Molecular Plant Advance Access originally published online on October 8, 2007
Molecular Plant 2008 1(1):75-83; doi:10.1093/mp/ssm007
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© The Author 2007. Published by Oxford University Press on behalf of CSPP and IPPE, SIBS, CAS.
Abscisic Acid, High-Light, and Oxidative Stress Down-Regulate a Photosynthetic Gene via a Promoter Motif Not Involved in Phytochrome-Mediated Transcriptional Regulation
a Fundación Instituto Leloir, and IIBBA-CONICET, C1405BWE-Buenos Aires, Argentina
b IFEVA, Facultad de Agronomía, Universidad de Buenos Aires and CONICET, 1417 Buenos Aires, Argentina
1 To whom correspondence should be addressed. E-mail casal{at}ifeva.edu.ar, tel. 5411 4524–8070/71 Ext. 8123, fax 5411 4514–8730
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Abstract |
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 TOP Abstract INTRODUCTIONRESULTSDISCUSSIONMETHODS |
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In etiolated seedlings, light perceived by phytochrome promotes the expression of light-harvesting chlorophyll a/b protein of photosystem II (Lhcb) genes. However, excess of photosynthetically active radiation can reduce Lhcb expression. Here, we investigate the convergence and divergence of phytochrome, high-light stress and abscisic acid (ABA) signaling, which could connect these processes. Etiolated Arabidopsis thaliana seedlings bearing an Lhcb promoter fused to a reporter were exposed to continuous far-red light to activate phytochrome and not photosynthesis, and treated with ABA. We identified a cis-acting region of the promoter required for down-regulation by ABA. This region contains a CCAC sequence recently found to be necessary for ABI4-binding to an Lhcb promoter. However, we did not find a G-box-binding core motif often associated with the ABI4-binding site in genes promoted by light and repressed by ABI4. Mutations involving this motif also impaired the responses to reduced water potential, the response to high photosynthetic light and the response to methyl viologen but not the response to low temperature or to Norflurazon. We propose a model based on current and previous findings, in which hydrogen peroxide produced in the chloroplasts under high light conditions interacts with the ABA signaling network to regulate Lhcb expression. Since the mutation that affects high-light and methyl viologen responses does not affect phytochrome-mediated responses, the regulation by retrograde and phytochrome signaling can finally be separated at the target promoter level.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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Photosynthesis is essential for plant survival but plants have evolved the ability to repress the development of their photosynthetic apparatus in the absence of light. When, immediately after seed germination, the shoot grows in full darkness beneath the soil, the seedling exhibits the etiolated pattern of development characterized by the presence of rudiments of the photosynthetic apparatus, reduced growth of the foliage and enhanced axis extension (Chen et al., 2004). In Arabidopsis, the expression of many photosynthetic genes requires the specific interaction of the bZIP transcription factor HY5 with the G-box sequence CACGTG (Chattopadhyay et al., 1998), and the action of many other transcription factors (reviewed by Casal and Yanovsky, 2005). In darkness, HY5 is degraded in the 26S proteasome thanks to the action of the E3 ligase COP1 (Osterlund et al., 2000; Saijo et al., 2003). In the light, COP1 migrates from the nucleus to the cytoplasm (Osterlund and Deng, 1998), allowing the levels of HY5 and other transcription factors required for de-etiolation to build up (Osterlund et al., 2000; Saijo et al., 2003; Seo et al., 2003).
In addition to its role as a trigger of de-etiolation, light has a second action on the expression of photosynthetic genes. Gene expression of chlorophyll-binding proteins of the light-harvesting complex of photosystem II (Lhcb) is down-regulated by high-light stress. Exposure to high light increases the reduced pool of plastoquinone between photosystem II and photosystem I and this signal causes the repression of Lhcb expression in the green algae Dunaliella tertiolecta (Escoubas et al., 1995). A similar mechanism operates in higher plants but the pathways of action of the redox state of plastoquinone are more complex and there is evidence in favour of additional redox signals (Oswald et al., 2001; Fey et al., 2005; Nott et al., 2006). In addition to the redox state of the plastoquinone pool and eventually of other components of the photosynthetic electron transport chain, high light can produce excess hydrogen peroxide, which can diffuse from the chloroplast to the cytoplasm and affect nuclear gene expression (Nott et al., 2006). In the bundle sheath cells of Arabidopsis leaves, the promotion of ASCORBATE PEROXIDASE 2 (APX2) expression by excess light appears to be mediated by hydrogen peroxide (Fryer et al., 2003). Furthermore, light increases the accumulation of carbohydrates and this, in turn, negatively regulates the expression of photosynthetic genes, suggesting that this indirect pathway could also mediate the effects of strong light (Rook et al., 2006).
In addition to high light, the hormone abscisic acid (ABA) also down-regulates the expression of Lhcb genes. Drought increases ABA levels and reduces Lhc expression in the leaves of light-grown tomato plants and these responses are absent in a mutant with impaired ABA synthesis, but exogenously applied ABA is effective in wild-type and mutant plants (Bartholomew et al., 1991). The levels of ABA inversely correlate with Lhc expression during embryogenesis in soybean and the addition of ABA to soybean cotyledons cultivated in vitro down-regulates Lhc expression (Chang and Walling, 1991). In Lemna gibba, application of ABA reduces the activity of an Lhcb promoter (Weatherwax et al., 1996).
Different pieces of evidence link ABA to reactive oxygen species. In guard cells, ABA induces the production of hydrogen peroxide and the activation of calcium channels by hydrogen peroxide mediates the induction of stomata closure by ABA (Pei et al., 2000). Disruption of two NADPH oxidase catalytic subunit genes, which function in the induction of hydrogen peroxide by ABA, impairs the activation of calcium channels and the subsequent closure of the stomata but these effects are rescued by exogenously applied hydrogen peroxide (Kwak et al., 2003). Other physiological processes such as root growth and seed germination are also less sensitive to ABA in mutants of these NADPH oxidase catalytic subunit genes, suggesting that hydrogen peroxide could function downstream of ABA in different contexts (Kwak et al., 2003). The ABA insensitive 1 (abi1) and abi2 mutants, defective in genes encoding protein phosphatase 2C-like enzymes, respectively impair ABA induction of reactive oxygen species or the stomata closure response to hydrogen peroxide (Murata et al., 2001). Hydrogen peroxide negatively regulates in-vitro protein phosphatase activities of ABI1 and ABI2 (Meinhard and Grill, 2001; Meinhard et al., 2002). The abo1 mutant shows enhanced sensitivity of stomata closure and seedling growth inhibition in response to ABA and is more resistant to the oxidative stress generated by the application of methyl viologen (MV, paraquat) (Chen et al., 2006). The glutathione peroxidase 3 enzyme plays a role as general scavenger of hydrogen peroxide but, in addition, it physically interacts with ABI2 and, to a lesser extent, with ABI1 and is required for ABA-induced responses (Miao et al., 2006).
The available information suggests that ABA and high-light stress could converge to control Lhcb expression. In fact, ABA acts synergistically with hydrogen peroxide to promote APX2 expression (Fryer et al., 2003). Furthermore, in detached Arabidopsis leaves, the activity of the plastocyanin gene promoter depends on the interaction between sugar levels, photosynthetic electron transport and ABI4 (Oswald et al., 2001). However, the evidence in favour of this convergence is not fully conclusive. In Lemna gibba and Arabidopsis thaliana, the condition that increases ABA content is prolonged darkness and not light (Weatherwax et al., 1996). High-light exposure of Arabidopsis plants acclimated to low light reduces Lhcb expression in wild-type and ABA signaling or synthesis mutants, including abi4, which shows a weaker response only 15 min after the treatment but not later on (Koussevitzky et al., 2007). Finally, in microarray experiments, elements involved in ABA responsiveness are present in gene clusters induced by high light with reduced infra-red but repressed by high light containing infra-red (Rossel et al., 2002). The aim of the present work is to investigate whether ABA, high-light stress and phytochrome signaling converge to control the activity of an Lhcb promoter by sharing a cis-acting sequence.
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RESULTS |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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ABA Counteracts the Promotion of Lhcb Activity by Phytochrome
Two-day-old, dark-grown seedlings of Arabidopsis thaliana were exposed to 24 h of continuous far-red light (FR) to activate phytochrome A or left as dark controls. One hour before the beginning of FR, the seedlings were sprayed with an ABA solution or with a solution lacking ABA in factorial combination with the FR or dark condition. The seedlings were harvested 24 h after the begining of FR. In dark-grown seedlings, the addition of ABA had little or no effect on the activity of an Lhcb promoter fused to the GUS reporter (Figure 1). The activity of the Lhcb promoter increased significantly in response to FR and this promotion was partially counteracted by the ABA treatment.
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To further characterize the system, we introduced an Lhcb promoter into the gain-of-function abi1-1 background, which negatively regulates ABA signaling (Gosti et al., 1999), and investigated the response to ABA in seedlings exposed to FR. The abi1-1 seedlings showed higher GUS activity than the wild-type and failed to respond to ABA (Figure 2).
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Definition of the cis-Acting Sequence Required for ABA Responsivity
We conducted a deletion analysis of the promoter as a first step to identifying a region important for ABA responsivity in FR-treated seedlings. Increasingly shorter promoter lengths caused reduced activity and reduced response to ABA (Figure 3A). The –152 bp or shorter fragments failed to respond to ABA, suggesting that elements important for ABA responsiveness could be located between –176 and –152 bp. Although reduced promoter activity and response correlated in this analysis, the introduction of mutations in cis-acting elements important for promoter activity (GATA1-m and AAAATCT-m; Cerdán et al., 2000 and references therein) did not affect the relative impact of the ABA treatment (Figure 3A). Furthermore, even the shortest fragment retained responses to light (data not shown). This suggests that the –176 to –152 bp region contains elements selectively important for the ABA response.
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In subsequent experiments, we introduced a series of 6 bp mutations within the –176 and –139 bp region (Figure 3D). These mutations had no significant effects on the basal activity of the Lhcb promoter in darkness, which showed little response to ABA (Figure 3B). Under FR, the substitutions named –165 and –159 fully eliminated the response to ABA (Figure 3C). These substitutions did not affect the activity in the absence of an ABA treatment. In other words, the sequence –170 GGACCACAGTAG –159 contains elements necessary for the inhibition caused by ABA but not for the induction of Lhcb activity by FR.
The Response to Osmotic Stress is Impaired in the –165 Mutated Promoter
ABA is involved in plant responses to salinity, sugars, osmotic stress, and cold (Finkelstein et al., 2002; Xiong et al., 2002; Rook et al., 2006). To investigate whether these effects converge to the same Lhcb promoter region to control its activity, transgenic seedlings bearing either the wild-type or the –165 mutated promoter (Figure 3D) were exposed to FR in factorial combination with different concentrations of glucose, NaCl, or polyethilene glycol (PEG, used to reduce the water potential of the substrate). All these conditions reduced the activity of the wild-type promoter. However, the mutated promoter failed to respond to any of these treatments (Figure 4), indicating that the effects of glucose, salt, or PEG require a common cis-sequence. In the control promoter, the inhibitory effects of glucose and NaCl were not stronger than that of PEG, indicating that under our conditions, the negative regulation was largely caused by the reduced water potential of the substrate. Actually, the effect of glucose was much weaker than that of PEG, suggesting that it might represent a balance between the negative osmotic effect and a positive effect of glucose. A combination of negative and positive actions of glucose on the activity of other photosynthetic gene promoters has been reported previously (Acevedo-Hernandez et al., 2005).
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The –165 Mutation Does Not Affect the Inhibition of Lhcb Activity Caused by Low Temperature
Low-temperature treatments induce the expression of Lhcb1*3 in dark-grown seedlings of Arabidopsis and have no effects on other members of the family (Capel et al., 1998). Here, we investigated the effect of a low-temperature condition given simultaneously with FR. Dark-grown seedlings were transferred to FR at either 22 or 4°C. In our case, low temperature significantly reduced the activity of the Lhcb promoter. This treatment was equally effective in the –165 mutant promoter (Figure 5). This indicates that the sequence required for responsivity to ABA is dispensable for the response to low temperature.
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The –165 Promoter Mutation Reduces the Inhibition of Lhcb Activity Caused by High Photosynthetic Light
To investigate whether the promoter region necessary for the inhibition induced by ABA is also required for the response to high light, 2-d-old etiolated seedlings bearing the wild-type or the mutated promoter were transferred to a range of fluence rates of white light (16 h light, 8 h darkness). Compared to dark controls, seedlings exposed to 2 µmol m–2 s–1 showed increased Lhcb promoter activity and the –165 mutation did not affect this response (Figure 6). In the wild-type promoter, activity peaked at 55 µmol m–2 s–1 and gradually decreased at higher irradiances. Compared to the wild-type promoter, the –165 mutation increased Lhcb activity at 55 µmol m–2 s–1 and higher irradiances (Figure 6). Although 55 µmol m–2 s–1 is not a high irradiance for green plants, seedlings are particularly susceptible to photo-oxidative damage during de-etiolation (Armstrong et al., 2000). Therefore, activity of the wild-type promoter represents a balance between photomorphogenic promotion and inhibition by light stress at 55 µmol m–2 s–1 and higher irradiances. In the –165 promoter, this inhibition is reduced.
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The –165 Promoter Mutation Reduces the Inhibition of Lhcb Activity Caused by MV
One of the signals that could mediate between the high-light condition and the inhibition of Lhcb expression is the production of hydrogen peroxide in the chloroplasts. MV enhances the production of superoxide and hydrogen peroxide in the chloroplasts. We therefore tested the effect of MV placed in the growth medium on the activity of Lhcb in plants grown under 55 µmol m–2 s–1 white light. Consistently with the above observations (Figure 6), Lhcb activity in the absence of MV was enhanced by the –165 mutation and the data are expressed relative to this condition to focus on the effect of MV. Increasing the concentration of MV in the substrate decreased Lhcb promoter activity but the wild-type sequence was more sensitive than the –165 mutant promoter, particularly at moderate concentrations of MV (Figure 7).
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The –165 Mutation Does Not Affect the Inhibition of Lhcb Activity Caused by Norflurazon
The –165 promoter mutation significantly reduced the impact of MV, which generates hydrogen peroxide in the chloroplasts. We therefore investigated whether the response to the plastidic signal generated by Norflurazon was also affected by the promoter mutation. Norflurazon inhibits carotenoid synthesis and this results in photo-oxidative damage, accumulation of Mg-protoporphyrin IX and reduced Lhcb expression (Batschauer et al., 1986; Koussevitzky et al., 2007). The activity of the Lhcb promoter significantly decreased in response to Norflurazon and this effect was similar in wild-type and –165 promoters (Figure 8).
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DISCUSSION |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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The activity of an Lhcb promoter in transgenic Arabidopsis seedlings is significantly reduced by exogenously applied ABA (Figure 1), extending previous observations in tomato (Bartholomew et al., 1991), soybean (Chang and Walling, 1991), and Lemna gibba (Weatherwax et al., 1996). This response is impaired in the abi1-1 mutant allele background (Figure 2), which negatively regulates ABA signaling (Gosti et al., 1999). In the –453 bp promoter background, the effect of ABA is significantly larger in etiolated seedlings simultaneously treated with continuous FR to activate phytochrome A than in dark controls, suggesting that ABA specifically counteracts the promotion by light (Figure 1). However, in preliminary experiments involving a larger promoter fragment (–756 bp), we observed a relatively large effect on dark-grown seedlings, suggesting that other points of control could exist in addition to that defined here.
The region required for ABA responsiveness was first defined by means of a promoter deletion analysis and then refined by 6 bp substitutions. Mutations at any of two contiguous 6 bp regions fully abolished the response to ABA, indicating that the sequence –170 GGACCACAGTAG –159 contains elements that are indispensable for ABA responses. The central portion of this region contains the CCAC motif, which is required for the binding of the APETALA 2-domain transcription factor ABI4 to an Lhcb promoter in yeast one-hybrid assays (Koussevitzky et al., 2007). ABI4 is required for some responses to ABA (Finkelstein et al., 2002). In particular, the down-regulation of a minimal light-responsive unit and of the small subunit of ribulose-1,5-bisphosphate carboxylase gene in response to ABA or hexoses is impaired in the abi4 mutant background (Acevedo-Hernandez et al., 2005). The sequence CACCTCCA found in the latter promoters is required for their ABA responsiveness and for binding of ABI4 in gel retardation assays (Acevedo-Hernandez et al., 2005). The ABI4 protein from Zea mays binds to the CACCG consensus region of different promoters controlled by ABA and sugars (Niu et al., 2002). Therefore, the sequence identified here as necessary for ABA responses of the Lhcb promoter is likely to bind ABI4.
Binding of ABI4 has been proposed to negatively regulate the expression of photosynthetic genes by impairing the binding of a positive regulator to an overlapping or closely spaced (1–3 bp) G-box core motif (ACGT) (Acevedo-Hernandez et al., 2005; Koussevitzky et al., 2007). However, in the Lhcb promoter investigated here, the G-box core is not present. Furthermore, the mutations that decrease ABA responsiveness do not reduce the response to FR (Figure 3). Immediately after the CCAC motif predicted to be necessary for ABI4-binding, there is a AGTAG sequence (i.e. –170 GGACCACAGTAG –159), in which the first adenine interrupts what could had been a G-box core motif. It is therefore tempting to speculate that while, in other promoters, ABI4 could reduce activity by impairing the access of a G-binding factor necessary for tissue and light responses (Koussevitzky et al., 2007), in promoters like the one described here, ABI4 could act via different mechanisms, potentially involving interaction with more distant transcription factors (not necessarily binding a G-box) or with the general transcription machinery.
A mutation of the Lhcb promoter that abolished the response to ABA also reduced the impact of high-light stress, providing operational evidence in favour of the convergence of these two signals. The abi4 mutation causes only a transient reduction in the impact of high light on the activity of Lhcb (Koussevitzky et al., 2007). As proposed by Koussevitzky et al. (2007), other transcription factors could operate redundantly with ABI4. Therefore, the mutation of one of these trans-acting factors would result in a weak effect but the mutation in the cis-acting factor theoretically needed for the action of all the redundant transcription factors would abolish the response.
Hydrogen peroxide produced in the chloroplasts under high light can operate as a retrograde signal controlling nuclear gene expression (Nott et al., 2006; Fryer et al., 2003). The mutation of the promoter that impaired ABA and high-light responses of Lhcb also reduced (although it did not eliminate) the response to MV, which increases hydrogen peroxide production by the chloroplasts. Based on present and previous results, we propose a model in which high photosynthetic light increases hydrogen peroxide production in the chloroplasts; this signal interacts with the ABA network eventually at different points, one of which could be ABI4, finally operating on a common cis-acting region. Previous attempts had failed to separate at the promoter level the regions necessary for phytochrome induction of activity from those required for negative regulation by chloroplast retrograde signals (reviewed by Nott et al., 2006). Here, we show that this separation is possible because a mutation that impairs the responses to hydrogen peroxide produced in the chloroplast does not affect the promotion by phytochrome A. Despite the reduced response to MV, the mutated promoter retained normal responses to Norflurazon. A differential impact of MV and Norflurazon had already been reported for cyanobacteria (Thomas et al., 1998). The expression of the Lhcb1*3 gene is induced by low temperature in dark-grown seedlings of Arabidopsis (Capel et al., 1998). Here, we show that in FR-treated seedlings, low temperature actually inhibits Lhcb expression (Figure 5). The –165 mutated promoter responded normally and this result is consistent with the notion that low-temperature regulation of gene expression is relatively independent of ABA signaling (Xiong et al., 2002).
When a seedling emerges from the soil, exposure to light strongly promotes the activity of Lhcb expression but this effect is partially counteracted by a negative regulation that operates at moderate and high fluences of photosynthetic light. This balance would help to regulate the size of the photosynthetic antenna according to the environmental conditions and the physiological status of the seedling, in particular, the ability to utilize the products of the photochemical reactions of photosynthesis. The convergence of ABA, osmotic stress, and high-light signals could be functionally important because low availability of carbon dioxide caused by stomata closure due to water deficit-induced ABA signals and high light are two conditions that tilt the balance between photochemical and carbon-fixation reactions of photosynthesis in favour of the former. A reduction in antenna size would re-establish the balance and avoid the damage caused by reactive oxygen species.
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METHODS |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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Transgenic Lines Carrying Fragments of the Lhcb1*2 Promoter
We used transgenic lines of Arabidopsis thaliana accession Columbia carrying fragments of the –453 bp Lhcb1*2 promoter of Nicotiana plumbaginifolia fused to the coding region of gusA. This promoter has been intensively characterized in previous studies (Cerdán et al., 1999; 2000; Mazzella et al., 2001) and bears a distribution of motifs important for promoter activity very similar to that of Lhcb1*1 and Lhcb1*2 of Arabidopsis thaliana. The promoter deletions –176, –134, and –128 and the mutations GATA1-m and AAAATCT-m have been described earlier (Cerdán et al., 2000). New constructs in the context of the –453 to +67 fragment of Lhcb1*2 were obtained by PCR with specific primers bearing a HindIII tail at its 5’ end using a pUC19-derived plasmid bearing the –453 (HindIII) to +67 (BamHI) fragment of the Lhcb1*2 promoter as a template. The amplified fragments were cut with HindIII and BamHI and subcloned in the pBI101.2 vector containing the gusA reporter gene and sequenced. The fragments were introduced into Arabidopsis accession Columbia by way of Agrobacterium tumefaciens, using the floral dip method (Clough and Bent, 1998). The nature and integrity of the transgene were verified by PCR. The –176 bp promoter was introduced into the abi1-1 background to investigate the impact of ABI1 on the activity of this promoter.
Experimental Settings
Approximately 100 seeds were sown on 1% agar in clear plastic boxes (40x33x15 mm height), incubated for 3 d in darkness at 4°C. The seeds were transferred to 22°C, exposed to 40 min red light and incubated for 2 d in darkness. Then, the seedlings were either exposed to continuous FR (60 µmol m–2 s–1) for 24 h or remained as dark controls before harvest. For ABA treatments, the seedlings were sprayed with a 300 µM ABA (Sigma, St Louis) solution in water 60 min before transfer to FR. This dose was chosen because lower doses were saturating for the Lhcb promoter in Landsberg erecta but not in Columbia. In the experiments in which the seedlings were exposed to photosynthetically active radiation, light was provided at the indicated fluence rates by high-pressure sodium lamps (Lucalox LU/400/40, Hungary). For the treatments with glucose (Sigma), NaCl (Anedra), polyethileneglycol (PEG, Sigma), or MV (Sigma), the seeds were sown on a layer of filter paper (Whatman number 1) placed on top of the agar and, 60 min before the beginning of the light treatment, the filter paper holding the seedlings was placed on fresh agar containing the indicated concentrations of glucose, NaCl, PEG, or MV. For the treatments with Norflurazon (San 9789, Sandoz), the seeds were sown on water-soaked filter paper (without agar) and the herbicide added after chilling. Extractions and measurements of β-glucuronidase (GUS) activity were conducted as described earlier (Cerdán et al., 2000).
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Acknowledgements |
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We thank Edith Trejo for technical support and ABRC (University of Ohio) for their provision of the abi1-1 mutant. This work was financially supported by Agencia Nacional de Promociòn Científica y Tecnológica (Argentina) grant PICT 32492 to JJC, University of Buenos Aires grant AG021 to JJC, Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina) grants PIP 5958 to JJC and PIP grant 06082 to RJS.
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