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First published online July 14, 2006; 10.1105/tpc.106.041277 The Plant Cell 18:1887-1899 (2006) © 2006 American Society of Plant Biologists Arabidopsis ABA INSENSITIVE4 Regulates Lipid Mobilization in the Embryo and Reveals Repression of Seed Germination by the Endosperm[W]Department of Biology, Centre for Novel Agricultural Products, University of York, York YO10 5YW, United Kingdom 1 To whom correspondence should be addressed. E-mail iag1{at}york.ac.uk; fax 44-1904-328762.
Regulation of seed germination requires coordinate action by the embryo and surrounding endosperm. We used Arabidopsis thaliana to establish the relative roles of embryo and endosperm in the control of seed germination and seedling establishment. We previously showed that endospermic oil reserves are used postgerminatively via gluconeogenesis to fuel seedling establishment and that lipid breakdown is repressed by abscisic acid (ABA) in embryo but not endosperm tissues. Here, we use RNA amplification to describe the transcriptome of the endosperm and compare the hormone responses of endosperm and embryo tissues. We show that the endosperm responds to both ABA and gibberellin but that ABA in particular regulates nuclear but not plastid-encoded photosynthetic gene expression in the embryo. We also show that ABA INSENSITIVE4 (ABI4) expression is confined to the embryo, accounts for the major differences in embryo response to ABA, and defines a role for ABI4 as a repressor of lipid breakdown. Furthermore, ABI5 expression in the endosperm defines a second region of altered ABA signaling in the micropylar endosperm cap. Finally, embryo and endosperm ABA signaling mutants demonstrate the spatial specificity of ABA action in seed germination. We conclude that the single cell endosperm layer plays an active role in the regulation of seed germination in Arabidopsis.
Arabidopsis thaliana seeds exhibit a common form of dormancy known as coat induced or coat enhanced. These terms describe the important role of tissues surrounding the seed in the maintenance of dormancy. In Arabidopsis, the availability of mutants has focused attention on the role of the testa in coat-enhanced dormancy, but in general, the term covers all tissues surrounding the embryo, which include the endosperm and pericarp where present (Bewley and Black, 1994  ). The key role of these embryo-surrounding tissues in the control of germination is neatly demonstrated by the fact that damaging or removing them breaks dormancy and stimulates embryo growth in many species.
The endosperm in the mature Arabidopsis seed consists of a single cell layer resembling the cereal aleurone. Until recently it was believed to be of little importance once the seed has reached maturity (Berger, 1999
In tobacco and tomato (Solanum lycopersicum), both of which contain comparatively large endosperms in the mature seed, the endosperm is a major focus in efforts to understand the control of germination. In addition to its function as a storage tissue, in these species and others, the endosperm has been shown to exert control over germination by secreting cell wall loosening enzymes that weaken the mechanical resistance of the micropylar endosperm cap to radicle protrusion (reviewed in Bewley, 1997b
Seed dormancy and germination are strongly under the control of phytohormones and their responses. Genetic analysis of seed germination in Arabidopsis has revealed that ABA and gibberellins (GAs) are crucial regulators (Bentsink and Koornneef, 2002
We have shown previously that embryo and endosperm tissues can be successfully isolated from mature Arabidopsis seeds after the seed coat has undergone programmed cell death (Penfield et al., 2004
Differential Gene Expression in the Embryo and Endosperm during Germination To probe in detail the phytohormonal responses of the embryo and endosperm during germination, we undertook global expression profiling using the ATH1 gene chip 1 d after transfer to 22°C after 3 d of cold stratification. At this time point, shortly after radicle emergence, the percentage decrease in storage lipid is significantly more advanced in endosperm compared with embryo tissues, whereas transcriptional activity of various storage lipid–related genes as determined by promoter-reporter gene activity is detectable in both (Penfield et al., 2004 , 2005). Additional transcriptome data sets were generated from seeds that were stratified for 3 d and transferred to 22°C for 1 d, having been maintained throughout on media containing either 20 µM ABA or 20 µM paclobutrazol (PAC). We harvested embryo and endosperm tissue in triplicate samples and compared gene expression.
First, we noticed that the number of probe sets (12,190) found to be expressed in the endosperm using the ATH1 chip was very similar to that in the embryo (13,121). These numbers closely resemble the number of genes found to be expressed in other Arabidopsis tissues, excluding pollen (Schmid et al., 2005
Using highly stringent criteria, we identified embryo- and endosperm-specific transcripts during germination. To qualify, genes must be scored as present in all three replicate samples in the expressed tissue and must be called absent in the nonexpressed tissue in at least two of the three replicate experiments. Genes whose function has been previously addressed in other published work and fulfill these criteria are shown in Supplemental Table 1 online. The Arabidopsis extensin-like gene EPR1 is known to be expressed solely in the endosperm during germination and was used previously as a marker for endosperm identity (Dubreucq et al., 2003 ; Penfield et al., 2004). This control gene was found to be expressed highly in endosperm samples yet was absent in the embryo (3749.8 ± 122.6 versus 25.2 ± 4.5; see Supplemental Table 1 online), indicating the high fidelity of the microarray data. The highest expressed genes were consistent with known endosperm functions and included various putative proteases, transporters, and cell wall–modifying enzymes. One of these, EXPANSIN2 (EXP2), has been described as an early GA-induced transcript during seed germination (Ogawa et al., 2003). An EXP2:GUS (for ß-glucuronidase) fusion confirmed that its expression was indeed endosperm specific (data not shown). Comparison with online data sets suggested that the expression of this gene is not detected in any other tissues except for low expression in seeds after imbibition (www.genevestigator.ethz.ch). Given the high endosperm expression of EXP2 in our data sets, we concluded that EXP2 is a marker for endosperm tissue in nondormant imbibed or germinating seeds. One notable gene, MYB101, was found to be highly expressed in endosperm tissue yet absent from the embryo. MYB101 is a homolog of the cereal GAMYB transcription factor required for the strong induction of amylase expression in the endosperm during germination (Gubler et al., 1995). Endosperm expression of MYB101 has been shown previously (Gocal et al., 2001); however, this study also detected expression in the embryo. Embryo-specific transcripts included known chloroplast-associated genes and those associated with shoot apical meristem function (see Supplemental Table 1 online).
To understand the functional specialization of embryo and endosperm tissues, we compared the two transcriptomes using Metabolic MapMan (Thimm et al., 2004
Prominent among bins highly expressed in the embryo relative to the endosperm are those for transcription, amino acid activation, and protein synthesis (Table 1). As the amino acids used for early postgerminative protein synthesis are likely derived from seed storage proteins, this suggests an embryo tissue more specialized for reserve use than the endosperm. The number of observable ribosomes in embryo and endosperm cells correlates strikingly with protein synthesis–related gene expression, with embryo cells containing approximately five times more ribosomes than the endosperm (Figures 1C and 1D).
Transcriptomic Response of Embryo and Endosperm Tissues to ABA
To understand which processes were under embryo-specific ABA regulation, we used MapMan to identify functional categories of genes that were ABA regulated in the embryo but not the endosperm (see Supplemental Figure 2 online) and using the Wilcoxon rank sum test identified bins of genes regulated by ABA in the embryo, endosperm, or both (Table 2 ). Several bins were found to be significantly changed in gene expression by ABA treatment in the embryo but not the endosperm. Strikingly, this group of bins was dominated by genes involved in major plastid functions: these included the photosynthetic light reactions, the Calvin cycle, tetrapyrolle synthesis, and fatty acid synthesis. In fact, genes encoding components of the photosynthetic reaction centers were downregulated by ABA in the embryo yet actually upregulated by ABA in the endosperm. A number of bins representing secondary metabolism were also ABA downregulated in the embryo only. The role of ABA in the inhibition of chloroplast development in young seedlings is well known; however, ABA had no significant affect on the expression of chloroplast-encoded gene expression in either embryo or endosperm (Figures 2C and 2D). Therefore, ABA influences chloroplast metabolism exclusively through the regulation of the nuclear genome.
Several MapMan bins were also found to be significantly affected by ABA in both tissues. Prominent among these were groups of cell wall–related enzymes, such as pectinesterases, pectate lyases, and cell wall–modifying enzymes (expansins and xylogucan endotransglycosylases; Table 2). This suggests that the cell wall is a major target of ABA signaling in both the embryo and endosperm and that this role of ABA is mediated by signal transduction components expressed in both tissues. ABA-upregulated bins in both embryo and endosperm include those representing oleosins and aspartate degradation. We found no major targets of ABA repression that were unique to the endosperm. Hence, the endosperm is both qualitatively and quantitatively different in its ABA response compared with the embryo. Previously, we used reporter gene studies to show that ABA affects the transcription from a number of promoters of key storage reserve mobilization-related genes (Pritchard et al., 2002 ; Penfield et al., 2004). In the latter study, the temporal induction of reporter gene activity at 1 d after imbibition correlated strongly with endogenous enzyme activities. However, other published data on steady state transcript levels reported that these transcripts were already elevated in imbibed seeds (Rylott et al., 2001). Our study also shows that reserve mobilization is not dramatically regulated at the level of steady state transcript levels in either the embryo or endosperm by ABA and that transcripts are already accumulated at high levels in nongerminating PAC-treated seeds (see Supplemental Table 2 online). This agrees with previous published array work that showed that the transcription of key enzymes in ß-oxidation and the glyoxylate cycle is already induced in late seed development (Schmid et al., 2005).
Comparing this data set to the AtGenExpress ABA treatment experimental data (http://www.weigelworld.org/research/projects/resources/microarray/AtGenExpress/; 24 h imbibed seeds with and without 30 µM ABA and 7-d-old seedlings with or without 3 µM ABA for 3 h), we were able to identify 52 ABA-induced probe sets representing 51 genes whose expression was affected twofold or greater by ABA treatment in all four experiments (embryo, endosperm, seed, and seedling; see Supplemental Table 3 online). This same analysis revealed eight probe sets twofold or greater repressed by ABA in each experiment. This included many known stress- or desiccation-responsive genes and a number of transcription factors. These can be considered a core set of genes that respond to ABA independently of seed tissue type. Comparing this core set with the dry seed data sets of the wild type, abi4-1, and abi5-1 of Nakabayashi et al. (2005)
ABA and GA Synthesis and Response in the Embryo and Endosperm
At the transcript level, the endosperm also expresses many genes required for ABA synthesis and catabolism, suggesting that the endosperm might also be able to make and degrade ABA. This has been further demonstrated by a recent report that two carotenoid cleavage dioxygenase isoforms are expressed in the endosperm of maturing seeds and are required for dormancy (Lefebvre et al., 2006 ). One of these, NCED9, was still expressed in an endosperm-specific manner in germinating seeds (Table 3). Multiple genes have been shown to control and affect the ABA response of young seedlings. We analyzed the expression of major ABA response genes in our data set and noted differences between the embryo and endosperm. The expression level of ABI1, ABI2, ABI3, and ABI5 was similar in the embryo and endosperm. However, although expressed at low levels in both tissues, ABI4 transcripts were much less abundant in the endosperm and were classified as absent in eight out of nine array experiments by MAS5. We used real-time RT-PCR to clarify ABI4 expression in the seed. This clearly showed that while ABI3 and ABI5 are indeed expressed in both the embryo and endosperm, ABI4 was undetectable in the endosperm (Figure 3A
). Furthermore while ABI4 was highly induced at the transcriptional level by ABA in the embryo, this effect could not be observed in the endosperm. To further analyze the expression of the ABI genes in the seed, we examined the activity of the GUS reporter fused to the ABI3, ABI4, or ABI5 promoters (Parcy et al., 1994; Soderman et al., 2000; Brocard et al., 2002; Figures 3B to 3I). ABI3 was expressed ubiquitously throughout the seed, including the endosperm (Figures 3B to 3D). ABI3 is required for the regulation of oleosin gene expression by ABA (Crowe et al., 2000), and it is interesting to note that transcripts for oleosins are upregulated by ABA in both the embryo and endosperm, in agreement with the expression pattern of ABI3 observed in seeds (Table 2; see Supplemental Figure 2 online). In agreement with the real-time RT-PCR data, the ABI4 promoter directs GUS expression in the embryo only (Figures 3B, 3E, and 3F). Therefore, this result is confirmed by three independent methods of expression analysis. One further surprise was the expression of ABI5:GUS in the endosperm. Unlike ABI3, ABI5 expression was confined to the micropylar region of the endosperm (Figures 3B, 3G, and 3H). This region is important for the regulation of seed germination in many species and is characterized by differential gene regulation and cell wall composition compared with the lateral endosperm in many species (Bewley, 1997b). So ABI5 expression defines two domains of altered ABA sensitivity in the endosperm.
ABI4 Determines the Sensitivity of Seed Lipid Breakdown to ABA Given that both ABI4 and ABI5 are not expressed in the majority of endosperm tissues, we reasoned that the lack of either could in principle be responsible for the ABA insensitivity of lipid catabolism in the endosperm. To examine whether ABI4, ABI5, or both are required for the ABA inhibition of triacylglycerol (TAG) breakdown, eicosenoic acid levels were measured in embryos of the wild type and abi4-1 and abi5-1 mutants in the presence of ABA 5 d after imbibition (Figure 4 ). In wild-type embryos (Columbia-0 and Wassilewskija), TAG breakdown was estimated at 20 to 30% after 5 d of ABA treatment. Both the abi4-1 and abi5-1 mutants germinated at high frequency in the presence of ABA, yet the level of eicosenoic acid in 5-d-old abi5-1 mutants was similar to that in nongerminating wild-type seeds, indicating that ABI5 does not play a role in the ABA regulation of TAG breakdown. However, the abi4-1 mutant could break down virtually all its embryo-stored TAG in the presence of ABA. Therefore, we concluded that ABI4 expression determines the sensitivity of lipid reserve mobilization to ABA in the seed.
The Endosperm Is Required for the ABA and GA Regulation of Seed Germination in Arabidopsis Germination in many endospermic seeds, including tobacco, tomato, and lettuce (Lactuca sativa), is characterized by controlled loosening of the micropylar endosperm cell walls to facilitate radicle emergence (Bewley, 1997b ). This is achieved by the activity of multiple categories of cell wall–modifying enzymes, including ß-mannanase, ß-1,4-glucanase, expansins, xyloglucan endotransglycosidases, and polygalacturonases. Our expression data reveal that this group of genes is highly expressed in the Arabidopsis endosperm during germination (see Supplemental Table 4 online).
As ABA and GA signal transduction appeared to operate normally in the Arabidopsis endosperm, and the expression of multiple cell wall–modifying enzymes in the Arabidopsis endosperm was confirmed, we reasoned that the endosperm might play an active role in the phytohormonal regulation of Arabidopsis seed germination. Among the genes involved in ABA signaling during seed germination, we noted that the NADPH oxidase rbohD was highly expressed in the endosperm (Table 3). It has previously been shown that the atrbohd atrbohf double mutant exhibits reduced ABA inhibition of seed germination (Kwak et al., 2003
We also analyzed the germination and establishment of abi4-1 mutant seeds in the presence of ABA and PAC. As ABI4 expression is confined to the embryo, we reasoned that the response of the abi4-1 endosperm to both ABA and PAC should be similar to the wild type. The abi4-1 mutant shows significant PAC- and ABA-resistant germination (data not shown). We observed that abi4-1 mutants germinating on concentrations of PAC or ABA inhibitory to wild-type seeds became entangled in the endosperm despite the completion of radicle emergence. In many cases, a ring of endosperm tissue remained attached to abi4-1 hypocotyls, and occasionally seedling development proceeded with the seedling encased in the endosperm (Figures 5C and 5D). Although we cannot completely rule out an ABI4-independent ABA- and PAC-responsive mechanism in the embryo that could account for these observations, in the context of our analysis, it seems likely that an ABA-repressible and GA requiring endosperm loosening is responsible. This is not surprising given that ABI3 and ABI5 are both expressed in the endosperm and presumably involved in mediating subsets of ABA responses. Therefore, these results show that in common with other seeds, the Arabidopsis endosperm plays an active role in the regulation of seed germination and seedling establishment.
We have used RNA amplification to facilitate tissue-specific transcript profiling and dissection of the ABA response in seeds. This type of approach adds extra value and resolution to transcriptome studies compared with the analysis of more complex groups of tissues (Lee et al., 2005 ). This investigation has enabled the description of the endosperm transcriptome and has been successful in understanding the molecular basis of differential ABA signaling in the seed. Furthermore, using the new findings, we have been able to demonstrate a previously unknown role for the Arabidopsis endosperm in the control of seed germination by ABA.
ABI4 Is an Embryo-Specific Regulator of TAG Breakdown
The second major difference in ABA signaling between the embryo and endosperm was the ABA sensitivity of photosynthesis-associated nuclear-encoded gene (PhANG) expression. ABA had a strong inhibitory effect on the expression of these genes in the embryo. This effect of ABA on plastid function was found to be specific to the nuclear genome, as ABA had no effect on chloroplast-encoded gene expression (Figures 2C and 2D). PhANGs with embryo-specific ABA-sensitive expression included those encoding the photosynthetic apparatus, the Calvin cycle, and tetrapyrrole biosynthesis. Interestingly, MapMan analysis of PhANG expression in the endosperm suggests that ABA treatment actually results in a small upregulation of the transcript levels of these genes in the endosperm, rather than the inhibition seen in the embryo (see Supplemental Figure 2 online; P = 0.046). Interestingly, PhANG expression is also a known key target of ABI4. For instance, ABI4 regulates the sugar and ABA responsiveness of the plastocyanin and chlorophyll a/b binding protein 2 (CAB2) promoters (Dijkwel et al., 1997
In the embryo, the glyoxylate cycle and gluconeogenesis are induced 1 d after imbibition, but here, we report that this is not accompanied by an increase in steady state transcript levels (see Supplemental Table 2 online), although we cannot rule out that these do not increase at later time points. The level of expression of reserve mobilization genes in our analysis strongly resembles that observed during late seed development and in dry seeds (Nakabayashi et al., 2005
The Endosperm Is Required for ABA and GA Regulation of Seed Germination
Plant Material Arrays were performed on isolated embryo and endosperm tissue from the Landsberg erecta ecotype. The ABI3:GUS, ABI4:GUS, and ABI5:GUS lines were gifts from Ruth Finkelstein. The abi4-1 and abi5-1 mutants were obtained from the Nottingham Arabidopsis Stock Centre. The rbohd mutant was a gift from Jonathan Jones.
Affymetrix Gene Chip Experiments and Data Analysis
Comparison with public domain Affymetrix ATH1 data sets was achieved by downloading entire data sets from NascArrays (http://affymetrix.arabidopsis.info/narrays/experimentbrowse.pl) and from Nakabayashi et al. (2005)
Real-Time RT-PCR and GUS Expression Analysis
Transmission Electron Microscopy
Fatty Acid Determinations
rbohd Germination Assay
Accession Numbers
Supplemental Data
We thank Ruth Finkelstein and Jonathan Jones for sharing plant material. This work was supported by the Garfield-Weston Foundation.
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: Ian A. Graham (iag1{at}york.ac.uk).
[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.106.041277. Received January 20, 2006; Revision received May 11, 2006. accepted June 7, 2006.
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ABSTRACT
INTRODUCTION
4000 genes expressed differentially in either the embryo or endosperm. Plotting embryo and endosperm transcript levels supported this view, showing a broad correlation in gene expression levels between the two tissues (R2 = 0.75; 
-amantin (Rajjou et al., 2004
