Journal of Experimental Botany, Vol. 51, No. 352, pp. 1939-1944,
November 1, 2000
© 2000 Oxford University Press
Original Papers |
Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings
Department of Biochemistry and Food Science, Faculty of Agriculture, Kagawa University, Miki, Kagawa 761-0795, Japan
Received 23 February 2000; Accepted 12 June 2000
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Abstract |
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Lettuce (Lactuca sativa L.) seedlings were subjected to anoxic stress after ABA-pretreatment (ABA-PT) or hypoxic-pretreatment (H-PT). The H-PT increased the survivability of the anoxia in roots of the seedlings by 5.2-fold compared to that of non-pretreated (N-PT) seedlings. ABA-PT also increased the survivability at concentrations greater than 1 µM, and the survivability increased with increasing ABA doses. At 100 µM ABA, the survivability was 4.5-fold greater than that of N-PT seedlings. During pretreatment periods, alcohol dehydrogenase (ADH, EC 1.1.1.1) activity in the roots became 3.1- and 3.4-fold greater than that of N-PT seedlings following 100 µM ABA-PT and H-PT seedlings, respectively. After the onset of anoxic stress, ADH activities in all roots increased, but the activities in H-PT and ABA-PT roots remained much greater than that in N-PT roots, and the average ethanol production rate for the initial 6 h was 5.3, 4.0 and 1.4 µmol g-1 FW h-1 for H-PT, ABA-PT and N-PT roots, respectively. Roots of the seedlings lost ATP rapidly under anoxic stress; however, the decrease in ATP was much slower in the ABA-PT and H-PT seedlings than in the N-PT seedlings. These results suggest that the ABA-PT and H-PT may maintain ATP levels due to activation of ethanolic fermentation, which may be one of the causes of the increasing anoxia tolerance in the seedling roots. Measurement of endogenous ABA levels, however, showed that ABA levels did not increase during the H-PT, suggesting that the H-PT does not increase tolerance through an increase in ABA levels.
Key words: Abscisic acid, alcohol dehydrogenase, anoxia tolerance, ATP, Lactuca sativa.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Oxygen deficiency in the root zone of plants occurs with several environmental stresses, for example, flooding, waterlogged soil and ice encasement (Crawford, 1982
; Vartapetian and Jackson, 1997). Low oxygen stress dramatically alters the pattern of gene expression in many plants (Sachs and Ho, 1986; Sachs et al., 1996), and many plants have evolved a series of adaptive physiological and biochemical changes which enhance their ability to survive the adverse conditions (Ricard et al., 1994; Plaxton, 1996; Vartapetian and Jackson, 1997).
The survivability of several species exposed to mild hypoxia during a subsequent period of severe hypoxia or anoxia was greatly improved (Johnson et al., 1989; Andrews et al., 1994; Ellis et al., 1999). The improved tolerance of the plants by hypoxic-pretreatment (H-PT) was associated with greater concentrations of ATP and with increased activity of alcohol dehydrogenase (ADH; VanToai et al., 1995; Drew, 1997; Germain et al., 1997).
Exogenous abscisic acid (ABA) was also able to increase anoxia tolerance in Arabidopsis (Ellis et al., 1999) and maize seedlings (Hwang and VanToai, 1991). However, the mechanism of the acclimation to anoxia by ABA-pretreatment (ABA-PT) remains unknown. The objective of this study was to investigate the effects of ABA-PT and H-PT on anoxia tolerance in lettuce seedlings. Thus, survivability, ADH activity, and ethanol, adenine nucleotides and endogenous ABA levels were determined in lettuce roots of H-PT and ABA-PT seedlings subjected to anoxic stress.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Plant material
Seeds of lettuce (Lactuca sativa L. cv. Grand Rapids; purchased from Takii Ltd, Kyoto, Japan) were sterilized in a 2% (w/v) solution of sodium hypochlorite for 15 min and rinsed four times in sterile distilled water. All further manipulations were carried out under sterile conditions. The seeds were germinated on two sheets of moist filter paper (No 1; Toyo Ltd, Tokyo) at 25 °C in daily cycle of 12/12 h light/dark in a growth chamber. Light was provided from above with two white fluorescent lamps (3.2 W m-2 at plant level; FL20SPG, National, Tokyo). After 2 d, uniform seedlings were selected and transferred, in groups of 25, to 9 cm Petri dishes each containing two sheets of filter paper moistened with 10 ml Murashige and Skoog medium (Murashige and Skoog, 1962
). After being kept in the daily cycles for a further 5 d, the seedlings were used for ABA-PT and H-PT.
Pretreatments with hypoxia and ABA
For H-PT, the medium in the Petri dishes was replaced with fresh Murashige and Skoog medium and the Petri dishes were placed into jars (5 l) at 25 °C in the daily cycle in the growth chamber described above. Distilled water (200 ml) was placed at the bottom of the jar to maintain humidity and the Petri dishes were elevated above the water. A stream of 5% O2 (balance N2) was passed continuously through the jar at a rate of 200 ml min-1 for 24 h. Non-pretreated (N-PT) seedlings were supplied with air flowing at 200 ml min-1.
For ABA-PT, the medium in the Petri dishes was replaced with fresh Murashige and Skoog medium containing ABA (cis,trans-ABA; Sigma, USA) and the Petri dishes were placed in the growth chamber described above. After 24 h, the seedlings were rinsed five times with distilled water and the filter paper in the Petri dishes was moistened with fresh Murashige and Skoog medium.
Anoxic treatment
After ABA-PT and H-PT, the Petri dishes were placed into jars (5 l) as described above and a stream of N2 was passed continuously through the jar at 200 ml min-1 for 24 h. Non-stressed seedlings were supplied with air flowing at 200 ml min-1.
Survivability determination
The lettuce roots were considered to have survived if their root tips resumed elongation after anoxic treatment (Johnson et al., 1989). Just after the anoxic treatment, 50 roots for each determination were marked with waterproof ink at 10 mm from the root tip and allowed to grow under aerobic condition at 25 °C in the growth chamber for 48 h. Then, the distance was measured with a ruler between the root tip and the mark, and surviving roots that resumed extension were counted. The percentage survivability was determined by reference to the survival number of the non-stressed seedlings.
Extraction and determination of ABA
For quantification of endogenous ABA in roots of lettuce seedlings, two jars for each treatment were removed from the chamber, and the roots of the seedlings were harvested, frozen immediately with liquid N2 and stored at -80 °C until extraction.
Fifty frozen roots of the seedlings for each treatment were placed in a mortar containing liquid N2 and ground to a fine powder using a pestle. Powdered tissue was suspended in methanol containing 2.5 mM citric acid monohydrate and 0.5 mM butylated hydroxytoluene at a ratio 15 ml g-1 tissue according to the ABA extraction method described earlier (Walker-Simmons, 1987). The extract was then stirred for 36 h in the dark at 4 °C and centrifuged at 3000 g for 15 min at 4 °C. After passing the supernatant through a C18 Sep-Pak cartridge (Waters, Tokyo, Japan) with aqueous 70% methanol, the eluate was dried and ABA concentration was determined with an ABA immunoassay detection kit (Sigma). The overall recoveries of ABA (cis, trans-ABA) added to the extraction medium containing root powder before homogenation were 87±6% (mean±SE) as calculated from five replications.
Extraction and assay of ADH
Root powder was prepared as described above and homogenized with 5 vols of ice-cold solution containing 100 mM TRIS-HCl (pH 8.0), 10 mM Na-ascorbate, 10 mM DTT, 50 mM bovine serum albumin, and 5% (v/v) glycerol. The homogenate was centrifuged at 30 000 g for 30 min and the supernatant was used immediately for measurements of ADH activity (Hanson et al., 1984).
ADH activity was measured spectrophotometrically by monitoring the oxidation of NADH at 340 nm (as described by Kato-Noguchi and Watada, 1997). The overall recovery of ADH activity through the quantification process was 85±7% (mean±SE) according to five repeated assays with pure enzyme in the extract. Protein was determined by the method of Bradford using bovine 
-globulin as a standard (Bradford, 1976).
Extraction and determination of ethanol
Quantification of ethanol was carried out by gas chromatography as described previously (Kato-Noguchi and Watada, 1997). Root powder (3 g FW equivalent) was homogenized with 15 ml of 0.1 M HCl. A 2 ml aliquot of extract was incubated in a Teflon sealed 5 ml screw-cap test tube at 70 °C. After 20 min incubation, a 1 ml sample of head-space gas was analysed in a gas chromatograph equipped with a FID detector (Shimadzu, Kyoto, Japan) and a Porapac Q column (3 mmx3 m; GL Science, Tokyo). Internal standards for ethanol added to the extraction medium before sample homogenation showed 79±6% (mean±SE) recovery as calculated from five replications.
Extraction and determination of adenine nucleotides
Root powder was homogenized with 5 vols of ice-cold 0.4 M HClO4 and the homogenate was kept for 30 min in an ice-bath with occasional shaking. Then, the mixture was centrifuged at 30 000 g for 15 min at 4 °C and the supernatant was neutralized with 5 M K2CO3. The precipitated potassium perchlorate was removed by centrifugation (30 000 g, 5 min) and the supernatant was used for analyzing adenine nucleotides (Bergmeyer, 1985).
Adenine nucleotides were quantified spectrophotometrically according to the methods described earlier (Mohanty et al., 1993). The overall recoveries of ATP, ADP and AMP added to the extraction medium containing root powder before homogenation were 82±6%, 79±7% and 84±5% (mean±SE), respectively, as calculated from five replications.
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Results and discussion |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Survivability
Seven-day-old lettuce seedlings that had been subjected to ABA-PT, H-PT or N-PT were exposed to 24 h anoxic stress followed by a 48 h recovery period (Fig. 1
). The survivability of the N-PT seedlings was 15% that of non-stressed seedlings, whereas the survivability of the H-PT seedlings was 78% that of the non-stressed seedlings (Fig. 1A), indicating that the H-PT increased the tolerance of the seedlings. Increasing tolerance to anoxic stress by H-PT has been reported in maize, rice, tomato, wheat, and Abrabidopsis roots (Johnson et al., 1989; Waters et al., 1991; Germain et al., 1997; Ellis and Setter, 1999; Ellis et al., 1999).
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The ABA-PT also increased the survivability of the lettuce roots at concentrations greater than 1 µM and the survivability increased with increasing ABA doses, leveling off at 100 µM (Fig. 1B
). When plotted against the logarithms of doses, the dose–response curve was linear between 20% and 60% survivability of non-stressed seedlings. At 100 µM ABA, the survivability increased to 60% that of the non-stressed seedlings. Thus, the ABA-PT increased the subsequent tolerance of the roots of the lettuce seedlings subjected to anoxic stress (Fig. 1), although its maximum effectiveness was 20% lower than that of the H-PT.
ABA is known to play an important role in mediating plant responses to several environmental stresses (Davies and Mansfield, 1983; Zeevaart and Creelman, 1988; Sánchez-Serrano et al., 1991). Endogenous ABA levels are significantly increased by low temperature, dehydration and wounding stresses in many plant species, and the increased ABA improved the tolerance of the plants to these stresses (Zeevaart and Creelman, 1988; Sánchez-Serrano et al., 1991). Even though exogenous ABA increased the anoxia tolerance (Fig. 1), H-PT did not affect the ABA level in roots of lettuce seedlings and the level in the H-PT and N-PT roots was not increased by anoxic stress (Table 1), which supports the results of maize (Dolferus et al., 1994). These results suggest that the H-PT does not increase tolerance through an increased endogenous ABA level.
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ADH activity
The effect of ABA-PT and H-PT on ADH activity in lettuce roots was determined just after the pretreatments (Fig. 2). The H-PT increased ADH activity which was 3.4-fold greater than that of the N-PT roots. The ABA-PT also increased the ADH activity and the increase in ADH activity by ABA-PT was greater at higher doses of ABA up to 100 µM. The maximum ADH activity was 3.1-fold greater compared to that in the N-PT seedlings. After the onset of anoxic stress, all ADH activities in the roots were increased, but the differences in their activity remained (Fig. 3). At 12 h, the activity in ABA-PT and H-PT roots was 1.8- and 2.0-fold greater than that in the N-PT roots, respectively.
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) roots of lettuce seedlings after the onset of anoxia. Seven-day-old lettuce seedlings were treated with 100 µM ABA-PT or H-PT for 24 h and exposed to anoxic stress. N-PT seedlings (
) were incubated in air for 24 h without any pretreatment and transferred to the anoxia. Means±SE from three independent experiments with four assays for each determination (n=12) are shown.Induction of ADH during low oxygen conditions has been observed in many plant species (Kennedy et al., 1992
; Ricard et al., 1994; Tadege et al., 1998). When oxygen becomes limiting, glycolysis accelerates and replaces the Krebs cycle as the main source of energy (Rivoal and Hanson, 1994; Drew, 1997). The advantage of ADH induction in low oxygen conditions is reported to be an acceleration of the ethanolic fermentation pathway, which allows the continuation of glycolysis owing to pyruvate consumption and recycling of NAD+ (Kennedy et al., 1992; Ricard et al., 1994). Moreover, ADH is necessary for removal of acetaldehyde because of its phytotoxic effect (Perata and Alpi, 1991) and for tight cytoplasmic pH regulation (Roberts et al., 1984). Furthermore, ADH null mutants of maize and Arabidopsis seedlings were more sensitive to the anoxic stress than their wild types (Johnson et al., 1989, 1994). Therefore, induction of ADH and activation of ethanolic fermentation was considered to be one of the strategies for plants to survive in low oxygen conditions (Kennedy et al., 1992; Ricard et al., 1994; Drew, 1997).
Although the biological role of ADH is apparent only under low oxygen conditions, dehydration and low temperature stresses as well as low oxygen stress are able to induce expression of the ADH gene (Adh) in Arabidopsis seedlings (Jarillo et al., 1993; Dolferus et al., 1997). Exogenous ABA also induced ADH in maize seedlings (Hwang and VanToai, 1991) and Adh in Arabidopsis seedlings (de Bruxelles et al., 1996). This Adh induction in Arabidopsis by ABA was found to be mediated by the same cis-acting promoter elements as dehydration stress. However, Adh induction by low oxygen and low temperature is independent of ABA induction, and two additional independent signal transduction pathways which require different promoter elements are involved (de Bruxelles et al., 1996; Dolferus et al., 1997). These findings support the hypothesis that, although both H-PT and ABA-PT induced ADH in the lettuce roots (Fig. 2) and increased anoxia tolerance of the roots (Fig. 1), their ADH induction pathways may be independent.
Ethanol production
For estimation of the activity of glycolysis and ethanolic fermentation, their end product, ethanol concentration, was determined in lettuce roots (Fig. 4). The concentrations in all roots were low at time 0 and immediately increased after the onset of anoxic stress. However, the increasing rate was greater in H-PT and ABA-PT than in N-PT. The average production rates of ethanol for the initial 6 h were 5.3, 4.0 and 1.4 µmol g-1 FW h-1 for H-PT, ABA-PT and N-PT roots, respectively. After 12 h, the concentrations in the H-PT and ABA-PT roots became 2.6- and 2.1-fold greater than that in the N-PT roots, respectively. It had been reported that exogenous ABA induced the glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase (EC 1.2.1.12) and enolase (EC 4.2.1.11), which are known to play an important regulatory role in glycolysis for the maintenance of a high-energy status (Velasco et al., 1994; Forsthoefel et al., 1995; Sachs et al., 1996). A number of glycolytic enzymes were also found to be induced by H-PT (Sachs and Ho, 1986; Waters et al., 1991; Sachs et al., 1996; Germain et al., 1997). Thus, ethanol production in lettuce roots (Fig. 4) indicates that glycolysis and ethanolic fermentation may be more active in H-PT and ABA-PT roots than in N-PT roots.
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ATP and total adenine nucleotide concentrations
Figure 5 shows the changes of ATP and total adenine nucleotide concentrations in lettuce roots after the onset of anoxic stress. During the initial 6 h N-PT roots rapidly lost ATP and total adenine nucleotides which then decreased gradually, in agreement with the results of others (Roberts et al., 1984; Johnson et al., 1989). The ATP and total adenine nucleotide concentrations in the ABA-PT and H-PT roots also decreased under the stress. However, their decreases were much slower in the ABA-PT and H-PT roots than in N-PT roots. Twelve hours after the onset of anoxia, ABA-PT and H-PT roots contained 2.8- and 3.3-fold as much ATP, respectively, as N-PT roots and 2.4- and 2.8-fold as much total adenine nucleotides as N-PT roots, respectively. Thus, the ABA-PT and H-PT roots of lettuce seedlings maintained higher ATP and total adenine nucleotide levels under the anoxic stress.
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One determinant in anoxic-induced cell damage in the plant root is cytoplasmic acidification due to a net influx of protons into the cytoplasm from the vacuole (Saint-Ges et al., 1991
; Fox et al., 1995). Increased availability of ATP could contribute to reducing this acidification (Roberts et al., 1984; Felle, 1996). Against the free energy gradients, H+-translocating ATPases in the tonoplast can drive H+ ions to the vacuole from the cytoplasm (Johnson et al., 1994; Felle, 1996). Thus, the greater level of ATP is considered to be a significant contributory factor to the subsequent plant survival under anoxic stress (Johnson et al., 1989; Bouny and Saglio, 1996; Drew, 1997). It was also reported that energy metabolism of ADH null mutants in several plants declined much more than their wild types (Johnson et al., 1989, 1994) and that the ADH null mutant of Arabidopsis did not have increased tolerance to low oxygen stress by H-PT (Ellis et al., 1999).
In summary, the ABA-PT and H-PT increased the subsequent tolerance of lettuce roots subjected to anoxic stress (Fig. 1). The ABA-PT and H-PT increased ADH activity and ethanol production in the roots (Figs 2, 3, 4). Under the stress, declines in ATP and total adenine nucleotides were much slower in the ABA-PT and H-PT roots than the N-PT roots (Fig. 5). Thus, the present results suggest that the ABA-PT and H-PT may increase anoxia tolerance due to maintenance of the glycolytic flux for production of ATP under oxygen-limiting conditions. Measurement of endogenous ABA levels, however, showed that they were not increased by the H-PT and anoxic stress (Table 1), showing that the H-PT does not increase tolerance through an increased endogenous ABA level. In addition, survivability, ethanol and adenine nucleotides in H-PT roots were somewhat greater than those in ABA-PT roots.
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Notes |
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1 Fax: +81 87 891 3086. E-mail: hisashi{at}ag.kagawa\|[hyphen]\|u.ac.jp
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Abbreviations |
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ABA, abscisic acid; ABA-PT, ABA-pretreatment or ABA-pretreated; ADH, alcohol dehydrogenase; Adh, alcohol dehydrogenase gene; H-PT, hypoxic-pretreatment or hypoxic-pretreated; N-PT, non-pretreatment or non-pretreated..
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