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First published online June 23, 2006; 10.1105/tpc.106.040824 The Plant Cell 18:1862-1872 (2006) © 2006 American Society of Plant Biologists AGL80 Is Required for Central Cell and Endosperm Development in Arabidopsis[W]Department of Biology, University of Utah, Salt Lake City, Utah 84112-0840 1 To whom correspondence should be addressed. E-mail drews{at}bioscience.utah.edu; fax 801-581-4668.
During plant reproduction, the central cell of the female gametophyte becomes fertilized to produce the endosperm, a storage tissue that nourishes the developing embryo within the seed. The molecular mechanisms controlling the specification and differentiation of the central cell are poorly understood. We identified a female gametophyte mutant in Arabidopsis thaliana, fem111, that is affected in central cell development. In fem111 female gametophytes, the central cell's nucleolus and vacuole fail to mature properly. In addition, endosperm development is not initiated after fertilization of fem111 female gametophytes. fem111 contains a T-DNA insertion in AGAMOUS-LIKE80 (AGL80). FEM111/AGL80 is a member of the MADS box family of genes that likely encode transcription factors. An AGL80–green fluorescent protein fusion protein is localized to the nucleus. Within the ovule and seed, FEM111/AGL80 is expressed exclusively in the central cell and uncellularized endosperm. FEM111/AGL80 expression is also detected in roots, leaves, floral stems, anthers, and young flowers by real-time RT-PCR. FEM111/AGL80 is required for the expression of two central cell–expressed genes, DEMETER and DD46, but not for a third central cell–expressed gene, FERTILIZATION-INDEPENDENT SEED2. Together, these data suggest that FEM111/AGL80 functions as a transcription factor within the central cell gene regulatory network and controls the expression of downstream genes required for central cell development and function.
The central cell within the female gametophyte (Figure 1A ) is essential for seed formation in angiosperms. Angiosperms undergo double fertilization, in which the female gametophyte's haploid egg cell and diploid central cell both become fertilized. After fertilization, the egg cell and central cell give rise to the seed's diploid embryo and triploid endosperm, respectively. Endosperm is important for the seed because it provides nutrients and other factors to the developing embryo during seed development and, in some species, to developing seedlings after germination (Olsen, 2004  ).
During female gametophyte development, a haploid megaspore undergoes three rounds of mitosis without cellularization to produce an eight-nucleate structure. Cellularization results in a seven-celled gametophyte containing three antipodal cells at the chalazal pole, one egg cell and two synergid cells at the micropylar pole, and a central cell in the center. The largest of these cells is the central cell, which inherits two nuclei referred to as the polar nuclei. In Arabidopsis thaliana and many other species, the polar nuclei fuse to form the diploid central cell nucleus (secondary nucleus) and the antipodal cells degenerate before fertilization. Thus, in the mature female gametophyte of Arabidopsis, the central cell occupies most of the volume of the embryo sac, is located at the chalazal pole, contains a large vacuole at its chalazal pole, and has a relatively large nucleus at its micropylar pole (Figure 1A) (Willemse and van Went, 1984 ; Huang and Russell, 1992; Yadegari and Drews, 2004).
Little is known about the molecular processes controlling the specification and differentiation of the central cell during female gametophyte development. During the last 10 years, many genes required for female gametophyte development have been identified and analyzed, including FERTILIZATION-INDEPENDENT ENDOSPERM (FIE) (Ohad et al., 1996
Expression-based screens have identified a battery of central cell–expressed genes, including Zea mays MADS1 (Heuer et al., 2001 Here, we report the identification of a mutant, fem111, that has defects in central cell and endosperm development. We show that the fem111 mutant has a lesion in the AGAMOUS-LIKE80 (AGL80) gene. FEM111/AGL80 encodes a type I MADS domain–containing protein, which likely functions as a transcription factor. In the context of the ovule, FEM111/AGL80 is expressed exclusively in the central cell. We also show that FEM111/AGL80 is required for the expression of DME, indicating that FEM111/AGL80 is upstream of this gene in the central cell gene regulatory network. Thus, FEM111/AGL80 appears to encode a regulatory molecule controlling central cell differentiation during female gametophyte development.
fem111 Affects the Female Gametophyte but Not the Male Gametophyte We previously identified a large collection of female gametophyte mutants using the criteria of segregation distortion and reduced seed set (Yadegari and Drews, 2004 ). One of these mutants, fem111, is described here. As summarized in Table 1 , fem111 exhibited segregation distortion in self-crosses (P < 0.001), suggesting that the gametophyte generation is affected. To determine whether the fem111 mutation affects the female gametophyte, we crossed fem111/FEM111 females with wild-type males and scored the number of fem111/FEM111 and FEM111/FEM111 progeny. As shown in Table 1, transmission of the fem111 mutation was significantly reduced compared with that of the wild-type allele (P < 0.001). In addition, siliques resulting from this cross exhibited reduced seed set (47% aborted ovules; n = 300) (see Supplemental Figure 1 online). These observations indicate that fem111 affects the female gametophyte.
To determine whether the fem111 mutation also affects the male gametophyte, we crossed fem111/FEM111 males with wild-type females and scored the number of fem111/FEM111 and FEM111/FEM111 progeny. As shown in Table 1, transmission of the fem111 mutation through the male gametophyte was not significantly different from that of the wild-type allele (P > 0.5), indicating that the male gametophyte is not affected. As shown in Table 1, the penetrance of the fem111 mutation is 100% in the female gametophyte. As a consequence, we were not able to isolate homozygous mutants and, thus, were not able to evaluate whether this mutation affects the sporophyte generation.
fem111 Affects Central Cell Development In fem111 female gametophytes, all four cells were present (the antipodal cells degenerated normally), and the egg cell and synergid cells appeared indistinguishable from those of the wild type (Figures 1D and 1E). By contrast, the central cell in fem111 female gametophytes exhibited two defects: the nucleolus and vacuole both were smaller than those of the wild type (Figures 1D and 1E).
We analyzed female gametophytes at earlier developmental stages to determine why the nucleolus and vacuole are small in fem111 central cells. We first analyzed these structures in the wild type. The central cell is first formed during stage FG5. During this stage, the central cell contains the two polar nuclei that fuse to form a single nucleus (secondary nucleus) and a large vacuole that occupies most of the volume of this cell. The central cell's nucleolus is relatively small just after fusion (stage FG6) and enlarges as the female gametophyte matures (stages FG6 and FG7), until it reaches a diameter of
To analyze the maturation of the central cell's nucleolus and vacuole in fem111, we used CLSM to observe the female gametophytes within fem111/FEM111 pistils from flower stage 12c, which contain female gametophytes at stages FG4 to FG6 (Christensen et al., 1997 ). Female gametophytes at stages FG4 and FG5 exhibited no phenotypic variation (n = 113 female gametophytes), indicating that migration and fusion of the polar nuclei occur normally in fem111 female gametophytes. By contrast, two distinct populations of female gametophytes were observed at stage FG6. One population (54%) was indistinguishable from the wild type in all features, including the sizes of the central cell's vacuole and nucleolus (Figure 2). In the second population (46%), the central cell's vacuole and nucleolus had reduced size (Figure 2). Together, these data indicate that the phenotype conferred by fem111 first becomes apparent soon after fusion of the polar nuclei and includes defects in nuclear maturation and the maintenance of vacuole size.
fem111 Affects Endosperm Development
As with the wild type, fem111 female gametophytes at 18 h after pollination contained a degenerated synergid cell and a single-celled zygote (Figure 1F). In the wild type, egg cells and zygotes are distinguished by several structural features (see the legends of Figures 1B and 1C) (Faure et al., 2002 The absence of endosperm at 18 h after pollination could be attributable to either a failure to form endosperm or a delay in endosperm development. To distinguish between these possibilities, we analyzed fem111 seeds at 40 h after pollination. In wild-type seeds at this time point, endosperm consists of >50 nuclei and the embryo is at the globular stage (Figure 1H). By contrast, in fem111/FEM111 siliques, 45% of seeds at this time point did not contain endosperm nuclei (n = 100 seeds). Of those seeds lacking endosperm, 76% had a zygote-like structure (Figure 1I); in the remaining 24%, it could not be determined whether a zygote-like structure was present because the embryo sacs were collapsed. This result suggests that the failure to form endosperm is not the result of a delay in endosperm development. The data presented above suggest that the structural changes associated with the central cell are induced by pollination. To explore this possibility further, we emasculated stage 12c flowers, waited 42 h (corresponds to 18 h after manual pollination), and fixed ovule tissue for confocal analysis. The autofluorescence associated with the central cell in fertilized fem111 ovules was not observed in fem111 female gametophytes of unpollinated pistils at this time point (Figure 1G), indicating that these structural changes require pollination. Together, these observations indicate that the central cell in fem111 female gametophytes is not competent to give rise to endosperm, even when fertilized with wild-type pollen.
FEM111 Encodes the AGL80 MADS Domain Protein
This gene corresponds to AGL80, which encodes a type I MADS domain protein (Parenicova et al., 2003
The T-DNA is inserted immediately after the second nucleotide in the predicted open reading frame and is associated with a 6-bp deletion in the coding sequence. This observation suggests that fem111 is a null allele. However, we were not able to confirm this prediction because we were unable to obtain a homozygous line (Table 1), which precluded the analysis of FEM111/AGL80 expression in fem111 mutants.
FEM111/AGL80 Is Expressed in the Central Cell during Female Gametophyte Development
As shown in Figure 4B
, at the terminal developmental stage (stage FG7), AGL80-GFP expression was detected exclusively in the central cell. Figure 4B also shows that the AGL80-GFP fusion protein was localized to the nucleus, consistent with its predicted function as a transcriptional regulator. To determine whether FEM111/AGL80 is expressed at earlier developmental stages, we analyzed expression in flowers at stage 12c, which contain both uncellularized (stages FG4 and early FG5) and cellularized (late stage FG5 and stage FG6) female gametophytes (Christensen et al., 1997
To determine whether FEM111/AGL80 is also expressed in developing seeds, we analyzed AGL80-GFP expression at 8 to 72 h after pollination. During this period, AGL80-GFP expression was detected exclusively in the endosperm (Figure 4C). During endosperm development, AGL80-GFP expression was strongest in young seeds and diminished gradually at progressively older stages; expression was not detected in seeds older than 3 d after pollination. In reciprocal crosses with plants homozygous for the AGL80-GFP construct and the wild type, expression was detected only when the reporter construct was present in the female parent.
To analyze FEM111/AGL80 expression elsewhere in the plant, we performed real-time RT-PCR with RNA from various organs. Consistent with the expression of AGL80-GFP in the female gametophyte and endosperm, we detected FEM111/AGL80 expression in ovaries and young siliques (Figure 5
). In addition, expression was detected in roots, leaves, stems, young flowers, and anthers (Figure 5). Our results are consistent with previous studies showing expression of AGL80 in leaves, stems, siliques, and anthers (Parenicova et al., 2003
FEM111/AGL80 Is Required for the Expression of DME and DD46 during Central Cell Development The data presented above suggest that FEM111/AGL80 functions as a transcription factor within the central cell and controls the expression of downstream genes required for central cell development and function. To test this further, we analyzed the expression of the DME, FIS2, and DD46 central cell–expressed genes in fem111 mutants. We analyzed the expression of DME–ß-glucuronidase (GUS), FIS2-GFP, and ProDD46:GFP in fem111/FEM111 and wild-type plants.
In wild-type female gametophytes, DME-GUS (Choi et al., 2002
In wild-type female gametophytes, ProDD46:GFP (DD46 corresponds to gene At1g22015) is expressed in both the central cell and the synergid cells (Figure 6C) (J.G. Steffen, J. Macfarlane, and G.N. Drews, unpublished data). By contrast, in fem111/FEM111 plants, the reporter was expressed in the synergid cells but not in the central cell (Figure 6D) in approximately half of the ovules (Figure 6E). Together, these data indicate that FEM111/AGL80 is required for the expression of DME and DD46 but not FIS2 during central cell development.
FEM111/AGL80 Encodes a Type I MADS Domain Protein FEM111/AGL80 is a member of the MADS box family of genes. MADS box genes have been identified in a diverse array of organisms, including plants, animals, slime molds, algae, and fungi (Robles and Pelaz, 2005 ; Tanabe et al., 2005). Genes in this family encode proteins that contain a structurally conserved MADS domain through which they dimerize (Pellegrini et al., 1995) and bind DNA (Hayes et al., 1988; Treisman, 1992; Tilly et al., 1998). MADS domain–containing proteins function as transcriptional regulators that control many developmental processes in plants, including flowering time, specification of floral meristem identity, fruit development, specification of floral organ identity, and seed coat development (Irish, 2003; Robles and Pelaz, 2005).
Two groups of MADS box genes, referred to as type I and type II (including the MIKC type), are present in plants, animals, and fungi and are probably the result of a duplication event that occurred in a common ancestor (Alvarez-Buylla et al., 2000
In contrast with the type II genes, little functional characterization has been performed with the type I genes in plants. Functional information is available for only one type I gene, PHERES1 (AGL37), which is a target of the FIE/FIS2/MEA/MSI1 polycomb complex and is thought to play a role in endosperm development (Kohler et al., 2003b
FEM111/AGL80 Is Required for Central Cell and Endosperm Development
After pollination, endosperm fails to form from fem111 female gametophytes. Instead, the central cell cavity becomes filled with highly fluorescent material that resembles a degenerating synergid cell (Figure 1F), suggesting that fertilization triggers a cell death process in fem111 central cells. Degeneration of fem111 central cells does not occur in the absence of pollination (Figure 1G), suggesting that it may be induced by the fertilization process. At present, we do not know whether the central cell actually becomes fertilized, because the degeneration process was extremely rapid and prevented the observation of sperm nuclei in the central cell (Faure et al., 2002
We also detected AGL80-GFP expression in the endosperm (Figure 4C). Consistent with this observation, AGL80 expression was previously detected within the endosperm by in situ hybridization analysis (Parenicova et al., 2003
Fertilized fem111 egg cells give rise to zygote-like structures (Figure 1I). FEM111/AGL80 is not expressed in the egg cell (Figure 4B) or the developing embryo (Figure 4C). These observations suggest that the embryo development defect results from the lack of endosperm. Zygote-like structures were also observed in autonomously developing mea (fis1) and fis2 seeds (Chaudhury et al., 1997
Using real-time RT-PCR, we detected FEM111/AGL80 RNA in roots, stems, leaves, young flowers, and anthers (Figure 5). With the exception of the root expression, these results are consistent with those of a prior analysis of this gene (Parenicova et al., 2003
Models for FEM111/AGL80 Function
Growth Conditions Arabidopsis thaliana seeds were sterilized in chlorine gas and germinated on plates containing 0.5x Murashige and Skoog salts (Sigma-Aldrich M-9274), 0.05% MES, 0.5% sucrose, and 0.8% Phytagar (Life Technologies). Ten-day-old seedlings were transferred to Scott's Redi-Earth and grown under 24-h illumination.
Plant Transformation
Segregation Analysis
For self-cross analysis, fem111/FEM111 plants were allowed to self-pollinate, progeny seeds were collected, and the number of resistant and sensitive progeny was scored. Resistant progeny from the self-cross could be either heterozygous or homozygous for the fem111 T-DNA insertion. To distinguish between these possibilities, resistant plants were grown and seed set was scored; all resistant plants exhibited
Confocal Analysis
Analysis of GFP Expression Patterns
Gene Identification
Molecular Complementation Plants heterozygous for the fem111 allele and hemizygous for the rescue construct at a single locus were allowed to self-cross. The progeny seeds were germinated on growth medium containing 50 µg/mL kanamycin, and the number of resistant and sensitive plants was scored. We observed 77 kanamycin-resistant progeny and 43 kanamycin-sensitive progeny. Plants homozygous for the fem111 allele and homozygous for the rescue construct were identified by having progeny seeds that were 100% kanamycin-resistant and 100% hygromycin-resistant. These plants had seed set indistinguishable from the wild type.
Cloning the FEM111/AGL80 cDNA We identified the 5' and 3' untranslated sequences with RACE using the First Choice RLM-RACE kit (Ambion). For 5' RACE, the gene-specific outer primer was 5'RACE-Outer#2 (5'-AAGAGCGAGAGTTCGTGTACCTTC-3') and the gene-specific inner primer was 5'RACE-Inner#2 (5'-AAGAATCGTTGGAAATGTAAGCAAG-3'). For 3' RACE, the gene-specific outer primer was AGLSEQp4 (5'-AGCGACAGAAACTTTGAGGAGA-3') and the gene-specific inner primer was AGLSEQp6 (5'-TCGCAGGATTGAGATTTTAC-3'). This analysis showed that FEM111/AGL80 contains 5' and 3' untranslated regions of 51 and 109 bp, respectively.
Sequence Analysis
Generating AGL80-GFP This construct was introduced into Arabidopsis plants as described above, and transformed plants were selected by germinating seeds on growth medium containing 50 µg/mL hygromycin. The expression patterns reported in Results are derived from the analysis of 10 single-insert AGL80-GFP lines. Plants homozygous for both the AGL80-GFP construct and the fem111 T-DNA insert (as determined by kanamycin and hygromycin selection of progeny) had 100% seed set.
Real-Time RT-PCR RNA was extracted from these tissues using the Qiagen RNeasy kit according to the manufacturer's instructions (www.qiagen.com). DNA contamination was removed from samples using the Ambion TURBO DNA-free DNase kit according to the manufacturer's instructions. After DNase treatment, RNA samples were repurified using the Qiagen RNeasy kit according to the manufacturer's instructions. Aliquots of RNA (1 µg) were reverse-transcribed using the RETROscript kit (Ambion) according to the manufacturer's instructions.
For real-time RT-PCR, PCR was performed using the Roche FastStart DNA Master SYBR Green I master mix (www.roche.com) in a volume of 10 µL on a Roche LightCycler system. The PCR mixture consisted of 0.5 µL of cDNA, 0.5 µM primers, and 1x master mix. In every real-time RT-PCR run, ACTIN2 was used as an internal control to normalize for variation in the amount of cDNA template. The PCR primers used were MP1-1F (5'-GACTCTTTGTGGCATCACTGC-3') and MP1-1R (5'-CCTCAAAGTTTCTGTCGCTTTC-3'). The PCR program consisted of a first step of denaturation and Taq activation (95°C for 5 min) followed by 45 cycles of denaturation (95°C for 15 s), annealing (60°C for 15 s), and extension (72°C for 10 s). To determine the specificity of the PCR, the amplified products were subjected to melt curve analysis using the machine's standard method. The reported values are averages of four independent trials (two biological replicates and two technical replicates). We calculated relative expression levels as follows. We first normalized AGL80 transcript levels relative to a standard (ACTIN2) using the formula
Analysis of DME-GUS, FIS2-GFP, and ProDD46:GFP in fem111 Female Gametophytes To analyze promoter:reporter constructs in the fem111 mutant background, we crossed fem111/FEM111 plants as males with plants homozygous for the reporter construct. To identify F1 plants containing the fem111 T-DNA allele, PCR was performed with the primers RBMP2 (5'-GCGTTACCCAACTTAATCGC-3') and FEMCR1 (5'-ATCTTATAATACCAAATCCTACT-3'). Plants heterozygous for the fem111 T-DNA insertion and hemizygous for the reporter construct were allowed to self-cross. Progeny from the self-cross were then scored for the fem111 T-DNA insertion by PCR, as described above. One-quarter of these plants should also be homozygous for the reporter construct. To identify these plants, we made use of the fact that all reporter constructs were inserted into vectors conferring kanamycin resistance. Offspring containing the fem111 T-DNA allele were then allowed to self-cross. Seeds from this cross were plated on medium containing 50 µg/mL kanamycin, and the ratio of kanamycin-sensitive to kanamycin-resistant seedlings was scored. Plants that produced 100% kanamycin-resistant progeny were determined to be homozygous for the promoter:reporter construct.
Analysis of reporter expression was performed at stage FG7. Flowers were emasculated at stage 12c (Christensen et al., 1997
Accession Numbers
Supplemental Data
We thank Ramin Yadegari and members of the Drews laboratory for critical review of the manuscript. We thank Yeonhee Choi and Ramin Yadegari for the DME-GUS and FIS2-GFP lines, respectively. We thank Ed King and the Department of Biology Microscopy Facility for guidance with the microscopic analysis. This work was supported by Department of Energy Grant DE-FG02-04ER15620 to G.N.D. and USDA Cooperative State Research, Education, and Extension Services Fellowship 2004-35304-14931 to M.F.P.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Gary N. Drews (drews{at}bioscience.utah.edu).
[W] Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.106.040824. Received January 4, 2006; Revision received May 9, 2006. accepted May 19, 2006.
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TOP
ABSTRACT
INTRODUCTION
6 µm at the terminal developmental stage (stage FG7) (
CT = CT(AGL80) – CT(ACTIN2). Real-time RT-PCR was performed with cDNAs from anthers harvested from flowers at stages 10 to 13 (A; 
, Mß, and M
(Parenicova et al., 2003
2 test. 
