
impaired sugar sensing. Both mn1 and rgf1 showed
morphologically normal basal transfer cells but in the
rgf1 mutant the levels of BETL1 and BETL2 (BAP2)
proteins were decreased. 21 This did not occur in
mn1 or several starch biosynthetic mutants. The basal
transfer cell-specific INCW1 transcript shows sugar
dependent post-transcriptional regulation. 22 Thus,
sugars influence gene expression in the basal transfer
cells. The differentiation of transfer cells in other
systems has been shown to be dependent on solute
transport (reviewed by Thompson 11 ), hence it would
B
A
p
a
sa
se
C
wp
D
em
embryo
pericarp
BETL
ESR
starchy endosperm
conducting tissue
aleurone
subaleurone
BETL1
Figure 1.
Cell types of the cereal endosperm. (a) A
diagrammatic representation of a developing maize kernel
in longitudinal section. The pericarp is maternally derived
tissue that covers the kernel and the embryo is the
other product of double fertilization. Everything else
is endosperm. (b) A histological section through the
peripheral crown region of a mature maize kernel, showing
starchy endosperm (se), subaleurone (sa), aleurone (a)
and the pericarp (p). (c) A histological section of the
basal transfer layer cells showing the extensive cell wall
projections (wp) associated with this cell type. The cells to
the lower right part of the figure belong to the maternal
placental tissue, which unloads the solutes taken up into
the endosperm (upper left) by the transfer cells. (d) In
situ hybridization showing the expression of the BETL1
transcript specifically in the basal transfer layer.
cues demarcate the presumptive transfer cell region
even prior to cellularization. In barley, the END1
transcript accumulates in the syncitial endosperm
over the placental crease, the region destined to form
transfer cells. 12 It was hypothesized that a signal from
the placenta induces the expression of END1 and that
this transcript may be anchored to the cytoskeleton
in this region of the syncitial endosperm. The
function of this gene is currently not known. In
maize, transcripts for four genes, BETL1-4, are
transiently expressed in the transfer cells during
early- to mid-stage endosperm development. 13,14
Whether these genes have a developmental function
389
P. W. Becraft
peripheral cell layer adapts a starchy endosperm
fate. Therefore the wild-type DEK1 gene product
is required for the perception or response to the
positional cues that specify aleurone cell fate. In a
transposon-induced dek1 mutant, revertant sectors
as small as a single cell allowed aleurone cell
development. Because the revertant cell’s ability to
perceive or respond to the positional cues was not
restored until near the end of active cell division, the
positional cues that specify aleurone identity must
still be present late in development. Furthermore,
starchy endosperm cells in a peripheral position
remain competent to respond to those signals.
In a reciprocal experiment, Ds induced chromosome breakage was used to cause the loss of the
wild-type DEK1 gene in a dek1/DEK1 heterozygote,
uncovering the mutant allele in sectors. 28 Cells within
mutant sectors assumed starchy endosperm identity,
even in late sectors as small as two cells. Because
aleurone cells were clearly recognizable at earlier
stages of development, the late loss of DEK1 gene
function caused peripheral cells to lose aleurone
identity and switch fate to starchy endosperm. This
demonstrates that the positional cues that specify
aleurone identity are also required to maintain
it. Such transdifferentiation events demonstrate
that cell fate specification is a continual process
and highlight the developmental plasticity of the
endosperm.
The maize crinkly4 mutant causes mosaic aleurone
development. In regions that lack aleurone, the
peripheral cells develop as starchy endosperm. This
fate switch of peripheral cells indicates that CR4
is involved in the aleurone cell fate decision. The
identification of CR4 as a receptor-like kinase 27
suggested the exciting possibility that CR4 may be
the receptor for the positional cues that specify
aleurone identity. 24,27 CR4 is not specific to the
aleurone but rather regulates a wide variety of
cellular developmental processes in the plant and
endosperm, suggesting that the function is analogous
to a growth factor receptor, where a widespread
signal(s) regulates various responses in a contextdependent manner. 30 A region in the extracellular
domain shows similarity to the ligand-binding domain
of the mammalian tumor necrosis factor receptor
(TNFR) family suggesting that the ligand for CR4
(i.e. the putative positional cue for aleurone identity)
may be related to TNF. 27 Unfortunately, the TNF
family shows poor primary sequence conservation, 31
creating difficulty for sequence based strategies for
identifying TNF-related molecules as potential CR4
not be surprising if source–sink relationships were
important for inducing the formation of endosperm
transfer cells.
Aleurone
During cellularization, the periclinal division that
first sets aside a cellular peripheral cell layer gives
rise to two daughter cell lineages with different
fates; the internal daughter has the invariant fate
of producing only starchy endosperm cells while
the peripheral cell layer will produce aleurone cell
initials. Because of the different fates of the daughter
cells, this early periclinal division has been called
a formative division 4,23,24 and it was commonly
believed that the aleurone formed a separate
cell lineage from the starchy endosperm. 10,25–27
However it is clear, at least in maize, that this initial
cell division is not a determinative event but the
daughter cell fates remain plastic through late stages
of endosperm development. 28 This conclusion
is based on endosperm cell lineage analysis and
developmental genetic analysis of the DEK1 gene
function, required for aleurone cell fate.
Cell lineage analysis was conducted in maize
endosperm using a technique similar to that of
Barbara McClintock. 2 A chromosome breaking
Ds transposon was used to simultaneously mark
starchy endosperm and aleurone by uncovering
the wx and C1 markers, respectively. 28 The size
of a sector indicates the relative time during
development when an event occurred; small sectors
occurred late in development because there were
few cell divisions following the event. Small sectors
containing both aleurone and starchy endosperm
were observed, indicating that both cell types could
be derived from a common precursor at late stages of
development. These results show that the aleurone
cell lineage is not distinct but that the peripheral
cell layer contributes cells internally to differentiate
as starchy endosperm throughout development.
This is consistent with a report from wheat that
describes the redifferentiation of aleurone cells
to starchy endosperm following an aleurone cell
division that contributed a daughter cell internally. 29
That starchy endosperm cells can be derived from
the aleurone cell lineage implies that position, not
lineage, determines endosperm cell fate.
The question of aleurone cell fate determination
was further addressed by examining unstable dek1
alleles. 28 dek1 is a recessive mutation in which
aleurone differentiation fails to initiate and the
390
Cell fate specification in the cereal endosperm
starchy endosperm fate instead of aleurone. In a
sense then, the question of how starchy endosperm
cell fate is specified comes down to the question of
how the endosperm, with the same genetic makeup
as the embryo except for the 2 : 1 maternal : paternal
genomic ratio, is specified. This, in turn returns
to the question of the evolutionary origins of the
endosperm. More work is required before these
questions can be answered.
ligands. Genetic analysis suggests that a hierarchy
of genetic functions is involved in the specification
and differentiation of aleurone cells. 28 Genetics may
represent the most viable approach to identifying the
CR4 ligand and will help identify other components
of the CR4 signal transduction system.
Maternal : paternal genomic ratio is also important
for aleurone development because tetraploid
endosperm fails to differentiate an aleurone layer. 17
It was not reported whether tetraploidy caused the
peripheral endosperm cells to switch fate to starchy
endosperm or simply to differentiate incompletely.
Whether this particular effect was due to a regulatory
factor that controls aleurone development being
differentially imprinted in male and female gametes
or was a secondary consequence of disrupted transfer
cell differentiation cannot be determined at present,
but there is ample evidence that imprinting is
critical for aleurone development. Imprinting of
anthocyanin factors in the aleurone is a well-known
phenomenon 32,33 and Dappled mutants that disrupt
aleurone development only show phenotypes when
inherited through the female, suggesting they are
imprinted. 34
Among the molecular markers that have been
identified for the aleurone are lipid transporters, 35–37
Myo-inositol-1-phosphate synthase, 38 a defenserelated gene, 39 and in certain genotypes of maize,
genes of the anthocyanin biosynthetic pathway. 34,40
Specialized regions within the starchy endosperm
Within the starchy endosperm are several specialized
regions of note. These include the subaleurone, the
‘embryo surrounding region’ (ESR) and conducting
zone (Figure 1). The subaleurone is a cambial zone
of active cell division. Cells are small and generally
contain small amyloplasts in the early stages of starch
accumulation. 29,45 The specific expression of the
basic leucine zipper transcriptional factor, RISBZ1,
in the aleurone and subaleurone 46 suggests that the
subaleurone might in fact possess a distinct identity.
However, this might also merely reflect a phase in
starchy endosperm cell development because there is
a progression of cells passing from the subaleurone
to mature regions of the endosperm as new cells are
added to the periphery during endosperm growth.
Cells surrounding the embryo have a distinct
morphology, with compact size and dense cytoplasm
containing extensive rough endoplasmic reticulum. 47
This morphology suggests a synthetic function,
possibly producing substances to be taken up by
the suspensor of the developing embryo. Three
genes called ESR1-3 are specifically expressed in
this region. 48,49 The function of these genes is
unknown but the promoters of all three drive GUS
expression in the ESR indicating that regulators
function specifically within this region. 48 The pattern
is fairly static in the endosperm, initially surrounding
the whole embryo but as the embryo proper grows
up and out of this region, the ESR is left surrounding
just the suspensor.
It has been reported that developing maize
endosperm contains a column of elongated
conducting cells extending through the central
core of the endosperm from the transfer layer to
near the apex. 17 These cells are called prismatic
cells in barley 50 and are believed to transport solutes
throughout the kernel. Like the transfer cells and
aleurone, this conducting tissue failed to differentiate
in tetraploid endosperms, suggesting either that a
determinant is differentially imprinted in male and
Starchy endosperm
Starchy endosperm cells constitute the bulk of
the cereal endosperm and represent the major
storage site for starch and protein. Despite
intensive study, it is surprising that no genetically
defined regulatory factors for starchy endosperm
development have been isolated. Even among the
various metabolic pathways to storage product
accumulation, surprisingly few regulators have been
isolated. Mutants are known in many of the enzymes
of the starch biosynthetic pathway but no genetic
regulators have been identified. OPAQUE2 is the
only genetically defined regulator of storage proteins
that has been isolated. 41,42 The paucity of identified
genetic regulators in these systems suggests that
there is either a high degree of redundancy or that
such mutants are lethal, perhaps present in the many
non-descript defective kernel (dek) mutants. 43,44
Available evidence suggests that starchy endosperm
represents the default cell type because loss-offunction mutants cause peripheral cells to adapt a
391
P. W. Becraft
female gametes or that the activity of the transfer
layer is required for the differentiation of this tissue as
well. No molecular markers have yet been reported
for this tissue but two barley mutants specifically
eliminate this tissue from the endosperm. 50
Pattern formation in the endosperm
From the array of specialized cell types and molecular
markers, each with their characteristic spatial patterns
within the endosperm, it is apparent that pattern
formation is an essential component of endosperm
development. Analysis of mosaic aleurone mutants
of maize (Figure 2) suggested that endosperm
development is integrated by at least two systems. 28
Mosaic patterns of mutants that affect early steps of
the aleurone development have a strong tendency
for showing defective aleurone differentiation
preferentially in the abgerminal crown region,
reflecting a gradient from the silk scar region of the
kernel. The source of the positional information for
this gradient is not the embryo because a mutant that
altered embryo position did not alter the distribution
of the mosaic pattern. This pattern is reminiscent
of the anterior–posterior pattern shown by the
MEA, FIS2 and FIE genes of Arabidopsis. 51,52 These
putative chromatin-modeling factors are required
in the megagametophyte to inhibit endosperm
development until fertilization and are involved
in establishing axial pattern in the developing
endosperm (see accompanying article by Chaudhury 53 ). It will be interesting to see whether the
homologs of these genes are involved in establishing
the germinal–abgerminal pattern in maize.
Mutants that affect later stages of aleurone
differentiation show blocky patterns of mosaicism,
first in large patterns, then in smaller patterns,
suggesting that development is somehow integrated
in progressively smaller fields. What these fields
represent, whether the limits of a diffusible
factor, symplastic fields, or something else, and
the functional meaning of these fields in endosperm
development are questions that will be answered
as the genes that show these mutant patterns are
isolated.
(a)
(b)
(c)
Figure 2. Representative mutants showing the characteristic patterns for each class of mosaic aleurone phenotype. 28
The dark regions of the kernels contain anthocyanin
specifically in the aleurone. The light regions show areas
that fail to accumulate anthocyanin because aleurone
differentiation is perturbed. The highly characteristic
patterns of mutants in multiple genes suggest they reflect
an underlying developmental pattern. (a) The bareback*
mutant showing the germinal–abgerminal pattern also
observed in crinkly4 and dek1 mutants. (b) A collapsed2-o12
kernel showing a large blocky pattern of mosaicism, also
typical of several Dap and Msc mutants. (c) The white2-dek21
pattern consisting of small patches of aleurone.
Summary
cycle is highly modified, first to allow nuclear division
without cytokinesis, then to allow an unusual cytokinesis involving free cell wall growth in the absence of
nuclear division. Later the cell cycle is modified again
to allow endoreduplication in the starchy endosperm
The picture that emerges of endosperm development
is of a dynamic system, containing several novel
features. In early stages of development, the cell
392
Cell fate specification in the cereal endosperm
cells before they undergo programmed cell death.
The establishment of pattern and the specification of
cell fates are also very complex, involving positional
cues, signal transduction, chromatin modeling
factors, genomic imprinting, probable interactions
with maternal tissues and metabolic signaling.
Understanding how all these processes are integrated
to allow the development of a functional endosperm
will require much more research but the potential rewards of being able to improve seed composition, not
to mention the intellectual gratification, are ample.
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Development and functions of seed transfer cells. Plant Sci
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molecular markers from the barley endosperm coenocyte
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Acknowledgements
The author is grateful to members of the Becraft
lab for helpful discussions and critical reading of
the manuscript. Figures 1(c) and (d) were kindly
provided by Richard D. Thompson, Max Plank
Institute, Koln, Germany. Work in the author’s lab
is supported by grants from the National Science
Foundation (IBN-9604426) and the Department of
Energy, Energy Biosciences (DE-FG02-98ER20303).
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