1 Section of Plant Biology, University of California, One Shields Avenue, Davis,
CA 95616, USA
2 National Horticultural Research Institute, RDA, I-Mok dong 475, Jang-An Gu,
Suwon, Gyeonggi-Do, 440-706 Republic of Korea
3 Institute of Molecular and Cell Biology, 61 Biopolis Drive, Singapore 138673,
Republic of Singapore
4 Department of Agronomy, University of California, One Shields Avenue, Davis,
CA 95616, USA
¶ Author for correspondence (e-mail: sundar{at}ucdavis.edu).
Accepted 25 November 2004
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SUMMARY |
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Key words: Arabidopsis thaliana, Female gametophyte, Embryo sac development, Fertilization, Maternal effect, Transposon insertion mutants
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Introduction |
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In the past few years, several efforts have been carried out in order to
identify gametophytic mutations. Although the study of several gametophytic
mutants allowed the identification of genes involved in embryo sac development
(Christensen et al., 2002;
Drews and Yadegari, 2002
;
Grini et al., 2002
;
Huck et al., 2003
;
Kwee and Sundaresan, 2003
;
Rotman et al., 2003
),
dissection of the female gametophyte developmental pathway into defined genes
and functions is still an unaccomplished goal. The screening of T-DNA
insertion lines for functionally important gametophytic genes has led to the
identification of several T-DNA-tagged gametophytic mutants in
Arabidopsis (Feldman et al., 1997;
Bonhomme et al., 1998
;
Howden et al., 1998
;
Christensen et al., 2002
).
However, the analysis of T-DNA mutant collections suggested that T-DNA
insertional mutagenesis can be problematic for the identification and
characterization of mutations that affect female gametophyte development
(Bonhomme et al., 1998
). As the
primary target of T-DNA integration in the mutagenesis protocols is the embryo
sac, plants in which female gametophyte function, especially the egg cell, is
severely compromised might be difficult to recover from T-DNA insertional
knockout lines (Ye et al.,
1999
; Bechtold et al.,
2000
). Additionally, chromosomal rearrangements induced by T-DNA
can also affect gametophytic transmission.
We have previously described a transposon-based gene trap system in
Arabidopsis, which resulted in the first molecular characterization
of a female gametophyte-specific mutation from plants
(Sundaresan et al., 1995;
Springer et al., 1995
). More
recently, this system was used for an analysis of 20 transposon insertion
mutants affecting male gametophyte development in Arabidopsis
(Lalanne et al., 2004
). As the
transposon insertions are generated in sporophytic cells and the large
majority of such insertion lines carry single insertions of the Ds
transposable element without rearrangements or truncations
(Sundaresan et al., 1995
), the
use of transposon insertion lines is well suited for the study of genes
involved in gametophytic development.
In this report we used our transposon population for a forward genetic screen to identify genes involved in female gametogenesis and early embryo development. Ds insertion lines (24,000) were screened for segregation distortion and more than 300 mutant lines that have defects in either female or male transmission efficiency were recognized. A large collection of mutants showing female transmission defects was studied. The phenotype of 130 female gametophytic mutants was characterized, and the genes disrupted in those mutants were identified, providing a wide-ranging assessment of the genes and functions involved in embryo sac development and the transition to the sporophytic generation.
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Materials and methods |
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Cleared whole-mount preparations
Flowers from different developmental stages with at least 20 ovules per
pistil were dissected and cleared overnight in Hoyers solution
(Liu and Meinke, 1998). The
dissected pistils were observed on a Zeiss Axioplan imaging 2 microscope under
DIC optics. Images were captured on an Axiocam HRC CCD camera (Zeiss) using
the Axiovision program (version 3.1).
Fluorescence staining of pollen tubes
For pollen tube staining, 10 pistils containing at least 20 ovules each
were manually pollinated and opened longitudinally 24 hours after pollination
for each mutant. The pistils were cleared in 10% chloral hydrate at 65°C
for 5 minutes and washed with H2O, softened with 5 M NaOH at
65°C for 5 minutes and washed again with H2O. The pistils were
then treated with 0.1% Aniline Blue in 0.1 M K3PO4
buffer pH 8.3 for 3 hours in darkness and washed with 0.1 M
K3PO4 buffer. The pistils were mounted in a microscope
slide using a drop of glycerol and carefully squashed under a cover slip. The
pistils were observed using a fluorescence microscope.
Image processing
All images were processed for publication using Adobe Photoshop CS (Adobe
Systems, San Jose, USA).
Molecular analysis of the sequences flanking the Ds-insertion
The sequences flanking the Ds element were isolated with TAIL-PCR as
described by Liu et al. (Liu et al.,
1995) and sequenced with an Applied Biosystems (ABI) sequencer.
The flanking sequences obtained were run against BLASTN to identify the
genomic location of the Ds element. Specific nested primers within the
identified genes surrounding the Ds insertion site were designed and used in
combination with Ds-nested primers in further experiments to confirm the
sequence obtained from the TAIL-PCR reaction.
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Results |
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Mutants presenting defects in fertilization
A large fraction of mutants was found to be affected during
post-pollination processes. Among these, we found 18 mutants that appeared
normal at stage FG7, but were found to be unfertilized, suggesting that the
mutation is affecting embryo sac functions such as pollen tube guidance or
fertilization. These mutants were called UNE mutants (for unfertilized embryo
sac mutants). When post-pollination stages were analyzed, some of these lines
showed two intact synergids, suggesting that ovules were not attracting pollen
tubes or that they failed to undergo synergid cell death
(Fig. 3C).
|
Mutants presenting defects in embryogenesis
An unexpectedly large number of mutants, represented by 62 lines (48%),
exhibited fertilized embryo sacs in which the embryo development was arrested
at the one-cell zygotic stage (Table
2, Fig. 3D). In
general, endosperm development was also arrested in these mutants, containing
one to four big nuclei (Fig.
3D). However, six of the zygotic-arrest mutants showed normal
endosperm development (not shown). To determine if these mutants were due to
defects in the female gametophyte, we crossed all 62 mutant lines as females
using wild-type plants as pollen donors and we examined the resulting progeny
by scoring the number of mutant embryo sacs per silique at 24 to 48 hours
after pollination. In all the cases, the ratio of mutant to wild-type embryo
sacs found was at least 35%, demonstrating that the zygotic arrest arises from
the female gametophyte and is not rescued by wild-type pollen.
Eight mutants were found arrested at later stages of embryo development, ranging from two-cell stage to globular and early heart stages (Fig. 3E). These mutants are characterized by a slight general delay in embryo sac development and fertilization (up to 12 hours), with various levels of endosperm development. When these lines were crossed as females using wild-type plants as pollen donors, the ratio of mutant to wild-type embryos in the silique was 35-50%, indicating that the embryo arrest phenotype in this class also arises from a mutation of the female gametophyte.
These mutants with defects in embryogenesis were called MEE mutants (for maternal effect embryo arrest).
Identification of the genes involved in female gametophytic mutations
Thermal asymmetric interlaced PCR (TAIL-PCR)
(Liu et al., 1995) was
performed to isolate the flanking sequence surrounding the Ds element using
Ds-specific primers and arbitrary degenerated primers. The chromosomal
location of the flanking sequences was determined by nucleotide BLAST searches
and further confirmed by PCR using gene-specific primers in combination with a
Ds element primer. Using the current annotation of the Arabidopsis
genome, two out of the 127 (1.5%) insertion sites sequenced showed to be
within a predicted gene (hypothetical protein), while 19 (15%) are within
genes encoding proteins with an EST match but without any protein match
(unknown proteins). The rest of the tagged genes were classified according to
their biological role or biochemical function as described by Lin et al.
(Lin et al., 1999
). A
distribution of the genes disrupted in the female gametophytic mutants is
shown in Fig. 4, while the
identity of the disrupted genes classified by phenotypic category can be found
in Table 3 (a fuller
description of the genes based on the current annotation in the TAIR database
can be found in Table S2 in the supplementary material). As unlikely, but
possible, excision and nearby insertions of the Ds element could have occurred
prior to the establishment of the stable insertion line, it is probable that
although the mutants are tightly linked to the Ds insertion, some of the
mutants are not tagged. The first class of mutant lines represents mutants
with obvious defects in the development of the embryo sac. A large fraction
(13%) of these mutants represented disruptions of protein degradation
pathways. However, these were restricted to mutants that are arrested during
the nuclear division phase of megagametogenesis or in mutants presenting
embryo sacs with abnormal nuclear numbers and positions
(Fig. 4A). Genes implicated in
secondary metabolism, transcriptional regulation and signal transduction were
also found to be involved both in the nuclear division phase and in the
nuclear fusion phase. A transmembrane receptor protein was identified (line
EDA 23, Table 3) as well as a
guanine nucleotide exchange protein (Line EDA 10,
Table 3). The latter protein is
an interactor of PRK1 (Park et al.,
2000
), which is a receptor-like kinase with serine/threonine
kinase activity isolated from petunia and involved in embryo sac development
(Lee et. al, 1997
). Genes
encoding proteins involved in electron-transferring systems (classified as
proteins involved in energy metabolism) were found disrupted in those mutants
exhibiting un-fused polar nuclei. Genes for calmodulin-binding proteins and
calcium-binding proteins were also found related to polar nuclei fusion (line
EDA 39 and EDA 34, Table 3).
Different classes of transcription factors were identified including
basic-helix-loop-helix-type transcription factors and CCAAT-binding factors
(Fig. 4A,
Table 3).
|
|
In the case of seven genes (At2g34790, At2g47470, At2g47990, At3g23440, At4g00020, At4g00310 and At4g13890), we found two independent insertion lines per gene, with the Ds element insertions at two different positions within the gene. Although, in general, similar or overlapping phenotypes were obtained when the terminal phenotype of each pair of mutant lines was compared, in the case of At3g23440 and At4g00020, the phenotype of the mutants was very different (Table 3). These divergences might arise from differences in the insertion sites of the Ds element into these genes, resulting in alleles that are not nulls but have different levels of residual expression. In the case of genes whose expression is required early for normal embryo sac development, as well as later for progression of embryogenesis, the observed differences in the terminal phenotypes might reflect such allelic variation. For example, two insertion mutants were recovered for the gene At3g23440: EDA 7 and MEE 37. Although for EDA 7 the insertion site is localized in the intergenic region downstream of the 3' UTR, in MEE 37 the Ds element is localized in the coding region of the gene.
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Discussion |
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Mutants arrested during embryo sac development
Within the category of mutants with embryo sac developmental defects, we
could find mutants arrested during the nuclear division phase of
megagametogenesis, mutants with abnormal nuclear numbers and positions and
mutants that became cellularized, but fail in polar nuclei fusion. An analysis
of the genes disrupted in these mutant lines showed that 13% of these encode
proteins involved in proteolysis, including components and regulators of
ubiquitin-mediated proteolytic pathways (At1g59680, At2g18080, At2g34920,
At2g48140, Table 3;
Fig. 4A; see Table S2 in the
supplementary material for all gene descriptions). However, genes in this
functional category were limited to mutants with defects in the nuclear
division phase of megagametogenesis, in accordance with the essential role of
proteolysis in cell division control (reviewed by
King et al., 1996). These
findings are also consistent with the isolation of two gametophytic mutants,
nomega (Kwee and Sundaresan,
2003
) and apc2 (Capron
et al., 2003
), in genes encoding components of the anaphase
promoting complex/cyclosome (APC/C), a large protein complex with ubiquitin
ligase activity. Receptor-protein kinases and known receptor kinase
interactors were also found to be involved during the nuclear division phase
of megagametogenesis (Fig. 4A;
At5g44700 and At1g01960, Table
3), as well as different classes of transcription factors
including basic helix-loop-helix-type transcription factors and CCAAT-binding
factors (Fig. 4A,
Table 3). An interesting
finding was the fact that genes encoding proteins located in endomembrane and
some of them involved in electron-transferring systems were found disrupted in
mutants that fail in polar nuclei fusion
(Fig. 4A; At1g70540, At1g72440,
At2g34790, At3g03810, At4g14040, Table
3). Previously, GFA2 - a member of the DnaJ protein involved in
oxidative phosphorylation and ATP production by the mitochondria - was found
to be required for the fusion of the polar nuclei in Arabidopsis
(Christensen et al., 2002
). As
a disruption of ATP-producing systems would cause pleiotropic effects on other
energy-requiring processes, not observed in these plants, other functions than
energy production can be disrupted in these mutants. As suggested for
gfa2 mutation, nuclear membrane fusion may require diffusible
factors, including hemes, cytochromes, carbon skeletons and thymidylates
(Mackenzie and McIntosh, 1999
;
Kushnir et al., 2001
;
Christensen et al., 2002
);
membrane contact may be required to shuttle lipids between different
compartments (Staehelin,
1997
).
Calmodulin-binding proteins and Ca2+-binding proteins were also
found related to polar nuclei fusion (At4g33050 and At4g00140,
Table 3). The involvement of
Ca2+ ions in membrane fusion has been reported earlier in somatic
protoplast fusion (Keller and Melchers,
1973). Furthermore, the requirement of Ca2+ ions has
previously been shown for the fusion of sperm with central cell protoplasts in
maize (Kranza et al., 1998
),
as well as in the fusion of sperm with egg cell protoplasts
(Kranz and Lorz, 1994
),
suggesting that Ca2+ ions might also be involved in membrane union
during polar nuclei fusion.
Female gametophytic mutants affecting the fertilization process
Fertilization in Arabidopsis requires controlled growth of the
pollen tube until it enters the micropyle to penetrate the female gametophyte
(Ray et al., 1997;
Shimizu and Okada, 2000
)
(reviewed by Higashiyama, 2003). From the analysis of pollen tube growth
pattern in Arabidopsis mutants defective in embryo sac development,
the female gametophyte was suggested to play a key role in pollen tube
guidance (Hülskamp et al.,
1995
; Ray, 1997
;
Shimizu and Okada, 2000
). The
pollen tube enters the female gametophyte by growing into one of the synergid
cells, where it ruptures at its tip releasing its contents. The synergid cell
penetrated by the pollen tube undergoes cell death, apparently at the time of
pollen tube discharge, or very shortly before pollen tube arrival
(Faure et al., 2002
;
Huck et al., 2003
). According
to previous observations, synergid cell death may be a requisite for normal
fertilization, decreasing the resistance to sperm cell migration during
fertilization (Willemse and van Went,
1984
; Huang and Russell,
1992
) and by facilitating the male gamete transfer from the pollen
tube to the egg and the central cell
(Russell, 1993
;
Fu et al., 2000
). An analysis
of the genes disrupted in our mutant collection with fertilization defects
showed a wide spectrum of functional categories
(Fig. 4B). Among these,
mitochondrial and endomembrane gene products, which are predominantly related
to electron transport systems, were found (e.g. At1g29300, At2g47470,
At3g03690, At3g10560; Table 3).
In mammals, the mitochondrial intermembrane space contains several cell death
activators that are released in response to a variety of cell death stimuli
(Green and Reed, 1998
;
Hengartner, 2000
;
Lam et al., 2001
). Although
much less is known in plants, several reports support a role for mitochondria
in cell death (Balk et al.,
1999
; Lacomme and Santa Cruz,
1999
; Navarre and Wolpert,
1999
; Stein and Hansen,
1999
; Sun et al.,
1999
; Balk and Leaver,
2001
). The release of cytochrome c from mitochondria has been
shown to be a primary cellular trigger for programmed cell death in plants
(Balk et al., 1999
;
Stein and Hansen, 1999
;
Sun et al., 1999
;
Balk and Leaver, 2001
).
However, several reports support a role for the endoplasmic reticulum during
programmed cell death in plants (Hayashi
et al., 2001
; Danon et al.,
2004
). In the present study, several genes related to cell death
pathways were isolated in mutants defective in synergid cell death. Among
these, proteins related to cytochome c maturity and with cytochrome P450,
another protein associated to plant cell death
(Godiard et al., 1998
) were
found (At2g47470 and At3g10560, Table
3). A gene encoding an oxysterol-binding protein was also detected
(At5g02100, Table 3),
suggesting that a pathway similar to the oxysterol-directed apoptosis, a well
known mechanism of cell death in animals
(Christ et al., 1993
;
Schroepfer, 2000
) and recently
reported associated to the hypersensitive response in barley
(Hein et al., 2004
) might be
involved in synergid cell death in the female gametophyte.
Additionally, a gene encoding an antioxidant enzyme was shown to be disrupted in a mutant with defects during the fertilization process (At3g63080, Table3). Antioxidant pathways might be active during this process, probably limiting the oxidative stress that cell-death signals, such as reactive oxygen species (ROS), can generate in the gametophyte.
Genes predicted to encode transcriptional factors were also found disrupted in lines with fertilization defects, both in pollen tube-attracting lines and in those lines that fail in pollen tube attraction. These genes belong to several different families of transcription factors, including the bHLH family, the MYB family and the bZIP family (e.g. At3g05690, At4g00050, At2g12940, At4g02590, At4g13640; Table 3) that might be responsible for the regulation of the specific processes required for fertilization, including pollen tube guidance and reception.
Female gametophytic mutants affecting embryo development
A large proportion (50.4%) of the gametophyte mutants isolated in our
collection exhibited embryo sacs that were fertilized, but with very early
arrest of embryo development (Fig.
3C). In general, delayed embryo sac development and a disruption
in endosperm development were also observed in this class of mutants. In all
the cases the mutation showed reduced transmission through the female
gametophyte, indicating that these lines are female-gametophyte mutants
displaying maternal effects on embryo and endosperm development. Maternal
effects can be caused by mutations in genes that are expressed during the
gametophyte development and whose gene products are required for embryo and
endosperm development. Examples of this kind of maternal gametophytic mutants
include the Arabidopsis capulet (cap1) and cap2
mutants (Grini et al., 2002),
the Arabidopsis proliferaI (prI) mutant
(Springer et al., 1995
;
Springer et al., 2000
) and the
maize maternal effect lethal (mell) mutant
(Evans and Kermicle, 2001
).
Maternal effects can be also caused by mutations in genes whose paternally
contributed alleles are imprinted. This is the case of the female gametophyte
mutants fie, mea and fis2, which present endosperm
development in the absence of fertilization
(Ohad et al., 1996
;
Chaudhury et al., 1997
;
Grossniklaus et al., 1998
).
The FIE, MEA and FIS2 proteins are related to the polycomb group proteins
(Ohad et al., 1996
;
Grossniklaus et al., 1998
;
Kiyosue et al., 1999
;
Luo et al., 2000
) and were
shown to be expressed in the central cell before fertilization as well as in
the developing endosperm (Luo et al.,
2000
). No fertilization-independent endosperm development was
observed in our mutant collection. On the contrary, endosperm development is
generally arrested in these lines, showing only one to four large nuclei
(Fig. 3C). These observations
are in accordance with the phenotype observed in prl and
mel1 mutants where the development of the embryo or endosperm is
severely affected very early in seed development
(Springer et al., 1995
;
Springer et al., 2000
;
Evans and Kermicle, 2001
). The
set of genes disrupted in these lines contains many potential signal
transduction components. Among them, receptor-like protein kinases,
phospholipase D and a response regulator of the two-component signal
transduction pathways were identified (At3g46330, At4g11850, At1g10470,
Table 3). Mutants defective in
early embryo development showed to have disrupted genes encoding transcription
factors that belong to different families such as MYB family, WRKY family and
TCP family (At2g21650, At2g34830, At3g15030, At1g25310,
Table 3;
Fig. 4C).
An interesting issue is whether the mutants with embryo and endosperm
phenotypes observed herein are due to a true maternal effect of the female
gametophyte (i.e. maternal factors) or due to delayed paternal genome
activation (Vielle-Calzada et al.,
2000). Although some of the phenotypes observed in mutants with
early arrest (1 cell zygote) of embryo development resemble those from female
gametophytic mutants exhibiting maternal effects
(Springer et al., 1995
;
Springer et al., 2000
;
Evans and Kermicle, 2001
),
much more detailed investigation will be needed in order to distinguish
between these two possibilities.
For those mutants exhibiting embryo development arrested at later stages
(from two-cell to globular stage), the defects might be ascribed to a
disrupted gene whose expression is required after fertilization or in specific
cells of the embryo. The phenotypes observed would be consistent with genes
described previously that are required to be zygotically transcribed from the
maternal allele only and regulated by genomic imprinting
(Vielle-Calzada et al., 2000).
The fact that some of these mutants showed a slight delay in embryo sac
development and fertilization might indicate that the wild-type genes are
expressed during the female gametophyte development, though they are not
essential for normal embryo sac development. The imprinted genes MEA,
FIS2 and FIE were shown to be expressed before pollination in
the female gametophyte. While MEA and FIS2 products are
found in the two polar nuclei and in the central cell nuclei, the FIE
product occurs in the central cell before pollination
(Luo et al., 2000
), consistent
with their proposed functions in the repression of endosperm development.
In summary, our analysis provides a comprehensive overview of the genes and functions that are required in the female gametophyte for its development into an embryo sac, and post-fertilization for the progression of embryogenesis in Arabidopsis. This study should serve as a basis for future studies addressed towards the elucidation of the molecular pathways involved in these crucial steps of plant reproduction.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/132/3/603/DC1
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ACKNOWLEDGMENTS |
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Footnotes |
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Present address: Cell Division LabTemasek Life Sciences Laboratory, 1
Research Link, The National University of Singapore, Singapore 117604,
Republic of Singapore
Present address: Temasek Life Science Laboratory, 1 Research Link, The
National University of Singapore, Singapore 117604, Republic of Singapore
Present address: State Key Laboratory of Plant Physiology and Biochemistry,
College of Biological Sciences, China Agricultural University, 2 Yuanmingyuan
Xilu, Beijing 100094, People's Republic of China
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