Journal of Experimental Botany, Vol. 51, No. 346, pp. 945-953,
May 2000
© 2000 Oxford University Press
Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo)
Institut Universitaire de Technologie Génie Biologique, 100 rue de l'égalité, 15000 Aurillac, France
Received 29 September 1999; Accepted 24 January 2000
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Abstract |
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The effects of zinc on growth, mineral content, chlorophyll a fluorescence, and detoxifying enzyme activity (ascorbate peroxidase (APX), EC 1.11.1.11; superoxide dismutase (SOD), EC 1.15.1.1) of ryegrass infected or not by Acremonium lolii, and treated with nutrient solution containing 0–50 mM ZnSO4 were studied. The introduction of zinc induces stress with a decrease in growth at 1, 5 and 10 mM ZnSO4 and a cessation of growth at 50 mM ZnSO4, in ryegrass plants infected by A. lolii or not. This decrease in growth may be due to an accumulation of zinc in leaves. Nevertheless, symbiotic plants showed higher values in tiller number, an advantage conferred by the fungus. After 24 d of Zn exposure, leaf fresh weights and leaf water content were lower in plants growing with Zn in the culture medium and no advantage was conferred by the fungus to its host. An increase in Zn supply resulted in a decrease of the Ca, K, Mg, and Cu content of the leaves, a reduction in the quantum yield of electron flow throughout photosystem II (
F/
and a lowering of the efficiency of photosynthetic energy conversion (Fv/Fm), compared to control plants. To counter this zinc stress, detoxifying enzymes APX and SOD increased (100%) when Zn reached the value of 50 mM in the nutrient solution. At 10 mM ZnSO4, the presence of the fungus in the plant led to an increase in the threshold toxicity of plants to zinc by a diminution of APX activity. Key words: Zinc toxicity, Lolium perenne, Acremonium lolii, antioxidant enzymes, chlorophyll a fluorescence.
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Introduction |
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In nature, the endophyte Acremonium lolii exists exclusively in a symbiotic relationship with perennial ryegrass (Lolium perenne, Siegel et al., 1985
; Clay, 1988). This endophytic fungus is dependent on the host for nutrition and transmission and, in return, provides its host with a defence against herbivory (Siegel et al., 1987). The greatest concentrations of endophyte occur in the basal portion of the leaf sheath and in the seed. It is now widely accepted that plants infected with endophytic fungi are often at a distinct advantage in times of biotic and abiotic stress compared to their endophyte-free counterparts (Latch, 1993). For example, under water-deficit conditions, some genotypes of symbiotic plants have been shown to have increased root growth (Knox and Karnok, 1992; Latch et al., 1985), greater photosynthesis (Bacon, 1993) and enhanced osmotic adjustment (West et al., 1990) compared to non-symbiotic individuals. At the present time, very little is known about the influence of this fungus concerning the protection of the plant faced with toxic concentrations of heavy metals in natural soils.
Among heavy metals, zinc is an important element for both plants and animals. It plays an important role in several plant metabolic processes, it activates enzymes and is involved in protein synthesis and in carbohydrate, nucleic acid and lipid metabolism. It forms complexes with DNA and RNA and affects the stability of these compounds (Collins, 1981; Pahlsson, 1989).
Heavy metal contamination of soils is one of the major environmental stresses for higher plants and there is increased interest in the use of plants to decontaminate soils polluted by heavy metals. In this process, called phytoremediation, higher plants are used to absorb contaminants from the soil into their roots and translocate them to shoots. However, when accumulated in excess in sensitive plant tissues, these components cause alterations in various vital growth processes, such as transpiration (Richardson et al., 1993), photosynthesis and photosynthetic electron transport (Krupa, 1993; Maksymiec and Baszynski, 1996; Yruela et al., 1996), biosynthesis of chlorophyll (Mocquot et al., 1996), as well as cell membrane integrity (De Vos et al., 1993; Sinha et al., 1997). In particular, zinc has been reported to have a negative effect on mineral nutrition (Chaoui et al., 1997; Ouariti et al., 1997) and enzyme activities related to metabolism (Ouariti et al., 1997; Ouzounidou et al., 1995; Van Assche and Clijsters, 1986).
The increased production of toxic oxygen derivatives can be caused by both natural and stress situations (Kampfenkel et al., 1995; Weckx and Clijsters, 1997). These highly cytotoxic species of oxygen can seriously disrupt normal metabolism through oxidative damage to cellular components (Halliwell, 1982). One of the most damaging effects of these molecular species and their products in cells is the peroxidation of membrane lipids (Tappel, 1973; Halliwell, 1982). An excess of redox active metals, for example, copper and iron, as well as metal ions unable to perform univalent oxidoreduction reactions, such as zinc, induces oxidative damage (Luna et al., 1994; Kampfenkel et al., 1995) and are also capable of affecting lipid peroxidation and antioxidative protection (Gora and Clijsters, 1989).
To counteract this metabolic dysfunction caused by abiotic stress, higher plants employ defence strategies. Effectively, in order to survive, plants need to respond to environmental stresses through a variety of biochemical reactions. To protect themselves from heavy metal poisoning, plant cells must develop a mechanism by which the metal ion, entering the cytosol of the cell, is immediately complexed and inactivated. This process is mediated by phytochelatins (Zenk, 1996). For their protection, plant cells are also equiped with oxygen radical detoxifying enzymes, such as superoxide dismutase (SOD) and ascorbate peroxidase (APX) (Asada, 1987; Foyer and Harbinson, 1994). The key role of superoxide dismutase in the protection against harmful oxidative reaction resulting from metal stress has been reported previously (Monk et al., 1989).
Thus, the aim of this study was to observe the consequences of the application of zinc (ZnSO4) in the culture medium of a perennial ryegrass (Lolium perenne L. cv Apollo), whether infected or not by the endophyte, Acremonium lolii. The behaviour of these two types of plant was compared through a study of growth, photosynthetic activity and antioxidant enzyme activities. The aim was to achieve a better understanding of the effects of zinc on oxidative stress and on the possible induction of a defence mechanism in ryegrass, and to see the influence of the fungus in the defence strategies of the plant against this heavy metal.
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Materials and methods |
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Material and growth conditions
Half of the ryegrass seeds (Lolium perenne L. cv. Apollo), infected by Acremonium lolii were treated with Triticonazole (1 g/100 mg) in order to eliminate the endophyte. The seeds were then germinated in vermiculite at 25 °C in the dark for 10 d. Seedlings were transferred to 1.0 l pots (2 plants per pot and 40 plants per treatment: 20 infected (I) and 20 not infected (NI)) containing a mixture of blond peat/pouzzolane (1/4–3/4), and watered daily with 150 ml of a nutrient solution (Coïc and Lesaint, 1975
). Plants were grown in a growth chamber (16/8 h light/dark) under lamps providing a light intensity of 400 µmol m-2 s-1, day/night temperature of 22/18 °C and 50/70% relative humidity. The presence of the endophyte in tillers and leaves was tested in infected plants as well as its absence in non-infected plants (Latch et al., 1984). Treatments were started after 45 d (corresponding to day 0 of the experiment) by adding 0 (control), 1, 5, 10, and 50 mM ZnSO4.7H2O to the nutrient solution. On days 0, 7, 10, 13, 17, 21, and 24, some leaves were frozen in liquid nitrogen and stored at -80 °C until use. At the end of the experiment (day 24), all tillers and leaves of the plants were harvested, weighed to determine fresh weight, and then dried after at least 5 d desiccation at 80 °C. The dry and fresh weights were used as a measure of growth.
Determination of tiller number
On days 7, 15 and 24 of the experiment, the number of tillers per plant was determined, and the value thus obtained was divided by the value obtained on day 0, in order to eliminate the heterogeneity of the plants at the beginning of the experiment.
Water content of the leaves
This parameter was expressed, using the values obtained for fresh and dry weights of all plants, according to (FW–DW)x100/FW.
Chlorophyll a fluorescence analysis
Measurements (days 0, 3, 7, 10, 13, 17, 21, and 24) of chl a fluorescence in air were made at room temperature in the growth chamber using the portable fluorescence monitoring system (FMS1, Hansatech Instruments Ltd., King's Lynn, UK). The parameters used to define the yield and quenching mechanisms of chl a fluorescence were those described previously (Genty et al., 1989) F/
, quantum yield of electron flow throughout photosystem II; Fv/Fm, maximal photochemical efficiency of the PSII, measured in pre-darkened (for 30 min) leaves). During the whole experiment, the measurements were always made on the same leaves.
Mineral analysis
The mineral content (Ca, K, Mg, Cu, Zn) of leaf tissue was determined by induction coupled plasma after dried mineralization of the dried material in HCl (Standard NFEN ISO 11885).
Enzyme measurements
Superoxide dismutase.
Frozen leaf tissue (100–150 mg) was ground in liquid nitrogen and homogenized in 1.5 ml of 0.25 M sucrose. The homogenate was centrifuged at 17 000 g for 20 min at 4 °C and the supernatant was used for the measurements. The activity of SOD (EC 1.15.1.1) was measured by the method of Nishikimi et al. (Nishikimi et al., 1972) and modified by Kakkar et al. (Kakkar et al., 1984). The assay mixture contained sodium pyrophosphate buffer (pH 8.3, 21 mM), 6.2 µM phenazine methosulphate, 30 µM nitro-blue tetrazolium (NBT), 52 µM NADH, and extract. The reaction was started by the addition of NADH. After incubation at 30 °C for 90 s, the reaction was stopped by the addition of 1 ml glacial acetic acid. The specific activity of the enzyme was determined (U mg-1 protein); one unit of SOD activity was defined as the amount of enzyme required to result in a 50% inhibition of the rate of NBT reduction measured at 560 nm.
Ascorbate peroxidase.
Frozen leaf tissue (100–150 mg) was ground in liquid nitrogen and homogenised in 1.5 ml of extraction medium containing HEPES 200 mM (pH 7.8), EDTA 2 mM, MgCl2 5 mM, DTT 1 mM, and sodium ascorbate 4 mM. The crude extract was centrifuged at 16 000 g for 5 min at 4 °C, and the supernatant was used for the measurements. Ascorbate peroxidase (EC 1.11.1.11) was measured spectrophotometrically according to Nakano and Asada (Nakano and Asada, 1987), modified by Vanacker et al. (Vanacker et al., 1998). The reaction mixture contained NaH2PO4 50 mM (pH 7), 500 µM ascorbate, 1 mM H2O2, and extract. A fall in absorbance at 290 nm was measured as ascorbate was oxidized. APX specific activity (nmol min-1 mg-1 protein) was calculated using an extinction coefficient of 2.8 mM-1 cm-1 for ascorbate at 290 nm. The water-soluble protein content of the leaf extracts was measured by the method of Bradford (Bradford, 1976) using bovine serum albumin as a standard.
Statistical analysis
Student's t test (one-tailed) was applied to determine the statistical significance of the results as compared to the different treatments (0, 1, 5, 10 and 50 mM ZnSO4) and as compared to NI/I.
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Results |
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When applying increasing concentrations of ZnSO4 to the nutrient solution, the Zn content of the leaves of plants infected or not infected by A. lolii was determined, and no differences were found (data not shown). Taking this into account, Fig. 1
shows the Zn content of the leaves (of both infected and non-infected plants), from day 0 to day 24, with increasing concentrations of ZnSO4 in the culture medium. It can be seen that this parameter increases with time and with the increase in concentration of heavy metal. During the experiment, the tillers were numbered and the ratio (tillers on a given day/tillers on day 0) for the plants NI and I for the different concentrations of ZnSO4 is shown (Table 1). Not surprisingly, over time, this ratio increased for both infected and non-infected plants, reflecting the growth of plants. However, at 50 mM ZnSO4 the ratio rapidly reached constant values. In addition, when ZnSO4 is applied to plants, the higher the concentration, the weaker the ratio, compared to controls. Table 1 shows the differences obtained between infected and non-infected plants. It can be seen that for an equal concentration of ZnSO4 in the nutrient solution (except for 50 mM), the infected plants showed higher values than the non-infected plants. In other words, the number of leaves was greater in infected plants, assuming that all tillers contain the same number of leaves.
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) 1 mM; (
) 5 mM; (
) 10 mM; (
) 50 mM.
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At the end of the experiment, on day 24, all the upper parts (tillers and leaves) of the plants were harvested to determine the fresh weights. There was a net decrease in leaf fresh weight with increasing Zn concentration whether the plants were infected or not (Fig. 2A
), and no difference was observed between both types of plants. The same result was obtained with dry weights (data not shown). The water content of the upper parts was also determined (Fig. 2B) and no difference was observed between plants infected or not by the fungus. The higher the Zn concentration, the more the water content of the leaves is affected, compared to controls. Figure 3 shows a negative linear correlation (r2=0.990) between dry weights and the Zn content of the leaves.
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The calcium, potassium, magnesium, copper, and phosphorus content of the leaves is influenced by the addition of zinc (5, 10 and 50 mM) in the culture medium from the 7th day of the experiment: an accumulation of zinc in the leaves leads to a decrease in the other ion levels. Nevertheless, no difference was observed between infected and non-infected plants (data not shown).
The quantum yield of electron flow throughout photosystem II (F/) and the efficiency of photosynthetic energy conversion (as determined by the Fv/Fm ratio) were followed during the course of exposure to growing ZnSO4 concentrations (Fig. 4). Whether the plants were infected or not, a net decrease can be seen in these two parameters at 50 mM ZnSO4 from day 0 until the end of the experiment (a decrease of approximately 80%). At 1, 5 and 10 mM ZnSO4, no difference was found in the Fv/Fm ratio and F/ during a large part of the experiment. Effectively, only on the 17th day could a marked difference be observed between the treatments. Nevertheless, no difference was observed between the symbiotic and the non-symbiotic plants whether in the decrease of the values with time or with Zn concentration.
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Activities of enzymes (SOD and APX) detoxifying the cells from active oxygen species were measured during the whole experiment period, and the values obtained in leaves of non-infected plants were compared with those of plants infected by A. lolii. The total superoxide dismutase activity was measured in leaves of both types of plants previously submitted to different levels of ZnSO4. At first, there was no difference between the two types of plants (data not shown). Figure 5
represents the total activity of SOD measured in leaves of NI and I plants, during the whole experiment, and for the different concentrations used in this study. It can be seen that for Zn concentrations of 1, 5 and 10 mM, SOD activity is significantly higher compared with controls for the whole experiment (except for day 7 at 1 mM ZnSO4), and significantly lower compared with values obtained at 50 mM ZnSO4 (except for day 21 at 10 mM ZnSO4). In addition, at 50 mM, the activity doubled from day 0 to day 10, reaching a value which remained constant for the rest of the experimental period.
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On the 10th day of the treatment, a large increase in the ascorbate peroxidase activity (Fig. 6
) was noted (an increase of approximately 100%) when the plants were exposed to 50 mM ZnSO4 and this remained relatively constant thereafter until day 24. In leaves of plants infected by A. lolii (Fig. 6A), no significant difference could be statistically demonstrated in the enzyme activity, either at 1, 5 or 10 mM, compared with the controls, from the beginning to the end of the treatment (except for 5 and 10 mM ZnSO4 from days 21 to 24). In leaves of plants not infected (Fig. 6B), the activity of this enzyme slightly increased with time at 10 mM, whereas no significant variation in values occurred compared with controls at 1 and 5 mM. Figure 7 shows the significant difference encountered at 10 mM between both types of plants. It was observed that ascorbate peroxidase activity is significantly higher in leaves of plants not infected by the fungus, from day 10 to day 21.
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Discussion |
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The seedlings of ryegrass (L. perenne) used for this study were watered daily with a nutrient solution (Coïc and Lesaint, 1975
). After 7 d of application of an additional amount of ZnSO4, only the highest concentration of this heavy metal (50 mM) led to nearly immediate visual stress symptoms of the metabolic processes of the plants. At this very high concentration, only a few days after the plants' exposure to the heavy metal, growth stops (the number of tillers no longer increases), compared to the controls and to the other concentrations used in this study (1, 5 and 10 mM). This indicates a very strong capacity of this perennial plant to protect itself against toxic metal concentrations. Ryegrass has apparently a great capacity to absorb Zn without any disturbance in its metabolism, as a large amount of ZnSO4 is required to inhibit growth, in comparison with other plants (MacNicol and Beckett, 1985). In fact, there is only a small number of plant species capable not only of growing in soils containing high levels of heavy metals, but also of accumulating high metal concentrations in shoots. The species capable of this are designated hyperaccumulators (Brooks et al., 1977) and can tolerate up to 40 mg g-1 DW in their upper parts (Chaney, 1993). The normal concentration of Zn in plants growing on unpolluted soil varies from 0.02–0.4 mg g-1 dry weight (Bowen, 1979). However, most plants show potential phytotoxicity at leaf tissue concentrations above 0.2 mg g-1 dry matter (Davis and Beckett, 1978). Nevertheless, ryegrass cannot be considered as a hyperaccumulator plant because, when growing with 50 mM ZnSO4, the Zn content of the leaves at the end of the experiment (day 24), reached the value of 17.3 mg g-1 DW, accompanied by marked visual stress symptoms at this stage of growth.
Growth inhibition and reduction of biomass production are general responses of higher plants to heavy metal toxicity (Ouariti et al., 1997). Inhibition of both cell elongation and division by heavy metals could explain, in part, the decline in biomass production (Arduini et al., 1994). In addition, it has been shown that growth of the upper plant parts is more sensitive to heavy metals, in spite of their low metal content compared with roots, with the hypothesis that roots could play an important role in the retention of metals by preventing an excess of toxic accumulation in the shoots (Mazhoudi et al., 1997). In the same way, roots of higher plants were considered as a barrier against heavy metal translocation to the top parts (Wallace and Romney, 1977), reflecting a potential tolerance mechanism operating in the root cells.
If zinc, like other heavy metals, leads to toxicity in leaves, it is now well known that this component, at high levels, can act as an efficient generator of toxic oxygen species, such as 
and H2O2, by inhibiting photosynthetic electron transport (Kappus, 1985). Here, when plants were submitted to different levels of ZnSO4, a net decline in the capacities of maximal photochemical efficiency of photosystem II (Fv/Fm) and in the quantum yield of electron flow throughout PSII (F/) was observed. Similar results were found with other species (Yruela et al., 1996; Maksymiec and Baszynski, 1996; Krupa, 1993). As before, it was observed that a very strong concentration of heavy metal (50 mM) is required to cause immediate stress to the leaves. At other concentrations, a period of up to 17 d was necessary to visualize a constraint caused by the metal. This result again underlines the strong capacities of ryegrass to counteract such conditions of stress.
Toxic oxygen species, generated by the presence of heavy metal in leaves, were evident (according to Chaoui et al., 1997), by the increased lipid peroxidation in all organs of bean seedlings treated with metals. Weckx and Clijsters (Weckx and Clijsters, 1997) showed that as soon as Zn was assimilated by the primary leaf of Phaseolus vulgaris, a higher H2O2 level was observed (effect significant 172 h after application of the metal). Apparently, an increase in the capacity of distinct enzymes seems to be a rather general response to phytotoxic doses of several heavy metals (Van Assche et al., 1988). Two enzymes of the cellular antioxidative system involved in H2O2 metabolism, were studied: SOD, which catalyses the disproportionation of radicals into H2O2 and molecular oxygen, and APX, an enzyme that scavenges H2O2. Total SOD activity was measured in leaves of plants submitted to different levels of ZnSO4. It was observed that activity of this enzyme was enhanced with increasing concentrations of the heavy metal. Weckx and Clijsters found that the total activity of SOD was not affected by Zn stress (application of 612 µM Zn to roots of 7-d-old intact bean seedlings) (Weckx and Clijsters, 1997). These authors explain this result assuming, (according to Scandalios, 1993), that oxidative stress could cause increased turnover and resynthesis of SOD with no net change in its concentration. Chongpraditnum et al. found that a Cu2+-mediated increase in SOD activity may possibly be the result of either a direct effect of these ions on the gene for SOD or an indirect effect, mediated via an increase in levels of ;Chongpraditnum et al., 1992). Seven days after application of 50 mM ZnSO4 in the culture medium, the leaf APX activity increased by more than 100% of the initial activity. At other concentrations (1, 5 and 10 mM), the increase was less evident, mainly in leaves of infected plants. The analysis of APX activity, accompanied with other assays such as monodehydroascorbate reductase, dehydroascorbate reductase and glutathione reductase, could tend to support the hypothesis that the H2O2 scavenging ascorbate–glutathione cycle might be activated in leaves of Zn-poisoned plants, an idea supported by Chaoui et al. (Chaoui et al., 1997). In this study, Zn toxicity induces intracellular oxidizing conditions leading to the production of reactive oxygen species; this was deduced from the stimulation of APX and SOD capacities in leaves of the plants. It can be said that ryegrass has a great potential for tackling toxic oxygen species that are produced under zinc toxicity through a co-ordinated increase in the activities of enzymes involved in their detoxification.
It is now well known that endophytes have a profound impact on the ecology of natural and managed ecosystems, primarily by enhancing host resistance to biological pests. However, endophytes also make grasses more tolerant to abiotic stresses (Bacon, 1993). Even though grasses are inherently well adapted to drought conditions, endophytes appear to enhance drought tolerance further (White et al., 1992). Recently, Liu et al. (Liu et al., 1996) reported that the growth of symbiotic plants were more tolerant to high soil aluminium content than non-symbiotic plants, with significant increases in root length, root mass and total biomass. Therefore an aim of this study was to investigate the effect of the fungus on the plant faced with an abiotic stress, such as Zn toxicity in the leaves.
Although there is no difference in fresh and dry weights between symbiotic and non-symbiotic plants, whatever the ZnSO4 concentration used (1, 5 and 10 mM), the number of tillers is higher in the former. The increase in the number of tillers is considered to be an important agronomic parameter of productivity and persistence of grasslands (Cooper and Saeed, 1949). This result supports the idea that in leaves of infected plants, the presence of the endophyte increases the threshold toxicity of plants to zinc. This improvement in tiller production may be due to a strong synthesis of indole acetic acid (Goodin, 1972) and Bacon and de Battista (de Battista, 1990) showed that the endophyte A. coenophialum, cultivated in vitro, can produce this hormone. However, in this study, the concentration of 50 mM ZnSO4 in the culture medium is such that the fungus cannot confer any significantly detectable advantage to its host.
In these experimental conditions, the addition of zinc in the culture medium led to a decrease in the level of calcium, potassium, magnesium, copper, and phosphorus in the leaves. In addition to stress induced by zinc, deficiency in these ions may contribute to a dysfunction of several metabolic processes such as photosynthesis, nitrate reduction, acid radicals neutralization, etc. With tall fescue submitted to water stress, Wilkinson et al. demonstrated that infected plants showed a significant increase in the potassium, calcium and magnesium content of the leaves compared to non-symbiotic plants (Wilkinson et al., 1989). In this case, the water content of the leaves decreased with growing concentrations of zinc in the culture medium, however, no difference was observed in the ion content of the leaves of ryegrass infected or not by A. lolii.
During stress conditions induced by zinc treatment, time-courses of APX and SOD activities do not show any difference between plants infected by the fungus or not, except for APX activity at 10 mM ZnSO4. Leaves of infected plants show lower activity of this enzyme compared with non-symbiotic plants. The hypothesis can be advanced that the fungus modifies the metabolism of the plant by favouring H2O2 scavenging throughout the catalase process.
Parameters of fluorescence chlorophyll a do not allow a significant role of A. lolii to be highlighted in the photosynthetic processes. Some authors (Richardson et al., 1993) found similar results on tall fescue exposed to drought stress.
According to these investigations, it can be concluded that ryegrass is able to endure high levels of zinc before demonstrating marked visual stress symptoms. Zinc toxicity causes oxidative damage, as indicated by increases of SOD and APX activities in leaves. In these conditions, the presence of the endophyte A. lolii improves the defence capability of the plant.
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Acknowledgments |
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We are deeply indebted to Mr Raynal (INA-PG Grignon) for the generous gift of seeds of L. perenne, Mr Leyrolle for statistical analysis, the ‘Laboratoire Départemental d'Analyses et de Recherche’ of Aurillac for mineral determination in the leaves, and Mme Arnaud for English proof reading.
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Notes |
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1 To whom correspondence should be addressed. Fax: +33 4 71 45 57 59. E-mail:muriel.bonnet{at}u-clermont1.fr
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Abbreviations |
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APX, ascorbate peroxidase; DW, dry weight; DTT, dithiothreitol; EDTA, ethylenediaminetetraacetic acid; FW, fresh weight; Fv/Fm, variable fluorescence to maximal fluorescence ratio;
F/F'm, quantum yield of electron flow throughout photosystem II; NBT, nitro-blue tetrazolium; PSII, photosystem II; s.e., standard error; SOD, superoxide dismutase.. |
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