Journal of Experimental Botany, Vol. 51, No. 342, pp. 107-113,
January 2000
© 2000 Oxford University Press
Low temperature-induced changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves
1 Biochemistry and Physiology Department, IACR-Rothamsted, Harpenden, Herts AL5 2JQ, UK
2 Department of Applied Genetics, John Innes Centre, Colney, Norwich NR4 7UH, UK
Received 24 April 1999; Accepted 24 June 1999
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Abstract |
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The distribution of antioxidants between bundle sheath and mesophyll cells of maize leaves was analysed in plants grown at 20 °C, 18 °C and 15 °C. The purity of the isolated bundle sheath and mesophyll fractions was determined using compartment-specific marker enzymes. In plants grown at 15 °C, ascorbate peroxidase, CuZn-superoxide dismutase (CuZn-SOD) and monodehydroascorbate reductase activities were increased in the bundle sheath cells, and glutathione reductase, dehydroascorbate reductase and monodehydroascorbate reductase activities were enhanced in the mesophyll cells. SOD was absent from the mesophyll of plants grown at 20 °C but an Fe-SOD activity was found in the mesophyll of plants grown at 15 °C. Foliar Mn-SOD activities were decreased at 15 °C compared to 20 °C. Catalase was undetectable in the mesophyll extracts of plants grown at 15 °C. Ascorbate and glutathione contents were considerably higher in the mesophyll than the bundle sheath fractions of plants grown at 20 °C. The ratios of reduced to oxidized forms of these antioxidants were significantly decreased in the bundle sheath, but increased in the mesophyll of leaves grown at 15 °C. Foliar H2O2 accumulated at 15 °C compared to 20 °C. Most of the foliar H2O2 was localized in the mesophyll tissues at all growth temperatures. The differential distribution of antioxidants between leaf bundle sheath and mesophyll tissues, observed at 20 °C, is even more pronounced when plants are grown at 15 °C and may contribute to the extreme sensitivity of maize to low temperatures.
Key words: antioxidants. maize, bundle sheath, mesophyll, temperature.
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Introduction |
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Sub-optimal growth temperatures provoke oxidative stress in plants. The amount of H2O2 found in leaves increases as the growth temperature is decreased (Hodgson and Raison, 1991
; McKersie, 1991; Prasad et al., 1994; Wise and Naylor, 1987). The fluidity of plant membranes and their relative unsaturated fatty acid content are important in determining chilling sensitivity and membrane susceptibility to lipid peroxidation (De Santis et al., 1999). Equally important is the capacity for antioxidant defence available to protect membranes and other components from oxidative damage.
Many studies have linked chilling tolerance to antioxidant capacity in maize. Exposure to low temperatures causes an increase in CAT, GR and guaiacol peroxidase activities (Prasad, 1996, 1997). Similarly, decreased CAT, APX and MDHAR activities were found to be associated with chilling sensitivity during the early stages of development of four inbred lines of Zea mays (Hodges et al., 1997a, b). Higher GR activities and more ascorbate were found in leaves of the relatively chilling-tolerant Zea diploperennis than in the relatively chilling-sensitive Z. mays (Jahnke et al., 1991). Chilling-induced enhancement of the GSH pool and constitutively higher GR activities were found to contribute to chilling tolerance in Z. mays (Kocsy et al., 1996). High APX, MDHAR, DHAR, GR, and SOD activities and enhancement of the ASC and 
-tocopherol pools were observed in field-grown maize during periods when the plants were exposed to chilling (Fryer et al., 1998). The relationships between CO2 assimilation, photosynthetic electron transport and antioxidant enzymes observed in field-grown maize led to the suggestion that pseudocyclic electron flow was increased in plants grown at sub-optimal temperatures (Fryer et al., 1998). Whether this is the case or not, the antioxidant defences appear to provide crucial protection against oxidative damage in plants grown at sub-optimal temperatures. To be effective, however, antioxidants must be located close to the sites of oxidant production and close to sites at high risk of oxidative damage. Overexpression of SOD in transformed maize led to increased protection from oxidative stress (Van Breusegem et al., 1999), even though the leaves of transformants contained enhanced SOD activity only in the BS cells where SOD is localized in the untransformed leaves (A Kingston-Smith and CH Foyer, unpublished results).
Maize is a C4 plant of the NADP-malic enzyme class. C4 plants are characterized by a distinctive anatomy and possession of a CO2 pumping system that aids the C3 cycle in photosynthesis. CO2 is initially incorporated into C4 acids in the mesophyll cells. These are transported to the bundle sheath (BS) tissues where CO2 is liberated in the vicinity of the C3 cycle (Hatch and Osmond, 1976; Furbank and Foyer, 1988; Furbank and Taylor, 1995). It has previously been reported that antioxidants are differentially distributed between the BS and the mesophyll (M) cells in maize leaves (Doulis et al., 1997). Glutathione reductase (GR) and dehydroascorbate reductase (DHAR) activitites were found to be almost exclusively localized in the M cells whereas ascorbate peroxidase (APX) and superoxide dismutase (SOD) were largely absent from the M fraction. Catalase (CAT) and monodehydroascorbate reductase (MDHAR) were equally distributed between the two cell types (Doulis et al., 1997). The differential partitioning of antioxidants between BS and M cells was suggested to be related to the availability of reducing power, since the BS cells possess relatively low PSII and NADP-ferredoxin oxidoreductase activities (Doulis
et al., 1997). It was suggested that this low capacity for recycling reduced ascorbate and glutathione to the bundle cells leads to preferential oxidation of proteins in these tissues (Kingston-Smith and Foyer, 2000) and to the extreme sensitivity of photosynthesis in maize to low temperatures (Doulis et al., 1997; Kingston-Smith et al., 1999). In addition, the enzymes and metabolites of assimilatory sulphate reduction and GSH synthesis have been shown to be differentially partitioned between the BS and M cells of maize leaves; ATP sulphurylase and adenosine 5'-phosphosulphate sulphotransferase were localized in the BS cells whereas GSH synthetase, cyst(e)ine, 
-glutamylcysteine, and GSH were found mainly in the M cells (Burgener et al., 1998). The present study was undertaken to determine the effect of growth temperature on the intercellular localization of H2O2, ascorbate, glutathione, and antioxidant enzyme activities in maize leaves.
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Materials and methods |
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Plant material and growth conditions
Maize (Zea mays L. var. H99) plants were grown for 4–5 weeks in Fitotron growth chambers (SGC 660/C/PPL, Sanyo, Loughborough, UK) at 20 °C, 18 °C and 15 °C, with a 16 h photoperiod and a PPFD of 300 µmol m-2 s-1. This irradiance allowed growth without photoinhibition or photo-oxidation (Kingston-Smith et al., 1999
) and this is important for effective comparisons of antioxidant activities.
Whole leaf, BS and M extraction
Whole leaf, BS and M fractions were compared in plants grown at 20 °C, 18 °C and 15 °C. Whole leaf extracts were prepared by removing the midrib and freezing the lamina segments in liquid N2. The leaf segments were ground with an extraction buffer consisting of 100 mM Bicine buffer (pH 7.8), 1 mM EDTA, 5 mM MgCl2, 0.1% Triton X-100, 1 mM bensamidine, 1 mM PMSF, 10 mM leupeptin, and 5 mM DTT. The M extrusion technique (Leegood, 1985) was used for rapid extraction of the M sap as described previously (Doulis et al., 1997). M sap was obtained by isolation into 100 µl of ice-cold extraction buffer; in this case each leaf segment was rolled once. The M sap, collected under vacuum, was centrifuged at full speed for 5 min in a Microfuge E (Beckman) and the supernatant was used immediately for enzyme assays. BS extracts were prepared by rolling all of the M sap from the maize leaf segments. The BS strands remaining following this procedure were frozen in liquid N2 and contents extracted as described for whole leaves. The purity of each fraction was determined by measuring the activities of the BS and M marker enzymes, Rubisco and PEP carboxylase, respectively. In all of the following experiments the contamination of M extracts by Rubisco was no more than 10% while the contamination of BS strands by PEP carboxylase was no more than 16%.
Measurement of enzyme activities
Maximal Rubisco activity was determined according to Parry et al. (Parry et al., 1988). PEP carboxylase activity was measured according to the method of Wong and Davies (Wong and Davies, 1973).
GR (EC 1.6.4.2) was determined spectrophotometrically at 340 nm in a reaction mixture containing 50 mM Tris–HCl buffer (pH 7.6), 1 mM GSSG and 10 mM NADPH, as described earlier (Foyer and Halliwell, 1976). APX (EC 1.11.1.11) was determined in separate extracts prepared in extraction buffer containing 2 mM sodium ascorbate (according to the method of Hossain and Asada, 1984). SOD (EC 1.15.1.1) was measured according to McCord and Fridovich (McCord and Fridovich, 1969) in the absence or presence of 5 mM KCN or 2 mM H2O2. MDHAR (EC 1.6.5.4) activity was assayed according to Arrigoni et al. (Arrigoni et al., 1981). DHAR (EC 1.8.5.1) was determined as described by Dalton et al. (Dalton et al., 1993). Catalase (EC 1.11.1.6) was measured according to Aebi (Aebi, 1984).
Chlorophyll and protein were determined in whole leaf, BS and M extracts according to the methods of Arnon (Arnon, 1949) and Bradford (Bradford, 1976), respectively.
Ascorbate, glutathione and H2O2 analyses
Ascorbate was determined by HPLC with a Dionex 500 chromatography system (Castillo and Greppin, 1988). Glutathione was determined as extractable low-molecular thiol weight by the method of Griffith (Griffith, 1980). H2O2 was determined as described by Guibault et al. (Guibault et al., 1967).
Statistical analyses
Significant differences between the means were calculated according to Student’s t-test.
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Results |
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In maize leaves about 40% of the total chlorophyll is located in the mesophyll thylakoids (Woo et al., 1971
). This distribution was similar at 20 °C, 18 °C and 15 °C. In all following analyses data are therefore expressed on a chlorophyll basis since the precise distribution of chlorophyll between BS and M cells is known. The activity of Rubisco in the M fractions was used as an estimate of the contamination by BS components while the activity of PEP carboxylase in the BS fractions was used to estimate contamination by components arising from the M tissues (Leegood, 1985; Doulis et al., 1997). In all cases cross-contamination of cell types was less than 16%. The following data have not been corrected for contamination because it is useful to present the raw data on antioxidant activities in both M and BS fractions for comparison.
Little or, in some cases, no APX was found in the M fractions isolated from maize leaves of plants grown at 20 °C, 18 °C or 15 °C (Fig. 1). The low APX activity found in the M fraction was equivalent to the level of contamination by BS components
(Fig. 1). APX activity was increased in the leaves of plants grown at 15 °C compared to those grown at 20 °C. Seven times more APX activity was found in the BS tissues of leaves grown at 15 °C compared to those grown at 20 °C.
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DHAR was increased in leaves of plants grown at 15 °C compared to 20 °C. DHAR activity was localized only in the M fractions at all growth temperatures, activity found in the BS being equivalent to the level of contamination (Fig. 1). Foliar MDHAR activity was decreased in the leaves of plants grown at 15 °C compared to those grown at 20 °C. At 15 °C MDHAR was predominantly found in the BS extracts (Fig. 1). GR activity was exclusively found in the M cells at all three growth temperatures (Fig. 1). GR activity increased in the M fractions from leaves at 15 °C compared to those grown at 20 °C.
SOD activity was increased in plants grown at 15 °C compared to 20 °C (Fig. 2). Most of the SOD activity in the leaves was found in the BS, very little, SOD activity being detectable in the M
(Fig. 2). The activity of CuZn-SOD was estimated using the inhibitor KCN, while MnSOD was estimated by its resistance to KCN and H2O2. Fe-SOD was detected by its sensitivity to H2O2 and its resistance to KCN. CuZn-SOD and Mn-SOD were below the level of detection in M extracts, but were high in BS fractions of plants grown at 20 °C. CuZn-SOD and Fe-SOD activities were increased in the leaves of plants grown at 15 °C compared to 20 °C, whereas Mn-SOD activity was highest at 20 °C (Fig. 2). Fe-SOD was detectable in M extracts of plants grown at 15 °C but CuZn-SOD and Mn-SOD activities remained below the limits of detection (Fig. 2). Foliar catalase activity decreased in leaves of plants grown at 15 °C compared to those grown at 20 °C (Fig. 3). Catalase activity was found in both M and BS extracts at 20 °C but was undetectable in M extracts from plants grown at 18 °C and 15 °C.
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H2O2 was detected in both the M and BS fractions of maize leaves at all growth temperatures (Fig. 3). The foliar H2O2 content increased in leaves of plants grown at 15 °C compared to 20 °C. The amount of H2O2 present in the BS was lower than that of the M fractions at all growth temperatures, but it was increased in both compartments when plants were grown at 15 °C.
GSH increased in leaves of plants grown at 15 °C compared to 20 °C (Fig. 4). GSH and GSSG were found in both M and BS fractions. At all temperatures more GSH was detected in the M fraction than in the BS. The ratio of GSH to GSSG was similar in the M and BS extracts of plants grown at 20 °C but it was much lower in the BS fractions than in the M fractions isolated from leaves grown at 15 °C (Fig. 4).
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The amount of ascorbate was decreased in leaves grown at 15 °C compared to 20 °C whereas the amount of dehydroascorbate was greatly increased in the latter compared to the former (Fig. 5
). The observed increase in DHA at 15 °C was almost entirely due to an increase in DHA in the BS tissues which had a very low ascorbate content at 15 °C and 18 °C. In marked contrast, the ratio of ascorbate to DHA was high in the M extracts from leaves of plants at all growth temperatures (Fig. 5).
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Discussion |
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Tolerance to sub-optimal temperatures is a complex and multi-faceted trait requiring adaptation of many cellular processes. In maize, mitochondrial function is impaired in chilled seedlings (De Santis et al., 1999
) while chilling-induced photoinhibition of photosynthesis is a major factor limiting yield (Prioul, 1996; Fryer et al., 1998). In both cases chilling-induced oxidative stress has been implicated in loss of function. This suggests that antioxidant defence is central to survival of sub-optimal temperatures (Prasad, 1996, 1997; Hodges et al., 1997a, b). In support of this view, antioxidant enzyme activities have been used to screen maize populations for chilling resistance (Hodges et al., 1997b).
The M and BS cells of maize leaves clearly have very different capacities of antioxidant defence at optimal temperatures (Doulis et al., 1997; Burgener et al., 1998) and this difference is even more pronounced at sub-optimal growth temperatures. Foliar GR and DHAR activities were significantly increased at 15 °C but were exclusively located in the M extracts at all growth temperatures. Fe-SOD mRNA, but not Mn-SOD mRNA or CuZn-SOD mRNA, was found in M (Van Breusegem, 1997). This enzyme, which is exclusively localized in the chloroplasts and is important in protecting the thylakoid membranes from oxidative stress (Arisi et al., 1998), was significantly increased at 15 °C. Fe-SOD activity was not detected in the BS under these circumstances. In contrast, Mn-SOD which is mainly localized in the mitochondrial matrix (Jackson et al., 1978) and in peroxisomes (del Rio et al., 1998) was detectable only in the BS tissues. Mn-SOD activity was decreased at 15 °C and 18 °C compared to 20 °C. This may be important in contributing to the sensitivity of mitochondria to low temperatures in maize (De Santis et al., 1999).
Several chilling-responsive nuclear genes have been isolated; one of these is catalase (Prasad et al., 1994; Anderson et al., 1994, 1995; Prasad, 1997). In maize leaves catalase activity is uniformly distributed between M and BS (Doulis et al., 1997). Foliar catalase was decreased in plants grown at 15 °C and 18 °C relative to 20 °C with activity being preferentially lost from the M. Since the M is also largely devoid of APX activity, these cells must have a limited capacity for H2O2 detoxification, particularly at 15 °C. H2O2 is probably removed by ascorbate and GSH in a non-enzymatic reduction. Foliar H2O2 contents increased in plants grown at 15 °C compared to 20 °C. Chilling-induced enhancement of H2O2 has been observed previously in maize leaves (Okuda et al., 1991; Kingston-Smith et al., 1999). The increase in H2O2 may be due to the loss of CAT activity. CAT activity was below the level of detection in the M fractions at 18 °C and 15 °C.
The M is able to maintain large pools of reduced ascorbate and glutathione despite a large increase in H2O2 content. This may be explained by the presence of GR and DHAR in the M and the capacity for NADPH production in these tissues. The BS has much lower ascorbate and GSH contents than the M cells, particularly at 15 °C, presumably because the BS is largely devoid of GR and DHAR. At 15 °C transport between the cell types may be restricted. Although ASC increased significantly in the BS fractions at 15 °C, the ratio of reduced to oxidized ascorbate strongly decreased. The increase in DHA in the BS at low temperatures is consistent with decreased recycling of DHA. If plasmodesmatal function is inhibited at 15 °C such that transport between M and BS is decreased, then transfer of DHA and ASC between the BS and M cells will be impaired.
APX activity is much higher in plants grown at 15 °C than 20 °C, suggesting a requirement for greater rates of H2O2 detoxification at the lower growth temperature. The observed decrease in the ratio of ascorbate to DHA in the BS indicates the presence of increased oxidative stress. In contrast, the M compartment which has high DHAR and GR activities maintains high ascorbate to DHA ratios and high GSH to GSSG ratios at 15 °C, indicating low rates of oxidative stress. The BS cells would appear to have less ability to withstand oxidative stress when maize plants are grown below 20 °C. Ascorbate regeneration from DHA and GSH regeneration from GSSG require cycling of the oxidized forms to the M cells where GR and DHAR are localized. Reduced ascorbate and reduced glutathione must then be transported back to the BS cells to provide antioxidant protection. Any situation which limits transport between the two cell types will tend to leave the BS tissues open to oxidative damage.
The differential distribution of antioxidants and antioxidant enzymes in BS and M cells at 15 °C may be crucial to the susceptibility of each cell type to oxidative damage. BS cells have the capacity to detoxify superoxide and H2O2, but the regeneration of ascorbate from DHA and GSH from GSSG is restricted. Ascorbate regeneration in the M can only occur via MDHAR activity or by non-enzymic reduction by reduced ferredoxin. In the M non-enzymatic reduction of superoxide to H2O2 must be predominant, but the appearance of Fe-SOD activity in the chloroplasts of leaves grown at 15 °C indicates the facultative induction of this enzyme under situations of enhanced superoxide production. Moreover, M cells do not appear to suffer from oxidative damage arising from H2O2 accumulation at 15 °C, whereas a marked increase in the number of carbonyl groups on BS proteins (indicative of increased oxidative damage) was observed at 15 °C compared to 20 °C (Kingston-Smith and Foyer, 2000). There is a strong oxidation of BS proteins from leaves of maize plants grown at low temperatures and treated with methyl viologen (Kingston-Smith and Foyer, 2000). Even if the oxygen partial pressure is lower in the BS than in the M cells due to Kranz anatomy, BS cells suffer from oxidative damage arising from H2O2 accumulation at 15 thinsp;°C. Detoxification of H2O2 through APX activity is necessary since CAT activity is decreased at 15 °C. The non-enzymatic reduction of H2O2 is restricted in the BS by the absence of reduced forms of ascorbate and GSH. The bundle sheath could be a weak point in maize leaves and this may partially determine the sensitivity of this plant to low temperatures.
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Acknowledgments |
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We thank Dr Ana Jimenez for discussion on ascorbate and H2O2 analyses. This work was funded by the European Commission (AIR1-CT92-0205, Engineering Stress Tolerance in Maize) and by an EEC Research Training Fellowship (FAIR CT-96-5055) to GP.
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Notes |
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3 To whom correspondence should be addressed. Fax: +44 1582 763010. E-mail: gabriela.pastori@bbsrc.ac.uk
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Abbreviations |
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APX, ascorbate peroxidase; ASC, ascorbate; BS, bundle sheath; CAT, catalase; CuZn-SOD, CuZn-containing superoxide dismutase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; DTT, dithiothreitol; Fe-SOD, Fe-containing superoxide dismutase; GR, glutathione reductase; M, mesophyll; MDHAR, monodehydroascorbate reductase; Mn-SOD, Mn-containing superoxide dismutase; PPFD, photosynthetic photon flux density; PSII, photosystem II; SOD, superoxide dismutase.
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