Journal of Experimental Botany, Vol. 52, No. 354, pp. 145-151,
January 2001
© 2001 Oxford University Press
Original Papers |
Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings
1 Hokkaido National Agricultural Experiment Station, Hitsujigaoka 1, Toyohira-ku, Sapporo 062-8555, Japan
2 Hokkaido Green-Bio Institute, Naganuma, Hokkaido 069-1301, Japan
Received 19 July 2000; Accepted 16 August 2000
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Abstract |
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Rice (Oryza sativa L.) seedlings, when kept at 42 °C for 24 h before being kept at 5 °C for 7 d, did not develop chilling injury. Chilling resistance was enhanced in parallel with the period of heat-treatment. The level of APX activity was higher in heated seedlings whereas CAT activity was decreased by heat stress. There was no significant difference in SOD activity between heated and unheated seedlings. The elevated activity of APX was sustained after 7 d of chilling. The cytosolic APX gene expression in response to high and low temperature was analysed with an APXa gene probe. APXa mRNA levels increased within 1 h after seedlings were exposed to 42 °C. Elevated APXa mRNA levels could also be detected after 24 h of heating. The APXa mRNA level in preheated seedlings was still higher than unheated seedlings under cold stress. The promoter of the APXa gene was cloned from rice genomic DNA by TAIL-PCR, and characterized by DNA sequencing. The promoter had a minimal heat shock factor-binding motif, 5'-nGAAnnTTCn-3', located in the 81 bp upstream of the TATA box. Heat shock induction of the APXa gene could be a possible cause of reduced chilling injury in rice seedlings.
Key words: Heat shock, chilling tolerance, ascorbate peroxidase, rice.
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Introduction |
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Many plants indigenous to the tropics and subtropics suffer chilling injury upon exposure to non-freezing temperatures below 12 °C (Lafuente et al., 1991
). Although some chilling-sensitive plants can be hardened, i.e. they exhibit increased resistance to chilling stress after exposure to intermediate temperatures (Moynihan et al., 1995), a few chilling-sensitive plants, including rice seedlings, do not show hardening.
In chilling-sensitive plants, oxidative stress is a major component of chilling stress (Hodges et al., 1997; Pinhero et al., 1997). Active oxygen species (AOS) such as hydrogen peroxide, superoxide radicals and hydroxyl radicals can react very rapidly with DNA, lipids and proteins, which causes severe cellular damage (Van Breusegem et al., 1999). Although AOS were thought to be involved in light-associated chilling stress, molecular and biochemical evidence was presented to indicate that low temperature also imposes oxidative stress in dark-grown maize seedlings during chilling treatment (Prasad et al., 1994a).
Several enzymes can efficiently detoxify AOS, however, during prolonged stress conditions, such detoxification systems get saturated and damage occurs (van Breusegem et al., 1999). A major hydrogen peroxide-detoxifying system in plant chloroplasts and cytosol is called the ascorbate-glutathione cycle, in which ascorbate peroxidase (APX) is the key enzyme (Asada, 1992).
Prior exposure to heat-shock temperatures has been shown to increase the tolerance of sensitive tissue to subsequent chilling (Lurie and Klein, 1991; Saltveit, 1991). Heat shock can result in oxidative stress, which induces the genes involved in the oxidative stress defence system (Morgan et al., 1986). In fact, pea and Arabidopsis apx1 gene expressions are induced by heat stress as well as oxidative stress and both have heat shock cis elements in their promoters (Mittler and Zilinskas, 1992, 1994; Storozhenko et al., 1998).
In the present study, the effect of prior high temperature exposure on the susceptibility of rice seedlings to chilling injury was examined. Changes in APX activity and the induction of transcriptions after exposure to high temperature were evaluated. This was carried out to determine the possible role of APX in increasing the chilling tolerance to plants previously subjected to high temperature. An analysis of the rice APXa gene promoter is also presented.
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Materials and methods |
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Plant material
Rice seeds (Oryza sativa L., cv. Kirara 397) were imbibed for 3 d in water at 27 °C and sown in moist vermiculite in 9 cm diameter plastic Petri dishes, and germinated in the dark at 25 °C and 80% RH. After 7 d, seedlings were exposed to 42 °C at 100% RH for 1, 3, 9, and 24 h before chilling at 5 °C at 80% RH in light or darkness for 7 d. Control seedlings were exposed to 25 °C. After chilling, rice seedlings were transferred to 25 °C in the growth chamber and grown for 7 d. The seedlings were evaluated for their percentage survival based on the observations that actively growing seedlings were identified as survivors and the non-growing and wilted seedlings were identified as non-survivors. All of the experiments were repeated at least twice.
Assays of APX, CAT and SOD
Leaves were homogenized with 50 mM phosphate buffer (pH 7.0) containing 1% Triton X-100. The homogenate was centrifuged at 12 000 g for 20 min at 4 °C and the supernatant was immediately used for the enzyme assay.
APX activity was determined (Saruyama and Tanida, 1995). The reaction mixture (1.0 ml) was composed of 50 mM potassium phosphate (pH 7.0) containing NaN3, 0.5 mM ascorbate, 1.54 mM H2O2, and the enzyme fraction. The oxidation of ascorbate was started by the addition of H2O2 and the decrease in the absorbance at 290 nm was monitored. Catalase (CAT) activity was measured by measuring the decrease in absorbance at 240 nm (as described by Tanida, 1996). Superoxide dismutase (SOD) activity was assayed by using an assay kit (SOD-Test Wako) based on NBT method (Beyer and Fridovich, 1987).
RNA analysis
The rice cytosolic APX gene probe was amplified by PCR from cDNA prepared from leaves of 24 h of heated rice seedlings using Taq DNA polymerase (GIBCO BRL) and the primers 5'-ACCCGCAGCCATGGCTAAGAACTAC-3' and 5'-ACTAGAAACCTCTTAAGCATCAGCG-3'. Primers were designed according to the known cDNA sequence of the rice APXa (Morita et al., 1997). The cloned PCR fragment was sequenced and was identical to the rice APXa. Total RNA was extracted from 1 g of shoots of rice seedlings by phenol/SDS method and purified by ethanol precipitation and LiCl precipitation. Purified total RNA (20 µg) was electrophoresed in 1.2% agarose gel and transferred onto nylon membrane, and allowed to hybridize with 32P-labelled APXa gene probe. Hybridization signals were visualized by an autoradiogram and a bio-imaging analyser (FUJIX, BAS 1000).
Isolation and analysis of rice APXa gene promoter
The upstream region of the APXa was amplified by the method of thermal asymmetric interlaced polymerase chain reaction (TAIL-PCR) from rice genomic DNA (as reported by Liu et al., 1995). The APXa-specific primers TR1 (5'-GTAGGAGATGGTGGGTATCT-3'), TR2 (5'-TATCTCCTCCTTGATGGGCT-3') and TR3 (5'-TCACGACGGGGTAGTTCTTA-3') were synthesized according to the known cDNA sequence of the rice APXa (Morita et al., 1997). In addition, an arbitrary degenerate primer, AD (GTNCGASWCANAWGTT) was synthesized (according to Liu et al., 1995). Three PCR reactions were carried out sequentially to amplify target sequences using nested APXa-specific primers (TR1, TR2 and TR3) on one side and an AD primer on the other. Amplified products from tertiary reaction with TR3 and AD were electrophoresed in 1.2% agarose gel, and a 400 bp fragment was eluted from the gel and cloned into pCRII vector by using TA-cloning (Invitrogen). The insert DNA was sequenced by using DNA sequencer (LIC-4200LS-2, Aloka).
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Results |
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Effect of prior high temperature exposure on the susceptibility of rice seedlings to chilling injury
Rice seedlings exposed to chilling temperature (5 °C) for 7 d developed severe symptoms of chilling injury (Fig. 1A
). Heating seedlings for 24 h at 42 °C before moving them to 5 °C prevented the development of these symptoms (Fig. 1B). When heated seedlings were placed for 4 d at 25 °C before being transferred to the low temperature, seedlings were no longer resistant to chilling (data not shown).
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The effects of different periods of heat treatment on resistance to chilling stress in rice seedlings were shown in Fig. 2
. After heating at 42 °C for 6 h, followed by chilling at 5 °C for 7 d, more than 50% of seedlings survived. During chilling treatment no significant difference was observed in the protective effect of a heat-shock pretreatment between dark-grown seedlings and light-grown seedlings. Chilling resistance was enhanced in parallel with the period of heat treatment. Twenty-four hours of exposure to 42 °C resulted in a drastic increase in survival rate after chilling.
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APX, CAT and SOD activities in response to heat and chilling stress
Changes in APX, CAT and SOD activity after exposure to 42 °C were evaluated. The total protein amounts were decreased at the highest rate of 10% after 24 h of heating (data not shown). The level of APX activity was higher in seedlings exposed to 42 °C whereas CAT activity in heated seedlings declined to lower levels. There was no significant difference in SOD activity between heated and unheated seedlings (Fig. 3). The effects of chilling stress on the activity of these enzymes in heated seedlings were examined (Fig. 4). The elevated activity of APX caused by heat stress slightly decreased but was still sustained at moderate levels under chilling. In contrast, the activity of CAT was drastically decreased by chilling stress. There was no significant difference in SOD activity between chilled and unchilled seedlings (Fig. 4). The increased and sustained activity of APX may be important in relation to the observed changes in the susceptibility of rice seedlings to chilling injury.
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APXa mRNA levels in response to heat and chilling stress
A cDNA encoding the cytosolic APX was cloned from heated rice seedlings. The clone was identical in DNA sequence to rice APXa (reported by Morita et al., 1997). To determine whether heat and chilling stress has an effect on the cytosolic APX mRNA levels, APXa gene expression was analysed with the APXa gene probe. This analysis revealed a 1.8-fold increase in a level of APXa mRNA after 1 h of heat stress (Fig. 5). Elevated APXa mRNA levels could also be detected after 6, 9, 12, and 24 h of heat stress. APXa mRNA levels declined under 7 d of cold stress both in preheated and control seedlings. However, the APXa mRNA level in preheated seedlings was still higher than unheated seedlings under cold stress (Fig. 5).
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Analysis of APXa promoter sequence
The upstream region including the promoter of the APXa gene was cloned from rice genomic DNA by TAIL-PCR. A 400 bp fragment amplified by the third nested PCR was characterized by DNA sequencing. The region had very low similarity to the Arabidopsis apx1 gene promoter except for one region located in the 81 bp upstream of the TATA box, which contains putative heat shock element (HSE) nGAAn and nTTCn (Fig. 6A). The HSE had a minimal heat shock factor (HSF) binding motif 5'-nGAAnnTTCn-3' which was the same as HSE of the Arabidopsis apx1 promoter (Fig. 6B). The CCAAT motif was also found at the -215 position.
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Discussion |
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Exposure of plants to one stress can elicit responses similar to those after exposure to other stresses and sometimes can protect the plant against another stress (Lurie and Klein, 1991
). The objective of this study was to determine whether heat stress could confer tolerance to low-temperature stress in rice seedlings. The data presented here clearly demonstrate that a treatment of rice seedlings at 42 °C before chilling at 5 °C prevented chilling injury. Similar effects have been found in many plants such as avocado (Woolf et al., 1995), cucumber (Lafuente et al., 1991; Jennings and Saltveit, 1994; McCollum et al. 1995), pepper (Mencarelli et al., 1993), and tomato (Lurie and Klein, 1991; Sabehat et al., 1996).
Studies on heat-stressed tomato fruits have shown a correlation between the accumulation of small heat shock proteins (smHSPs) and the acquisition of chilling tolerance (Sabehat et al., 1996, 1998; Kadyrzhanova et al., 1998). Some smHSPs may protect plants against chilling injury by preventing denaturation of proteins from chilling (Sabehat et al., 1998; Ukaji et al., 1999). Thus, smHSPs are assumed to be involved in the process to increase the chilling tolerance.
However, the primary cause of chilling injury was believed to be lipid peroxidation caused by an increase in oxygen radical generation induced by chilling stress (Prasad et al., 1994a, b). It was concluded that the tolerance of rice cultivars to chilling injury is closely linked to the cold stability of APX and CAT (Saruyama and Tanida, 1995). Therefore, the question whether heat stress enhances the active oxygen-scavenging system such as APX, CAT and SOD, which contributes to the survival of chilled rice seedlings, was addressed. The measurement of changes in the activity of these enzymes after exposure to 42 °C confirmed that APX was up-regulated by heat stress. Furthermore, increased APX activity was sustained after 7 d of chilling at 5 °C. This finding strongly suggests that APX is involved in the activity to increase chilling tolerance by heat stress. The important role of APX in relation to the increase of oxidative tolerance has been reported for many plants (Morita et al., 1999; Schoner and Krause, 1990; Rao et al., 1996; Tanaka et al., 1985; Willekens et al., 1994; Kubo et al., 1995; Conklin and Last, 1995; Ushimaru et al., 1992; Orvar and Ellis, 1997). Furthermore, the higher affinity for H2O2 (Chen and Asada, 1989; Scandalios et al., 1972; Elia et al., 1992) suggests that APX can work at low temperature (Saruyama and Tanida, 1995).
It has been demonstrated that exposure of seedlings to 42 °C enhanced the APXa mRNA level within 1 h. The heat-shock induction of the gene suggested that the APXa gene promoter might have HSE, which are binding sites for the regulatory heat shock factor (Chen and Pederson, 1993). The promoter of the APXa gene was cloned and characterized by DNA sequencing. The APXa promoter had sequence motifs characteristic of HSE identified in promoters of all heat-shock-inducible genes. The putative HSE is the sole conserved sequence among promoters of Arabidopsis apx1, apx2, pea apx1, and rice APXa (Storozhenko et al., 1998). Recently, in vivo analysis of the interaction between recombinant tomato HSF and the Arabidopsis apx1 promoter confirmed that the apx1 HSE represents a functional HSF-binding site (Storozhenko et al., 1998). Furthermore, the apx1 promoter with a mutated HSE loses inducibility and even becomes repressed under the heat-shock treatment (Storozhenko et al., 1998). It is, therefore, possible that the HSE in the rice APXa promoter contributes to the heat shock induction of the APXa gene, although further experiments are necessary to show whether the HSE in the rice APXa promoter is recognized by the HSF.
Different protein isoforms of cytosolic APX are known in Arabidopsis (Storozhenko et al., 1998). It is considered that rice also has a few different isoforms of cytosolic APX. The contribution of the APXa to the total extractable foliar APX activity remains unknown and should be addressed in the future.
In summary, as far as is known, the present study is the first in which APX was closely monitored during heat treatment and subsequent chilling. The results suggest that APX may play a role in heat-treatment-mediated protection of rice seedlings against chilling injury.
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Notes |
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3 To whom correspondence should be addressed. Fax: +81 11 859 2178. E-mail: yutaka{at}cryo.affrc.go.jp
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References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Asada K.1992. Ascorbate peroxidase—a hydrogen peroxidase-scavenging enzyme in plants. Physiologia Plantarum85, 235–241.
Beyer WF, Fridovich I.1987. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry161, 559–566.[Web of Science][Medline]
Chen G-X, Asada K.1989. Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant and Cell Physiology30, 987–998.
Chen J, Pederson DS.1993. A distal heat shock element promotes the rapid response to heat shock of the HSP26 gene in the yeast Saccharomyces cerevisiae. The Journal of Biological Chemistry268, 7442–7448.
Conklin PL, Last RL.1995. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiology109, 203–212.[Abstract]
Elia MR, Borraccino G, Dipierro S.1992. Soluble ascorbate peroxidase from potato tubers. Plant Science85, 17–21.
Hodges DM, Andrews CJ, Johnson DA, Hamilton RI.1997. Antioxidant enzyme and compound responses to chilling stress and their combining abilities in differentially sensitive maize hybrids. Crop Science37, 857–863.
Jennings P, Saltveit ME.1994. Temperature and chemical shocks induce chilling tolerance in germinating Cucumis sativus (cv. Poinsett 76) seeds. Physiologia Plantarum91, 703–707.
Kadyrzhanova DK, Vlachonasios KE, Ververidis P, Dilley DR.1998. Molecular cloning of a novel heat induced/chilling tolerance related cDNA in tomato fruit by use of mRNA differential display. Plant Molecular Biology36, 885–895.[Web of Science][Medline]
Kubo A, Saji H, Tanaka K, Kondo N.1995. Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Molecular Biology29, 479–489.[Web of Science][Medline]
Lafuente MT, Belver A, Guye MG, Saltveit ME.1991. Effect of temperature conditioning on chilling injury of cucumber cotyledons. Plant Physiology95, 443–449.
Liu Y-G, Mitsukawa N, Oosumi T, Whittier RF.1995. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. The Plant Journal8, 457–463.[Web of Science][Medline]
Lurie S, Klein JD.1991. Acquisition of low-temperature tolerance in tomatoes by exposure to high-temperature stress. Journal of the American Society for Horticultural Science116, 1007–1012.
McCollum TG, Doostdar H, Mayer RT, McDonald RE.1995. Immersion of cucumber fruit in heated water alters chilling-induced physiological changes. Postharvest Biology Technology6, 55–64.
Mencarelli F, Ceccantoni B, Bolini A, Anelli G.1993. Influence of heat treatment on the physiological response of sweet pepper kept at chilling temperature. Acta Horticulturae343, 238–243.
Mittler R, Zilinskas BA.1992. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. The Journal of Biological Chemistry267, 21802–21807.
Mittler R, Zilinskas BA.1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. The Plant Journal5, 397–405.[Web of Science][Medline]
Morgan RW, Christman MF, Jacobson FS, Storz G, Ames BN.1986. Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proceedings of the National Academy of Sciences, USA83,8059–8063.
Morita S, Kaminaka H, Masumura T, Tanaka K.1999. Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; involvement of hydrogen peroxide in oxidative stress signalling. Plant and Cell Physiology40, 417–422.
Morita S, Kaminaka H, Yokoi H, Masumura T, Tanaka K.1997. Cloning and characterization of cytosolic ascorbate peroxidase cDNA from rice (accession No. D45434). Plant Physiology113,306.
Moynihan MR, Ordentlich A, Raskin I.1995. Chilling-induced heat evolution in plants. Plant Physiology108, 995–999.[Abstract]
Orvar BL, Ellis BE.1997. Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. The Plant Journal11, 1297–1305.
Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA.1997. Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiology114, 695–704.[Abstract]
Prasad TK, Anderson MD, Martin BA, Stewart CR.1994a. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. The Plant Cell6, 65–74.[Abstract]
Prasad TK Anderson MD, Stewart CR.1994b. Acclimation, hydrogen peroxide and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology105, 619–627.[Abstract]
Rao MV, Paliyath G, Ormrod DP.1996. Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiology110, 125–136.[Abstract]
Sabehat A, Lurie S, Weiss D.1998. Expression of small heat-shock proteins at low temperatures. Plant Physiology117, 651–658.
Sabehat A, Weiss D, Lurie S.1996. The correlation between heat-shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiology110, 531–537.[Abstract]
Saltveit ME.1991. Prior temperature exposure affects subsequent chilling sensitivity. Physiologia Plantarum82, 529–536.
Saruyama H, Tanida M.1995. Effect of chilling on activated oxygen-scavenging enzymes in low temperature-sensitive and -tolerant cultivars of rice (Oryza sativa L.). Plant Science109, 105–113.
Scandalios JG, Liu EH, Campeau MA.1972. The effects of intragenic and intergenic complementation on catalase structure and function in maize: a molecular approach to heterosis. Archives Biochemistry and Biophysics153, 695–705.[Web of Science][Medline]
Schoner S, Krause GH.1990. Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta180, 383–389.
Storozhenko S, Pauw PD, Van Montagu M, Inzé D, Kushnir S.1998. The heat-shock element is a functional component of the Arabidopsis apx1 gene promoter. Plant Physiology118, 1005–1014.
Tanaka K, Suda Y, Kondo N, Sugahara K.1985. O3 tolerance and the ascorbate-dependent H2O2 decomposing system in chloroplasts. Plant and Cell Physiology26, 1425–1431.
Tanida M.1996. Catalase activity of rice seed embryo and its relation to germination rate at a low temperature. Breeding Science46, 23–27.
Ukaji N, Kuwabara C, Takezawa D, Arakawa K, Yoshida S, Fujikawa S.1999. Accumulation of small heat-shock protein homologs in the endoplasmic reticulum of cortical parenchyma cells in mulberry in association with seasonal cold acclimation. Plant Physiology120, 481–489.
Ushimaru T, Shibasaka M, Tsuji H.1992. Development of the O2 detoxification system during adaptation to air of submerged rice seedlings. Plant and Cell Physiology33, 1065–1071.
Van Breusegem F, Slooten L, Stassart J-M, Moens T, Botterman J, Van Montagu M, Inzé D.1999. Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant and Cell Physiology40, 515–523.
Willekens H, Van Camp W, Van Montagu M, Inzé D, Langebartels C, Sandermann H.1994. Ozone, sulfur dioxide and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiology106, 1007–1014.[Abstract]
Woolf AB, Watkins CB, Bowen JH, Lay-Yee M, Maindonald JH, Ferguson IB.1995. Reducing external chilling injury in stored ‘Hass’ avocados with dry heat treatments. Journal of the American Society for Horticultural Science120, 1050–1056.
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