1 Department of Plant Sciences, University of Oxford, South Parks Road, Oxford
OX1 3RB, UK
2 Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853,
USA
3 Syngenta, Jealott's Hill, Bracknell RG12 6EY, UK
* Author for correspondence (e-mail: hugh.dickinson{at}plants.ox.ac.uk)
Accepted 30 June 2003
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SUMMARY |
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Key words: globby1-1, Endosperm development, BETL, Aleurone, Cell fate, Cell proliferation, Cytokinesis, Maize
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Introduction |
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The maize seed is composed of an embryo and a persistent endosperm, and is
proving an effective model system for the study of basic mechanisms of plant
development. The endosperm is a simple structure that originates as a triploid
central cell, the result of the fusion of the diploid central cell nucleus
with one of the two sperm cell nuclei
(Kiesselbach, 1949). A
succession of free-nuclear divisions results in the formation of the
single-celled syncytium, which bears strong similarities to the
Drosophila blastoderm. Cellularisation of the syncytium is initiated
by the formation of radial microtubule systems (RMS), which emanate from the
nuclear envelopes. Adventitious phragmoplasts are deposited at the points of
intersection, forming open-ended tube-like alveolar structures with the open
end facing the interior of the endosperm
(Brown et al., 1994
;
Olsen et al., 1995
).
Coordinated mitotic divisions of nuclei within alveoli are followed by
cytokinesis, thus giving rise to a single peripheral layer of cells and a new
layer of open-ended alveoli (Olsen,
2001
). Cellularisation proceeds in a centripetal manner, as this
cycle is repeated, until the endosperm becomes fully cellular.
The molecular systems regulating early endosperm development, including the
transition from syncytial to cellular stages, remain unclear. Studies in
Arabidopsis have shown that the process of endosperm cellularisation
shares multiple components with cytokinesis
(Sørensen et al.,
2002). However, the isolation of a small but significant number of
mutations which specifically affect either cytokinesis only in the embryo
(Assaad et al., 1996
) or
cellularisation of the endosperm (Liu and
Meinke, 1998
; Sørensen
et al., 2002
), point to the existence of additional mechanisms
operating in these two structures
(Dickinson, 2003
).
Unlike Arabidopsis, maize endosperm develops four structurally and
functionally distinct tissues aleurone, basal endosperm transfer layer
(BETL), embryo-surrounding region (ESR) and starchy endosperm (SE)
which are believed to be specified during the free-nuclear to cellularisation
stages of development (Becraft,
2001; Olsen,
2001
). A significant number of mutants with defective aleurone
development have thus far provided valuable insight into aleurone cell fate
and differentiation (Becraft and
Asuncion-Crabb, 2000
; Becraft
et al., 1996
; Lid et al.,
2002
; Shen et al.,
2003
). By contrast, no mutants with structural defects in either
the BETL or the ESR domains alone have been identified, and as a result,
little is known of the mechanisms regulating BETL and ESR formation
(Becker et al., 1999
;
Becraft, 2001
).
We describe here a recessive lethal mutant characterised by a distinctive globular embryo and endosperm morphology, termed globby1-1 (glo1-1). A key feature of the glo1-1 phenotype is aberrant nuclear and cell proliferation in the early syncytial and cellular endosperm, respectively, which to our knowledge has not been previously reported for monocots. As a consequence of these early abnormalities, localised disruptions in cell organisation of the BETL arise, and some cells with aleurone characteristics form ectopically in the regions of SE and BETL. These findings are inconsistent with a previous model for aleurone development, where it was proposed that aleurone cell fate was acquired through signalling from the maternal tissue to the endosperm surface, mediated via the CRINKLY4 receptor kinase (Olsen, 1998). Instead, our data point to the presence of other unknown developmental cue(s) operating within the starchy endosperm that confer aleurone cell identity.
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Materials and methods |
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For genetic analysis and mapping, plants were grown in fields at Cornell
University (Aurora, NY). Glasshouse grown plants were used for all other
analyses and either grown at Oxford or Jealott's Hill, under the following
regime: 16 hours day length (supplemented with metal halide lamps at 250
mmols, when required) at 22-28°C during the day, and at 16-20°C at
night. Humidity levels were set at 40-50% daytime and
60-70% at
night.
Histology
Plants heterozygous for the glo1-1 allele were self-pollinated to
recover mutants, which segregated as a single recessive Mendelian trait (data
not shown). For analysis of early endosperm developmental stages, kernels were
harvested from the mid portion of the ear and the remaining kernels were left
to mature to score the mutant phenotype. Fresh hand sections of mature kernels
were obtained after imbibing seeds on wet tissue for 2 days, and cutting
through the central longitudinal axis with a sharp blade. For phenotypic
descriptions of developing embryos, we followed nomenclature according to Abbe
and Stein (Abbe and Stein,
1954).
Microscopy
For epifluorescence microscopy, kernels were trimmed along the mediolateral
axis and fixed with FAA (5% formaldehyde, 5% acetic acid, 45% ethanol) for 15
minutes under a gentle vacuum. After infiltration, samples were left overnight
at 4°C in fresh fixative, dehydrated through a graded ethanol series,
cleared with Histoclear (National Diagnostics, Hull, UK) and wax embedded in
Paraplast Plus (Sigma, St Louis, MO). Sections were cut at 8-10 µm, mounted
on Superfrost Plus slides (BDH) and stained with DAPI
(Ruzin, 1999) at a final
concentration of 1-2 mg/ml in Vectashield (Vector laboratories, Peterborough,
UK). Slides were examined with a Zeiss Axiophot microscope using a 50 W
mercury lamp and the following filter set: 365 nm excitation, 395 nm dichroic
and 420 nm long-pass emission.
For light microscopy and transmission electron microscopy (TEM), tissue was
fixed overnight in 100 mM phosphate buffer (pH 7.5), with 4% paraformaldehyde
and 1% gluteraldehyde at room temperature. The material was then washed in
four 15 minutes changes of phosphate buffer and treated in 1% aqueous osmium
tetraoxide buffer, followed by dehydration in a graded acetone series and
embedding in epoxy resin. Thick sections were cut at 2 µm with a
tungsten-coated glass knife, affixed to pre-treated glass slides, stained with
Toluidine Blue O (Feder and O'Brien,
1968) and viewed under bright field optics using a Zeiss AxioPhot
microscope. Ultra-thin sections were cut using a diamond knife at 80 nm,
stained with uranyl acetate and lead citrate on a 2168 Ultrostainer (Carlsberg
System), and collected on 2 mm copper grids coated with Butvar B98 support
film. Grids were examined with a JEOL 2000EX TEM operating at 80 kV
accelerating voltage and negatives were digitally imaged after conventional
development.
mRNA in situ hybridisation
In situ hybridisation was performed on developing kernels at 7 and 10 days
after pollination (dap) according to Jackson
(Jackson, 1991), with minor
modifications. Briefly, kernels were trimmed along the medial-lateral axis and
immediately fixed in ice-cold FAA, dehydrated in an ethanol series, and
embedded in wax. Sections were cut at 10-12 µm and affixed onto pre-treated
Superfrost Plus slides (BDH). Riboprobes were labelled using the DIG RNA
labeling mix (Boehringer Mannheim, catalogue number 1175025) according to
manufacturer's instructions, and slides were hybridised overnight at 50°C.
Slides were viewed with a Zeiss AxioPhot microscope under DIC3-5 optics and
images were digitally recorded.
GUS marker gene analysis
Plants were genotyped for ß-glucuronidase (GUS) transcriptional
fusions via PCR using GUS-specific oligonucleotides (data not shown), and
backcrossed to glo1-1/+ plants for three successive generations.
Kernels were cut longitudinally and GUS was detected histochemically according
to a method previously described
(Jefferson et al., 1987), with
slight modifications. After staining at 37°C overnight, the material was
fixed in phosphate buffer and wax embedded, as described above. Sections were
cut at 12-15 µm and viewed under Nomarski optics.
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Results |
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The glo1-1 mutation disrupts early endosperm
development
To determine when in endosperm development GLO1 function is required,
serial sections of sibling kernels were compared from wild-type and
self-pollinated glo1-1/+ heterozygous plants between 2 and 4 dap. We
examined endosperms that ranged from syncytial, to cellularising to fully
cellular stages of development. In wild-type syncytia, nuclei are suspended in
a thin layer of cytoplasm surrounding the large central vacuole
(Fig. 2A). Remarkably, subtle
structural differences and anomalies in the distribution of nuclei were
observed in 25% of syncytia examined from segregating, but not wild-type,
ears (Fig. 2B). We interpret
these anomalies as indicating the lack of GLO1 in these syncytia. At a point
when the first cell layer forms in wild-type syncytia
(Fig. 2C), we noticed an
unusual overproliferation of cells confined to basal regions of endosperms
interpreted as glo1-1 (Fig.
2D). By 4 dap, wild-type endosperms were fully cellular and had a
rounded, conical shaped morphology (Fig.
2E), whereas putative glo1-1 endosperms often showed
signs of constrictions around the mid-apical region
(Fig. 2F) that became greatly
accentuated during later stages of development. Our current data thus indicate
that the glo1-1 mutation affects both nuclear divisions in the
syncytium and endosperm cellularisation (summarised in
Table 1), which dramatically
alter subsequent development of the mutant endosperm.
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Interestingly, cell wall projections or `stubs'
(Fig. 3F,I,J) and multinucleate
cells were occasionally observed in both embryo (data not shown) and endosperm
cells (Fig. 3D,I). Using TEM to
investigate further these possible cytokinesis-associated defects, we examined
wild-type and mutant kernels in the sub-aleurone region, as it is the most
actively dividing area in the 8 dap endosperm
(Olsen et al., 1999). In
wild-type cells, the protoplast surface was lined by regular aggregations of
ER (Fig. 4A), a feature absent
in the mutant (Fig. 4B,E).
Irregular deposits of cell wall material
(Fig. 4B) and the appearance of
striking cell wall `stubs' in the mutant, comprising all elements of the
normal cell wall (Fig. 4B,C),
were also observed in addition to multinucleate cells
(Fig. 4D). Furthermore,
cell-cell adhesion appeared to be poor in glo1-1, with interfaces
between cells frequently featuring gaps and lacunae
(Fig. 4E,F). Interestingly,
multivesicular bodies (MVBs) were commonly associated with irregular cell wall
thickenings, where they appeared to secrete their contents through the plasma
membrane (Fig. 4E). Strikingly,
large intercellular lacunae that characterise the SE region in glo1-1
endosperms were bordered by isodiametric cells with dense cytoplasms, which
were microscopically indistinguishable from aleurone cells
(Fig. 4F).
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The identity and positioning of aleurone cells is irregular in
glo1-1
To ascertain the positioning of aleurone cells in glo1-1
endosperms, we introgressed pVP1-GUS plants (J.F.G.-M., unpublished data) in
the glo1-1 background, thus enabling GUS detection of aleurone cells.
We examined 10 dap wild-type kernels and found GUS staining patterns confined
to aleurone cells (Fig. 6A)
However, in glo1-1 endosperms, non-uniform expression in the aleurone
was occasionally observed (data not shown) as was the unexpected presence of
GUS in few cells of the central SE region
(Fig. 6B). More frequently, GUS
staining was observed in the BETL of severe glo1-1 endosperms
(Fig. 6C). An additional unique
feature of the glo1-1 phenotype was the appearance of discrete cysts
encapsulated by extremely thick cell walls proximally located to peripheral
regions of the endosperm. By using the pVP1-GUS reporter, we found that the
layer of cells investing these ectopic structures also showed GUS staining
(Fig. 6D), while cells of the
interior of these structures contained well-defined starch grains and did not
stain for GUS (Fig. 6E). Thus,
our current data indicate that cells with many features of the aleurone are
ectopically formed throughout the glo1-1 endosperm.
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Discussion |
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glo1-1 is required for embryo and endosperm development
Using a range of microscopic techniques, in situ hybridisation and reporter
gene assays, we have shown that early cellularisation events in the
glo1-1 endosperm are abnormal, and, as a result, lead to alterations
in cell fate and subsequent differentiation of endosperm tissues. Examination
of mutant embryos revealed severe cellular disorganisation with few
recognisable tissues formed. Taken together, these findings suggest that the
GLO1 product is essential for the regulation of cellular morphogenesis in
maize embryo and endosperm tissues.
It is possible that the variation observed in endosperm and embryo phenotypes among homozygous glo1-1 mutants results from varying gene dosage. Through the use of a B-A translocation affecting the long arm of chromosome 1, additional copies of the glo1-1 wild-type allele were introduced in either the embryo or endosperm independently, but this failed to rescue the mutant phenotype, suggesting that variations observed in glo1-1 mutant phenotypes are not attributable to differences in gene dosage. These studies also demonstrated that the glo1-1 mutation affects development of the embryo and endosperm independently. Moreover, we showed that wild-type (hyperploid) embryos were unable to develop in the presence of defective (hypoploid) endosperms, suggesting that under the glo1-1 mutant condition, development of the embryo is strongly influenced by the endosperm.
Interestingly, we found glo1-1 to be allelic to the EMS-induced
mutant gm*-N1303 (data not shown), originally described as a
germless mutant by Neuffer and Sheridan
(Neuffer and Sheridan, 1980).
The variation in seed phenotype observed between the two alleles (data not
shown) may be attributable to differences in genetic background (e.g.
Gethi et al., 2002
;
Vollbrecht et al., 2000
):
gm*-N1303 was described in a vigorous hybrid background, whereas the
glo1-1 allele is in a standard inbred line.
The glo1-1 mutation predominantly affects nuclear
division
Early endosperm development in many angiosperms is characterised by nuclear
migration and suppression of phragmoplast formation
(Brown et al., 1999;
Brown et al., 1994
;
Olsen, 2001
), requiring tight
coordination between the cell cycle and cytoskeletal organisation. Phenotypic
analysis of the glo1-1 mutant suggests that glo1-1 may
affect nuclear division, perhaps through a deregulation, or partial loss of
control of the cell cycle. Aberrant cellular development is often localised to
small patches within glo1-1 endosperms and may occur at different
developmental stages, leading to the observed range of glo1-1 mutant
phenotypes. Thus, early proliferation of nuclei in the syncytium would induce
a severe kernel phenotype, whereas random proliferation in the cellular
endosperm would result in minimal disruption to tissue organisation. Cell wall
aberrations and other defects typically associated with cytokinesis (see
Söllner et al., 2002
)
were apparent in glo1-1 kernels. These aberrations have been reported
in several seed mutants, many of which have led to early developmental arrest
of embryos (Consonni et al.,
2003
; Söllner et al.,
2002
). This link between defective cell division and suppression
of embryo morphogenesis may account for the lack of pattern formation in
glo1-1 embryos.
The GLO1 gene product therefore seems necessary for both nuclear division
and cytokinesis in the developing seed. Evidence from Arabidopsis is
accumulating that the processes of mitosis and cytokinesis are intimately
interrelated (Dickinson, 2003;
Mayer et al., 1999
;
Sørensen et al., 2002
),
and it remains possible that GLO1 is involved only in an aspect of nuclear
division which, when disrupted, causes secondary or downstream effects on
cytokinesis. This is also true for TITAN3, which encodes an SMC2
condensin (Liu et al., 2002
).
Mutant endosperms lacking the functional TITAN3 protein develop giant nuclei
in the syncytial cytoplasm, which consequently results in defective
cellularisation (Liu and Meinke,
1998
). Clearly, the role of GLO1 remains to be determined and
efforts are now under way to clone the glo1 gene using a closely
linked Ac element in regional mutagenesis
(Brutnell, 2002
;
Singh et al., 2003
).
Basal structures are predetermined in the syncytial endosperm
Disruptions to the basal endosperm region are witnessed from an early stage
in glo1-1 mutants, i.e. during syncytial development, when the ESR
and BETL are thought to be specified
(Becraft, 2001;
Olsen, 2001
).
Our data showed reduced levels of ZmESR gene expression in
glo1-1 kernels, often restricted to small regions of the ESR. This
may be a consequence of either aberrant development of other endosperm
tissues, impacting indirectly on the ESR, or defective development of the
embryo caused by the glo1-1 mutation. It has been proposed that the
ZmESR gene products are involved in cross-talk between embryo and
endosperm (Opsahl-Ferstad et al.,
1997), as ZmESR expression is absent in spontaneously
occurring embryo-less mutants
(Opsahl-Ferstad et al., 1997
).
Our observations are consistent with the interpretation that correct
establishment of the ESR relies upon successful development of the embryo
which is of course highly defective in glo1-1 kernels.
In glo1-1 endosperms, the BETL tissue was often disrupted to
various degrees, and reduced levels of two BETL-specific transcripts were
recorded defects that are likely to result from abnormal syncytial
development caused by the glo1-1 mutation. As BETL identity is held
to be acquired via maternally derived diffusible signal(s) or morphogen
gradient(s) present in the syncytium
(Becker et al., 1999), it
follows that the irregularities in the syncytium induced by the
glo1-1 mutation may affect the ability of specific basal nuclei to
perceive or act upon these positional cues. Our data therefore suggest that
BETL specification is a fixed process, which occurs only during a short period
in syncytial development. Nuclei that fail to perceive this information
(either through the action of glo1-1 or otherwise) are thus unable to
differentiate as BETL cell types. Therefore, if the acquisition of BETL cell
fate were both irreversible and to occur within a narrow developmental window,
then `BETL identity' must be passed on in a lineage-dependent fashion (see
Fig. 7 for proposed model),
which, although is rare for plants
(Scheres, 2001
), is common in
animal systems such as Drosophila where positional cues in
the blastoderm lead to lineage-dependent differentiation
(Lawrence and Struhl, 1996
).
In support of this hypothesis, we found that the BETL was frequently patchy in
glo1-1 endosperms. Additionally, it has been reported that following
interploidy crosses, endosperms (with a paternal excess genomic contribution)
often contain tiny interspersed clusters of BETL cells
(Gutierrez-Marcos et al.,
2003
). As BETL cells are known to undergo a finite number of
divisions (Slocombe et al.,
1999
), these clusters may have originated from a single nucleus
that had initially perceived the developmental cues to assume BETL cell fate.
The fact that cells occupying basal positioning in the glo1-1
endosperm are not able to adopt BETL cell identity, together with evidence
that BETL cells are observed in apical regions of endosperms following
interploidy crosses (Gutierrez-Marcos et
al., 2003
), would imply that basal positioning is not strictly
necessary for BETL cell fate. This contradicts previous models for BETL cell
development, where, according to Becker et al.
(Becker et al., 1999
),
induction of transfer cells is thought to occur either via a signalling
mechanism or through mRNA transport present in the basal endosperm region.
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Little information exists of how aleurone fate is determined; however, the
simplest model holds that aleurone cell fate is acquired through a steep
ligand gradient away from the maternal cell wall
(Olsen et al., 1998), which is
perceived at the endosperm surface by the CRINKLY4 receptor kinase
(Becraft et al., 1996
). Based
on microscopic observations and GUS marker gene expression analysis, our data
unexpectedly revealed that aleurone-like cells have the ability to form from
within the glo1-1 endosperm. Thus, aleurone formation cannot
exclusively rely upon maternally derived signals. Instead, we suggest that, at
least in glo1-1 endosperms, aleurone identity might be acquired
internally, perhaps as a result of signals from within the SE itself.
Certainly, studies have demonstrated that the aleurone and SE cells can
develop from common progenitors and that neither cell type fates are
terminally determined, as aleurone formation is dependent on the constant
input of positional cues (Becraft and
Asuncion-Crabb, 2000
; Becraft
et al., 2002
; Lid et al.,
2002
). This developmental plasticity is further supported by our
observations: anthocyanin-like pigment (data not shown) and patchy
reporter-GUS expression patterns observed in glo1-1 basal endosperms
suggest that the undifferentiated cells often observed within the BETL during
early development are capable of assuming aleurone identity at later
stages.
glo1-1 endosperms thus contain two classes of aleurone-like cells,
the first are peripherally located and bounded on their `outward face' by a
thickened wall, as in wild-type kernels (data not shown). The second class of
cells, despite their location within the SE, are also bounded on one or more
faces by thickened cell walls. Assuming differences in permeability between
these thickened walls and others of the endosperm, it is possible that
short-range cues that trigger aleurone formation may accumulate in these
cells. This interpretation is also supported by emerging evidence that cell
fate in plants is specified by short-range cell-cell interactions, mediated
through signal transduction cascades, as occurs in Drosophila and
C. elegans (Irish and Jenik,
2001; Marx,
1996
).
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ACKNOWLEDGMENTS |
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