JXB Advance Access originally published online on November 29, 2004
Journal of Experimental Botany 2005 56(411):417-423; doi:10.1093/jxb/eri039
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RESEARCH PAPER |
Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat
Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK
To whom correspondence should be addressed. Fax: +44 (0)1582 763010. E-mail: christine.foyer{at}bbsrc.ac.uk
Received 27 May 2004; Accepted 24 September 2004
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Abstract |
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Plants co-ordinate information derived from many diverse external and internal signals to ensure appropriate control of gene expression under optimal and stress conditions. In this work, the relationships between catalase (CAT) and H2O2 during drought in wheat (Triticum aestivum L.) are studied. Drought-induced H2O2 accumulation correlated with decreases in soil water content and CO2 assimilation. Leaf H2O2 content increased even though total CAT activity doubled under severe drought conditions. Diurnal regulation of CAT1 and CAT2 mRNA abundance was apparent in all conditions and day/night CAT1 and CAT2 expression patterns were modified by mild and severe drought. The abundance of CAT1 transcripts was regulated by circadian controls that persisted in continuous darkness, while CAT2 was modulated by light. Drought decreased abundance, and modified the pattern, of CAT1 and CAT2 mRNAs. It was concluded that the complex regulation of CAT mRNA, particularly at the level of translation, allows precise control of leaf H2O2 accumulation.
Key words: Catalase, diurnal cycle, drought, hydrogen peroxide, Triticum aestivum L
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Introduction |
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Drought stress is a complex syndrome involving not only water deprivation but also nutrient limitation, salinity, and oxidative stresses. Moreover, levels of light that are optimal for photosynthesis in well-watered plants become excessive in plants suffering water deprivation. Photosynthesis is particularly sensitive to water deficit because the stomata close to conserve water as available soil water declines. Stomatal closure deprives the leaves of carbon dioxide and photosynthetic carbon assimilation is decreased in favour of photorespiratory oxygen uptake. The process of stomatal closure and the enhancement of flux through the photorespiratory pathway increase the oxidative load on the tissues as both processes generate reactive oxygen species (ROS), particularly hydrogen peroxide (H2O2). Hydrogen peroxide is also generated as a secondary messenger in abscisic acid (ABA)-mediated stomatal closure (Pei et al., 2000
). In photorespiration, H2O2 is produced at very high rates by the glycollate oxidase reaction in the peroxisomes (Noctor et al., 2002). Moreover, superoxide production by the photosynthetic electron transport chain (via the Mehler reaction) is exacerbated by drought (Noctor et al., 2002).
Plants respond to diverse environmental signals in order to survive stresses such as drought (Pastori and Foyer, 2002). Strategies to minimize oxidative damage are a universal feature of plant defence responses. Hydrogen peroxide is eliminated by catalases (CAT) and ascorbate peroxidases (Chen and Asada, 1989; Scandalios et al., 1997). These enzymes rapidly destroy the vast majority of H2O2 produced by metabolism, but they allow low steady-state levels to persist presumably to maintain redox signalling pathways (Noctor and Foyer, 1998).
Catalase is essential for the removal of H2O2 produced in the peroxisomes by photorespiration (Noctor et al., 2000). Catalase activities decrease under conditions that suppress photorespiration, such as elevated CO2 (Azevedo et al., 1998). The importance of CAT in photosynthetic cells is demonstrated by observations in CAT-deficient mutants (Kendall et al., 1983) and in transformed tobacco in which the major leaf CAT isoform is decreased by antisense technology (Takahashi et al., 1997; Willekens et al., 1997). When such plants are placed in conditions favouring high rates of photorespiration (low CO2, high light, warm temperatures), photosynthesis is inhibited, the foliar antioxidant system is perturbed, and necrotic lesions appear on the leaves. Moreover, induction of defence-related proteins is observed, both locally in the necrotic regions and in leaves which do not suffer necrosis (Takahashi et al., 1997; Willekens et al., 1997). However, the CAT protein is susceptible to photoinactivation upon exposure to high light intensities (Shang and Feierabend, 1999) and leaf CAT activities have been shown to decline in certain stress conditions (Hertwig et al., 1992). There is now considerable evidence to show that CAT is one of the most rapidly turned over proteins in leaf cells particularly in stress conditions. Catalase gene expression and translation, as well as CAT protein turnover, are regulated in a complex manner that is far from resolved.
Plant catalases are encoded by a small gene family, usually composed of three isozyme genes which exhibit fairly complex spatial and temporal patterns of expression throughout the plant life cycle (Scandalios et al., 1997; Willekens et al., 1997). The wide diversity of plant CAT sequences has led to some discrepancies in the isozyme correlation in phylogenetic trees. This has been investigated and a model for the evolutionary divergence of monocot and dicot CAT genes has been proposed (Iwamoto et al., 1998). The presence of a G-box or ABRE (ABA responsive) element in the maize CAT1 promoter allows increased expression in response to exogenous ABA and osmotic stress (Guan and Scandalios, 2000). An antioxidant responsive element (ARE) is also present in the promoters of CAT1 and CAT3 underlying the important protective role of CAT in response to oxidative stress (Polidoros and Scandalios, 1999). In addition, the expression of some CAT genes is under circadian control (Zhong and McClung, 1996; Polidoros and Scandalios, 1998). The aims of the present study were: (i) to determine the effect of drought on H2O2 content and CAT activity in relation to photosynthesis in the leaves of a major crop species, wheat; (ii) to examine the effects of stress on the day/night abundance of mRNAs encoding the two major leaf CAT isoforms, CAT1 and CAT2, and (iii) to establish relationships between leaf H2O2 content, CAT activity, and CAT1 and CAT2 transcripts under optimal and stress conditions.
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Materials and methods |
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Plant material and growth conditions
Wheat (Triticum aestivum L.) plants were sown in individual pots and grown in a glasshouse at 20 °C and 550 µmol quanta m–2 s–1 at canopy height, as described by Noctor et al. (2002)
. Four varieties were used in this study: the spring varieties ‘Canon’ and ‘Cadenza’, the model cultivar ‘BobWhite’, and the winter variety ‘Buster’. The maximum soil-water content recorded in these experiments for well-watered conditions was 60%. Five-week-old plants of the four varieties were subject to mild and severe drought. Mild drought delivered a gradual water deprivation of 16 plants for up to 6 d, a point equivalent to a reduction to 40% of the original soil water content at day 6. Plants subject to mild drought were well-watered 12 h before the commencement of the treatment and provided with a lower reservoir of water throughout the experiment. Severe drought was carried out by rapid desiccation of 20 plants over 2–4 d to a final soil water content of 15–20% at the final harvest point. In these conditions, plants were well-watered 12 h before the treatment and the plants thereafter had no water supply throughout the duration of the drought period. Well-watered plants irrigated from above and below, of the same age were used as controls: 10 plants at the beginning of the treatment (control) and eight plants at the end of the treatment (developmental control). Three independent experiments were performed using third leaves from each individual plant, which were excised each day at 09.00 h, quickly frozen in liquid N2, and stored at –80 °C until extraction. Third leaves from three individual plants and three independent experiments were used for molecular analyses. CO2 assimilation was measured by an infrared gas exchange analyser (model WA-225-MK3, ADC, Hoddesdon, Hertfordshire, UK). Stomatal conductance was estimated from water vapour measured by infrared gas analysis as above. Studies on circadian rhythm were carried out in two independent experiments using 5-week-old ‘Cadenza’ plants, which were grown and treated as described above. Third leaves collected from six control plants, six mild-stressed plants, and six severely-stressed plants at different times during the day/night cycle, were frozen at –80 °C until extraction.
Analysis of CAT gene expression by RT-PCR
Gene sequences from wheat or Arabidopsis were obtained from the GenBank database. The accession numbers and primers designed for the sequences analysed are: Arabidopsis Actin-1 M20016
[GenBank]
; ATACT-F, 5'-GAGAAGATGACTCAGATC-3' and ATACT-R, 5'-ATCCTTCCTGATATCGAC-3'; wheat CAT1 E16461
[GenBank]
, CAT1-F, 5'-ACTACGACGGGCTCATG-3' and CAT1-R: 5'-GGAGCTGAGACGGCTTC-3'; wheat CAT2 X94352
[GenBank]
, CAT2-F, 5'-CCTTAATCAGCAGGGATG-3' and CAT2-R, 5'-AGATAGAACACGCGGAG-3'. PCR reactions were performed using a programmable Robocycler at annealing temperatures of 44 °C for Actin and 46 °C for CAT. For an accurate comparison and quantification of the transcript levels, the exponential phase of PCR amplification was determined by establishing the number of PCR cycles where the products exhibit an exponential phase: 35 cycles for Actin PCR products and 30 cycles for CAT PCR products. The identity of all PCR products was confirmed by sequencing analysis at the Department of Biochemistry of Oxford University.
H2O2 and catalase activity measurements
Leaf H2O2 contents and catalase activity were measured on the third leaf of control and drought-treated wheat plants. H2O2 was determined as in Veljovic-Jovanovic et al. (2002). Catalase activity was assayed as described by Vanacker et al. (2000) using 0.1 M HEPES pH 6.5, 10 mM MgCl2, and 5 mM EDTA.
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Results |
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Photosynthesis, leaf catalase activity, H2O2 accumulation and drought
The relationships between soil water content and leaf photosynthetic CO2 assimilation rates were similar in the three varieties ‘Canon’, ‘Cadenza’ and ‘Buster’ (Fig. 1). Severe inhibition of photosynthesis was observed only when the soil water content decreased to below 30%. Leaf water potentials and stomatal conductance showed similar trends with respect to drought in all varieties (Fig. 2). Based on these results, ‘Cadenza’ was chosen for further investigation and two experimental regimes (mild drought and severe drought) were identified from the data presented in Figs 1 and 2. ‘Mild drought’ is classified as exposure to gradual decreases in soil water to as low as 40% over 6 d. Severe drought is defined as exposure to rapid decreases in soil water to as low as 15–20% over 2–4 d. CO2 assimilation rates together with soil water content and stomatal conductance, were estimated in each of the following experiments: they did not vary from the pattern shown in Figs 1 and 2, and are hence not included here. Total leaf catalase activity was significantly increased only in response to severe drought, when the soil water content was less than 20% (Fig. 3). Leaf H2O2 concentrations, on the other hand, increased progressively as soil water content decreased (Fig. 4).
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Drought-induced shifts in the diurnal cycle of CAT gene expression
The abundance of CAT1 and CAT2 transcripts fluctuated over the day/night cycle in well-watered plants and this pattern was modified by drought (Fig. 5). Catalase1 mRNA levels were highest early in the light period (after 4 h) and lowest after 1 h dark (Fig. 6A). Catalase2 mRNA levels were also highest in the light, with a maximum after 12 h illumination (Fig. 6D). Like CAT1, CAT2 transcripts decreased rapidly following the transition to darkness with minimal values obtained after 1 h in the dark (Fig. 6D). To investigate whether these changes represented a diurnal rhythm in gene expression the fluctuations of CAT transcript levels were analysed over the 24 h light/dark cycle maintaining one set of plants in continuous darkness (Fig. 6A, D). The pattern of CAT1 expression in leaves maintained in complete darkness was almost identical to the pattern observed in control leaves maintained in the regular day/night conditions during the first 24 h. By contrast, the pattern of abundance of CAT2 transcripts was markedly shifted upon exposure to continuous dark (Fig. 6A, D). This suggests that CAT1 is regulated by circadian controls while CAT2 is modulated by light/dark.
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The pattern of CAT1 transcript abundance was modified by water deficit, with diurnal changes significantly shifted in time and intensity under mild and severe drought conditions (Fig. 6B, C). In plants subjected to mild drought the pattern of CAT1 expression was basically similar to that of the water-replete control with two maximal peaks at 09.00 h and 17.00 h. However, the CAT1 peak of expression at 17.00 h was strongly enhanced under mild drought compared with water-replete conditions, peak intensity being increased by about 2.5-fold. A different pattern of CAT1 transcript accumulation was observed in plants subjected to severe water stress (Fig. 6C). In this case, only one peak of CAT1 expression was observed. This occurred at 13.00 h, 4 h earlier than the peak observed in mild drought (Fig. 6B). Moreover, the increase in the peak of CAT1 transcripts was lower than that observed under mild drought (Fig. 6B, C).
The pattern of CAT2 transcript abundance was also modified by drought (Fig. 6D–F). In well-watered leaves, two significant peaks of CAT2 expression were observed, one occurring during the day at 17.00 h and the second was observed at night (after 5 h darkness). The pattern of CAT2 expression was also clearly different under mild and severe drought (Fig. 6E, F). Under mild drought, two significant peaks of CAT2 expression were observed during the day, at 09.00 h and 17.00 h. By contrast, the intensity of change in CAT2 expression was greatly decreased under severe drought with a small increase at 13.00 h (Fig. 6E, F).
Drought effects on photosynthetic performance in the light
Leaf CO2 assimilation began immediately when the light was switched on in all cases, with little indication of an induction period. Photosynthesis rapidly attained stable maximal rates, that were maintained throughout the light period in water-replete leaves (Fig. 6G). By contrast, leaves exposed to water stress showed a marked induction period before CO2 assimilation reached maximal rates (Fig. 6H, I). Moreover, overall photosynthesis performance was lower in water-stressed leaves than water-replete controls (Fig. 6H, I). For example, CO2 assimilation rates were between 25 and 30 µmol m–2 s–1 in water-replete leaves (Fig. 6G) and leaves exposed to mild drought (Fig. 6H), whereas maximal values no higher than 15 µmol m–2 s–1 were measured under ‘severe’ drought conditions (Fig. 6I). Moreover, a progressive decline in the rate of CO2 assimilation during the light period was found in leaves subjected to both mild and severe water stress (Fig. 6H, I).
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Discussion |
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Water availability is one of the major factors limiting plant productivity in the field. Photorespiration is greatly enhanced as a result of water deficits because the stomata close and CO2 assimilation is inhibited. The effects of limiting CO2 availability (as occurs when stomata close) on rates of wheat leaf H2O2 formation, extrapolated from measured rates of photosynthesis and photorespiration have previously been calculated (Noctor et al., 2002
). The robustness of plant cells to H2O2 and other oxidants is due to effective controls of oxidant levels by a versatile leaf antioxidative system. The general responses of wheat leaf antioxidants to drought are well documented (Smirnoff and Colombe, 1988; Pastori and Trippi, 1993; Menconi et al., 1995; Bartoli et al., 1999). This, together with an understanding of the crucial role of CAT in removal of H2O2 formed by photorespiration led to the present study being focused on the drought-induced regulation of catalase and H2O2 accumulation. The results presented here show that (i) H2O2 accumulates in wheat leaves in response to drought as water is depleted from the soil; (ii) CAT activity significantly increases only under severe drought; (iii) day/night CAT1 and CAT2 expression patterns are modified by mild and severe drought; and (iv) drought-induced changes in CO2 assimilation rates are comparable to those obtained in other studies.
Endogenous circadian rhythms in the activities of free radical detoxification enzymes are found in all living organisms (Hardeland, 2000). These are often associated with rhythms in metabolism, such as regulation of photosynthesis, that generate cycles in cellular redox state. Environmental signals and oxidative stress modify circadian controls (Hardeland, 2000), thus drought-induced changes in CAT expression patterns are not surprising. Similar responses have been reported in other drought-responsive genes (Carpenter et al., 1994; Cellier et al., 2000; Thompson and Corlett, 1995). It is shown that the expression of CAT1 and CAT2 is modulated by light in wheat as it is in maize and Arabidopsis (Acevedo et al., 1991; McClung, 1997). Wheat CAT1 expression shows characteristics of circadian control, as indicated by the persistence of the rhythm in darkness, and its expression pattern is equivalent to the clock-regulated maize CAT3 and Arabidopsis CAT2 genes (Acevedo et al., 1991; Zhong et al., 1994). Instead, CAT2 expression does not appear to be clock-regulated in wheat, similar to results reported for maize CAT2 and Arabidopsis CAT1 (Acevedo et al., 1991; McClung, 1997). Catalase isozyme gene correlations between species, and a model for the evolutionary divergence of CAT genes, have been proposed by Iwamoto et al. (1998). The results presented here agree with those of previous studies on CAT gene expression (Guan and Scandalios, 2000). Hence CAT1 and CAT2 transcript abundance is highest in the light and broadly correlated with H2O2 formation in photorespiration. However, the extent of CAT mRNA accumulation in leaves of plants experiencing drought is lower than that observed in well-watered plants in the light. The increase in CAT activity observed in leaves experiencing water deficits cannot therefore be explained by enhanced transcription. Translation of CAT mRNAs depends on the supply of the methyl group donors, from glycine and serine, whose production is greatly enhanced by photorespiratory carbon flow (Schmidt et al., 2002). Catalase protein synthesis is therefore linked to the photosynthetic and photorespiratory pathways (Schmidt et al., 2002).
It might be asked why regulation of CAT has this high degree of complexity. The answer must reside in the requirement of a precise control of leaf H2O2 levels. The role of H2O2 in stress-induced damage has long been recognized, but it is now also generally accepted that H2O2 is an integral component of cell signalling cascades (Mittler, 2002; Vranova et al., 2002) and an indispensable second messenger in biotic and abiotic stress situations (Green and Fluhr, 1995; Pastori and Foyer, 2002). More recently H2O2 has been reported to be intimately involved in a wide range of hormone-dependent developmental signalling processes, as well as in cell wall cleavage and associated cell wall growth (reviewed by Foyer and Noctor, 2003). Hydrogen peroxide is also considered to fulfil a signalling role in guard cells through the control of stomatal closure (Schroeder et al., 2001; Kohler et al., 2003). It was concluded that CAT regulation serves to limit excessive H2O2 accumulation while allowing essential signalling functions to occur.
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Acknowledgements |
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CM Luna gratefully acknowledges support from the Royal Society, UK (two short-term fellowships). Rothamsted Research receives grant-aid support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom.
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Footnotes |
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* Present address: Instituto de Fitopatología y FisiologíaVegetal (IFFIVE)-INTA, Camino 60 cuadras Km 51/2, 5009 Cordoba, Argentina.
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