Seasonal profiles of leaf ascorbic acid content and redox state in ozone-sensitive wildflowers

Cutleaf coneflower (Rudbeckia laciniata L.), crown-beard (Verbesina occidentalis Walt.), and tall milkweed (Asclepias exaltata L.) are wildflower species native to Great Smoky Mountains National Park (U.S.A.). Natural populations of each species were analyzed for leaf ascorbic acid (AA) and dehydroascorbic acid (DHA) to assess the role of ascorbate in protecting the plants from ozone stress. Tall milkweed contained greater quantities of AA (7-10 micromol g(-1) fresh weight) than crown-beard (2-4 micromol g(-1) fresh weight) or cutleaf coneflower (0.5-2 micromol g(-1) fresh weight). DHA was elevated in crown-beard and cutleaf coneflower relative to tall milkweed suggesting a diminished capacity for converting DHA into AA. Tall milkweed accumulated AA in the leaf apoplast (30-100 nmol g(-1) fresh weight) with individuals expressing ozone foliar injury symptoms late in the season having less apoplast AA. In contrast, AA was not present in the leaf apoplast of either crown-beard or cutleaf coneflower. Unidentified antioxidant compounds were present in the leaf apoplast of all three species. Overall, distinct differences in antioxidant metabolism were found in the wildflower species that corresponded with differences in ozone sensitivity.     

Acquired changes in stomatal characteristics in response to ozone during plant growth and leaf development of bush beans (Phaseolus vulgaris L.) indicate phenotypic plasticity

Bush bean (Phaseolus vulgaris L.) lines 'S156' (O3-sensitive)/'R123' (O3-tolerant) and cultivars 'BBL 290' (O3-sensitive)/'BBL 274' (O3-tolerant) were used to study the effects of O3 on stomatal conductance (gs), density, and aperture size on leaf and pod surfaces with the objective of establishing links between the degree of plant sensitivity to O3 and plasticity of stomatal properties in response to O3. Studies in open-top chambers (OTCs) and in continuously stirred tank reactors (CSTRs) established a clear relationship between plant developmental stages, degrees of O3 sensitivity and gs: while 'S156' had higher gs rates than 'R123' earlier in development, similar differences between 'BBL 290' and 'BBL 274' were observed at later stages. Gs rates on the abaxial leaf surfaces of 'S156' and 'BBL 290', accompanied by low leaf temperatures, were significantly higher than their O3-tolerant counterparts. Exposure to O3 in CSTRs had greater and more consistent impacts on both stomatal densities and aperture sizes of O3-sensitive cultivars. Stomatal densities were highest on the abaxial leaf surfaces of 'S156' and 'BBL 290' at higher O3 concentrations (60 ppb), but the largest aperture sizes were recorded on the adaxial leaf surfaces at moderate O3 concentrations (30 ppb). Exposure to O3 eliminated aperture size differences on the adaxial leaf surfaces between sensitive and tolerant cultivars. Regardless of sensitivity to O3 and treatment regimes, the smallest aperture sizes and highest stomatal densities were found on the abaxial leaf surface. Our studies showed that O3 has the potential to affect stomatal plasticity and confirmed the presence of different control mechanisms for stomatal development on each leaf surface. This appeared to be more evident in O3-sensitive cultivars.     

The ability of apoplastic ascorbate to protect poplar leaves against ambient ozone concentrations: a quantitative approach

Shoots of a sensitive (Populus nigra 'Brandaris') and a more tolerant (Populus euramericana 'Robusta') poplar clones were exposed for 30 days to Filtered Air or ambient O3-concentrations in fumigation cabinets. At regular intervals were determined: gas exchange of the leaves, the internal air space (Vair) and apoplastic water volume (Vapo) and the reduced (ASA) and oxidized (DHA) ascorbate concentration in the apoplast and in the mesophyll cells. The apoplastic ASA-concentration was 0.2 mM at the start of the experiment for both cultivars, while the effective cell wall thickness, estimated from Vapo, varied from 0.3 to 0.6 micron. Model calculations revealed that only 30% of the O3 molecules entering the apoplast was intercepted at these values. The O3-treatment induced a decline in stomatal conductance, an increase in Vapo and in the apoplastic ASA-concentration. As a result the estimated O3-flux to the cell membrane strongly declined. However, these responses occurred after the O3-induced reduction in photosynthesis. Moreover, they did not prevent early senescence of the leaves at a prolonged exposure. Therefore, it is concluded that the increase in apoplastic ASA-concentration was rather a general stress reaction of the affected poplar leaf than a (specific) defence reaction induced by O3. Our results suggest that other factors than the scavenging efficiency of apoplastic ASA were responsible for the difference in O3 sensitivity between both poplar cultivars.     

Influence of ozone stress on growth processes, yields and grain quality characteristics among soybean cultivars

Field studies were conducted at USDA Beltsville Agricultural Research Center, Beltsville, Maryland, in 1984 and 1985 using open-top chambers to acquire information on the responses of 12 soybean (Glycine max L. Merr.) cultivars to O3 stress and to examine the interactions between maturity groups and O3 stress. Cultivars representing Groups III, IV, and V were exposed for approximately 3 months to charcoal-filtered air (CF) and nonfiltered air plus 40 nl litre(-1) O3 (NF + O3). Ozone was added 6 h d(-1), 5 d week(-1) for 13 weeks. The CF effectively reduced the accumulative oxidant exposure (AOX) to less than 1.0 microl litre(-1) h and the NF + O3 treatment approximately doubled the ambient AOX (16.7 microl litre(-1) h) to about 30 microl litre(-1) h. The AOX estimates the total O3 exposure above 30 nl litre(-1) during an entire growing season. Plant growth rates and relative growth rates were reduced by 17.0 and 14.4%, respectively, when averaged over cultivars. Based on growth rates, the Group III cultivars were the most affected by O3 stress. Averaged over cultivars, leaf expansion rates, leaf conductance, and transpiration rates were lower in the NF + O3 treatment compared to the CF control; however, wide variation was found with the stomatal results from field observations. Combined over years and cultivars, grain yield was reduced by an average of 12.5% by O3 stress with 3 of 12 cultivars showing significant reductions. Grain protein content was increased by 0.7% by O3 stress, but cultivar differences were equal to the differences caused by the O3 treatments. Grain oil content was unchanged by the O3 treatments. Group IV cultivars showed the greatest decrease in grain yield due to O3 stress. Multiple regression analyses were calculated using the difference between the CF and NF + O3 treatment as a measure of O3 stress. Significant positive relationships were found among net assimilation rates, plant growth rates, relative growth rates, and leaf expansion rates, which suggest that growth analysis characteristics would be useful in addition to yield in air pollution tolerance improvement studies with soybeans.     

Screening of bean cultivars for their response to ozone as evaluated by visible symptoms and leaf chlorophyll fluorescence

Fourteen Italian cultivars of Phaseolus vulgaris were exposed to a single pulse of ozone (O(3), 150 nl l(-1)) or to filtered air (<3 nl l(-1)) for 3.5 h. O(3) sensitivity was assessed by recording the extent of visible symptoms, effects on chlorophyll (Chl) content and changes in Chl a fluorescence parameters. This paper reports the results of an initial screening of 14 bean cultivars that was used to select a small number of cultivars for further work. Seven cultivars showed visible symptoms of injury in the range of 2-60 h after the end of the O(3) fumigation. O(3) significantly depressed total Chl content in most cultivars and a significant correlation was found between Chl content and visible symptoms. Most cultivars showed a significant change in the F(v)/F(m) ratio, even when there were no visual symptoms. There was no relationship between the extent of visual symptoms and quenching coefficients, indicating that these parameters were of no use in the determination of sensitivity to O(3) stress.     

Response of cellular antioxidants to ozone in wheat flag leaves at different stages of plant development

The effect of ozone (O3) on growth, yield and foliar antioxidants of spring wheat (Triticum aestivum L. cv. Turbo) was investigated in 1990 and 1991 in Braunschweig, Germany. Plants were grown full-season in pots in open-top chambers ventilated with charcoal-filtered (CF) air to which one or two levels of O3 were added. Mean 8 h day(-1) (10.00-18.00 h) O3 concentrations in the CF and CF + O3 treatments were 5.9, 61.2 and 92.5 nl litre(-1) in 1990, and 4.7 and 86.4 nl litre(-1) in 1991. Plants that received the high O3 level showed symptoms of premature senescence of the oldest leaves and yield reductions in both growing seasons. The contents of ascorbate and glutathione and the enzyme activities of ascorbate peroxidase and glutathione reductase were measured in symptomless flag leaves in weekly intervals before and after the beginning of anthesis. Leaf age had a significant effect on all antioxidants investigated. The O3 exposures of about 90 nl litre(-1) increased the activity of ascorbate peroxidase and the concentration of glutathione, but there were no pollutant effects on ascorbate content and glutathione reductase activity. Measurements of the antioxidant levels throughout one day showed no clear indications of diurnal changes in the antioxidative capacity in wheat flag leaves. The results are discussed in relation to the role of antioxidants in O3 detoxification.     

Interaction between ozone and winter stress

In some countries, ozone (O3) is primarily a summer pollutant, but in much of Europe, elevated concentrations occur outside the growing season so perennials and over-wintering annuals may be subjected to the combined stresses of pollution, plus chilling, freezing, and winter desiccation. It is recognised that some air pollutants modify the response of plants to environmental stress, but little is known of interactions involving O3. This paper is part of a programme concerned with the effects of O3 on resistance to chilling, freezing, and winter desiccation. Pea (Pisum sativum L.) was used as a convenient model to confirm that O3 affects freezing resistance. The experiment also served as a further evaluation of the use of induced chlorophyll fluorescence kinetics to detect latent O3 injury. Two cultivars, 'Feltham First' and 'Conquest', were fumigated for 7 days, 7 h day(-1). Diffusive resistance and induced fluorescence were recorded daily during the period, then the plants were hardened at 4 degrees C day/2 degrees C night before exposure to 0, -2, -4, -6 and -8 degrees C. Ozone (0.075 ppm; 150 microg O3 m(-3)) caused stomatal closure in both cultivars, but the response was more rapid in 'Conquest'. There were also rapid effects on fluorescence kinetics, and it was concluded that FR, the rate of rise of induced fluorescence, is a useful parameter for indicating latent injury and for distinguishing between cultivars of different sensitivity. Exposure to O3 increased freezing injury and led to greater electrolyte leakage. The freezing resistance of 'Feltham First' was more affected than that of 'Conquest', probably because of the slower stomatal response to the pollutant leading to greater flux of O3 to the internal tissues. It is concluded that interactions involving pollutants and winter stress have implications for crop loss assessment. Perennials and over-wintering annuals should be exposed to the full range of environmental stresses.     

Relationship between leaf antioxidants and ozone injury in Nicotiana tabacum ‘Bel-W3’ under environmental conditions in São Paulo,SE – Brazil

Previous studies have reported that the extent of leaf injury in Nicotiana tabacum “Bel-W3” exposed to environmental conditions in the city of São Paulo is influenced by weather conditions. This influence may occur by means of antioxidant responses. Thus, this study aimed to evaluate whether daily antioxidant responses to environmental variations interfere on the progression of leaf injury on plants of this cultivar during their exposure in a state park of São Paulo and to determine a linear combination of variables, among antioxidants and environmental factors, which mostly explain this visible response. Plants were exposed at the mentioned site for 14 days in four different experiments. During each experiment, three plants were daily sampled to determine the accumulated percentage of leaf area affected by necrosis and antioxidant responses (concentrations of total ascorbic acid (AA) and activity of superoxide dismutase (SOD) and peroxidases (POD)). Ozone concentrations and weather conditions were also daily measured. Pearson correlations and multivariate analyses assessed the relationship between biological and environmental variables. Leaf injury appeared between the 3rd and 6th days of exposure and increased over the exposure periods. The daily concentrations of AA tended to decrease with time of exposure in all experiments, but the activity of SOD and POD oscillated during plant exposure. Positive correlations were observed between AA or SOD and O₃ concentrations, as well as negative correlations between AA and air temperature. The increasing percentage of leaf necrosis across the whole period was explained by decreasing levels of AA 2 days before injury estimation and by higher O₃ concentrations 5 days before (R² = 0.36; p < 0.001). The use of N. tabacum Bel-W3 as a bioindicator can be restricted by leaf antioxidant responses to both atmospheric contamination and weather conditions.     

Dose-response studies with the antiozonant ethylenediurea (EDU), applied as a soil drench to two growth substrates, on greenhouse-grown varieties of Phaseolus vulgaris L

To study plant growth and yield effects of the antiozonant ethylenediurea (EDU), which is frequently used for ozone crop loss assessments, dose-response studies were carried out with potted bean plants under greenhouse conditions in winter and spring. Two cultivars of Phaseolus vulgaris L., differing in sensitivity to ozone (O(3)), were grown in unfiltered air on a sandy loam rich in organic matter and on a vermiculite-clay mixture. Four treatments of EDU at concentrations from 300 to 800 mg liter(-1) were given as a soil drench during plant development. Foliar symptoms of EDU phytoxicity were observed at all doses, and plant biomass, particularly pod dry weight, was considerably reduced to increasing doses of EDU. Primary and first trifoliate leaf weight in EDU-treated plants increased as did the number of buds, indicating an extension of vegetative growth and a delay of reproductive processes. 'BBL 290' beans, which are O(3)-sensitive, were injured by EDU more than the O(3)-tolerant 'BBL 274'. The phytotoxic effects of EDU were more pronounced in the synthetic growth substrate than in field soil. In a second experiment, EDU was applied in concentrations from 100 to 400 mg liter(-1) to 'BBL 290' plants, exposed to filtered air or simulated levels of O(3) pollution. In field soil, plant growth and biomass partitioning in filtered air was only slightly altered by EDU, although leaf injury due to EDU occurred. In the vermiculite-clay mix, the biomass of most plant organs, particularly that of roots, was linearly reduced with increasing EDU doses. O(3) did not cause any alteration in plant biomass in field soil-grown and EDU-treated plants. Ozone leaf injury, which affected 67% of primary leaf area in non-treated plants, was completely suppressed by EDU doses as low as 100 mg liter(-1). This indicates that low concentrations of EDU, which do not affect plant growth in field soil, provide sufficient protection from O(3) injury. The need for careful EDU dose-response studies prior to field assessments is emphasized.     

Ozone stress and antioxidant substances in Trifolium repens and Centaurea jacea leaves

Ozone-sensitive (NC-S clone) and resistant plants (NC-R clone) of Trifolium repens and Centaurea jacea were exposed to moderate ozone concentrations in ambient air. The aim of this study was the investigation of the relation between ozone-sensitivity and leaf concentrations of antioxidants (ascorbic acid, total phenolics and total antioxidant capacity). NC-R clone showed the highest concentrations of antioxidants with 50-70% more ascorbic acid than NC-S. NC-R had about 5 times more ascorbic acid in the young leaves and 9 times more in the old leaves than Centaurea. In a fumigation experiment with acute ozone stress (100 nl L(-1)) the antioxidant levels changed profoundly. The ozone-injured leaves of NC-S had 6-8 times more total phenolics than uninjured leaves. Generally older leaves had lower antioxidant concentrations and were more prone to ozone injury than younger leaves. Ascorbic acid concentrations were closer related to the appearance of visible ozone injury than the other antioxidative parameters.     

Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) seedlings

Two black cherry families differing in sensitivity to ozone (O(3)) were used to test the hypothesis that leaf morphology is related to foliar sensitivity to O(3). Two uninjured sections of leaf tissue were sampled from a single leaf collected from each of 12 open-grown O(3)-tolerant and 12 O(3)-sensitive seedlings. Standard histological techniques and light microscopy were used to examine 11 morphological characteristics. The O(3)-sensitive genotype had significantly greater stomatal density, thinner palisade mesophyll layer and thicker spongy mesophyll layer, lower ratio of palisade to spongy mesophyll, greater leaf weight and leaf area. In addition, total leaf thickness, guard cell length, and specific leaf mass were also slightly greater for the O(3)-sensitive genotype.     

Assessment of the ozone tolerance of two soybean cultivars (Glycine max cv. Sambaíba and Tracajá) cultivated in Amazonian areas

Brazilian soybean cultivars (Glycine max Sambaíba and Tracajá) routinely grown in Amazonian areas were exposed to filtered air (FA) and filtered air enriched with ozone (40 and 80 ppb, 6 h/day for 5 days) to assess their level of tolerance to this pollutant by measuring changes in key biochemical, physiological, and morphological indicators of injury and in enzymatic and non-enzymatic antioxidants. Sambaíba plants were more sensitive to ozone than Tracajá plants, as revealed by comparing indicator injury responses and antioxidant stimulations. Sambaíba exhibited higher visible leaf injury, higher stomatal conductance, and a severe decrease in the carbon assimilation rate. Higher ozone level (80 ppb) caused an increase in cell death in both cultivars. Levels of malondialdehyde and hydrogen peroxide also increased in Tracajá exposed under 80 ppb. Sambaíba plants exhibited decreases in ascorbate and glutathione levels and in enzymatic activities associated with these antioxidants. The higher tolerance of the Tracajá soybean appeared to be indicated by reduced physiological injuries and lower stomatal conductance, which might decrease the influx of ozone and enhance oxidation-reduction reactions involving catalase, ascorbate peroxidase, ascorbate, and glutathione, most likely stimulated by higher hydrogen peroxide.     

An assessment of the impact of ambient ozone on field-grown crops in New Jersey using the EDU method: part 1-white potato (Solanum tuberosum)

Six potato cultivars were grown to maturity in field plots in New Brunswick, New Jersey, according to standard commercial practices over a 5-year period. One-half of the plots were given a periodic soil drench of an antioxidant (EDU) which has the capacity to protect foliage against ozone toxicity. Based upon visible foliar injury and total tuber yield, the cultivars Norland and Norchip proved significantly more sensitive to ambient ozone pollution than Green Mountain, Irish Cobbler, Belrus or Superior. When foliar injury was less than 20%, no impact on tuber yield was detected. However, when 75% of the foliage exhibited O(3) toxicity symptoms, tuber yield was reduced 25% and 31%, respectively, in 'Norland' and 'Norchip'. A review of results from studies in the US and Canada utilizing different assessment methodologies provides evidence that ambient ozone causes significant tuber yield reduction in sensitive white potato genotypes when foliar injury exceeds 20 to 40%.     

Photosynthetic inhibition and superoxide dismutase activity in soybean cultivars exposed to short-term ozone fumigations

Net photosynthesis (Pn) and mean stomatal conductance (gs) of soybean (Glycine max (M.) L.) cvs 'Dare', 'Essex' and 'Williams 82' were inhibited by exposure to 200 nliters liter(-1) ozone (O(3)) for 4 h. Changes in gas exchange rates were not uniform over time, and a near steady state condition was attained after fumigation for 2 h. There was no recovery of Pn or gs for up to 2 h following termination of O(3) application. The cv 'Dare' was considered most sensitive to O(3) since, in this cultivar, gs was least responsive during the initial 2.5 h of fumigation and the estimated internal O(3) flux was about 10% greater than in the other cultivars. Polyacrylamide gel electrophoresis of soybean leaf extracts, followed by activity staining for superoxide dismutase (SOD), revealed the presence of numerous major and minor bands. Cynide sensitivity of several isoforms indicated the presence of both Cu-Zn and Mn SODs. In cv 'Essex', each metalloform accounted for 50% of the total SOD activity. No qualitative differences in SOD banding patterns were evident among the three soybean cultivars before or after O(3) treatment. Ozone fumigation for 4 h did not significantly alter SOD activity in any cultivar. The contribution of gs, as a flux limitation, and SOD activity are discussed as tolerance mechanisms to O(3) in soybean.     

Differences in ability of NO2 absorption in various broad-leaved tree species

Absorption of nitrogen dioxide (NO(2)) by various broad-leaved tree species was determined by the (15)N dilution method. The tree seedlings were continuously exposed to 0.3 ppm (microl litre(-1)) NO(2) or the mixture of 0.3 ppm NO(2) and 0.1 ppm O(3) for 30 days. The total amount of NO(2)-nitrogen absorbed by a seedling during the 30-day exposure period primarily depended on the size of the seedling. Among the tested tree species, three cultivars of Populus showed the highest rate of NO(2) absorption per unit leaf area, reaching as much as 0.3 mg N per dm(2) per day. The absorption rates for Populus cultivars were more than four times greater than those for Viburnum or Cinnamomum which had the lowest rate. A highly significant correlation was recognised between the rate of NO(2) absorption and the stomatal conductance among the species. Three cultivars of Populus which had the highest rates of NO(2) absorption were most susceptible to the mixture of NO(2) and O(3). On the contrary, Cinnamomum, Viburnum and Quercus, which showed the lowest rate of NO(2) absorption, were very tolerant to the mixed gas. These results indicate that the species difference in susceptibility to the mixture of NO(2) and O(3) was mainly determined by the difference in rate of absorption of these gases. Exposure to NO(2) alone had no detrimental effect on the tested tree species.     

Apoplastic ascorbate contributes to the differential ozone sensitivity in two varieties of winter wheat under fully open-air field conditions

We studied leaf apoplastic ascorbates in relation to ozone (O₃) sensitivity in two winter wheat (Triticum aestivum L.) varieties: Yangfumai 2 (Y2) and Yangmai 16 (Y16). The plants were exposed to elevated O₃ concentration 27% higher than the ambient O₃ concentration in a fully open-air field from tillering stage until final maturity. The less sensitive variety Y16 had higher concentration of reduced ascorbate in the apoplast and leaf tissue by 33.5% and 12.0%, respectively, than those in the more sensitive variety Y2, whereas no varietal difference was detected in the decline of reduced ascorbate concentration in response to elevated O₃. No effects of O₃ or variety were detected in either oxidized ascorbate or the redox state of ascorbate in the apoplast and leaf tissue. The lower ascorbate concentrations in both apoplast and leaf tissue should have contributed to the higher O₃ sensitivity in variety Y2.     

How the redox state of tobacco 'Bel-W3' is modified in response to ozone and other environmental factors in a sub-tropical area?

This study intended to determine whether the redox state in plants of Nicotiana tabacum ‘Bel-W3’ fluctuates in response to the environmental factors in a sub-tropical area contaminated by ozone (São Paulo, SE - Brazil) and which environmental factors are related to this fluctuation, discussing their biomonitoring efficiency. We comparatively evaluated the indicators of redox state (ascorbic acid, glutathione, superoxide dismutase, ascorbate peroxidase, and glutathione reductase) and leaf injury in 17 field experiments performed in 2008. The redox state was explained by the combined effects of chronic levels of O₃ and meteorological variables 4-6 days prior to the plant sampling. Moderate leaf injury was observed in most cases. The redox state of tobacco decreases few days after their placement in the sub-tropical environment, causing them to become susceptible to oxidative stress imposed by chronic doses of O₃. Its bioindicator efficiency would not be diminished in such levels of atmospheric contamination.     

Visible and microscopic injury in leaves of five deciduous tree species related to current critical ozone levels

Because the current critical level of ozone (O(3)) for forest trees is based only on one species, the responses of five deciduous tree species were differentiated in a climate chamber experiment. The number of symptomatic leaves per tree was significantly increased, and stomatal conductance was decreased under 50% ambient+30 nl l(-1) O(3) as compared to 'normal' senescence at 50% ambient [O(3)]. Species with a high stomatal conductance did not show earlier or more leaf injury symptoms. The additional 30 nl l(-1) O(3) induced specific pectinaceous cell wall protrusions, phenolic cell wall incrustations, tonoplast vesicles, and inhomogeneous, condensed/precipitated phenolic material in the vacuoles. Due to added O(3), cell senescence was accelerated with increased electron-density of the cytoplasm, and initial chloroplast degeneration. The slow degeneration process started in mesophyll cells, and expanded into epidermal and finally guard cells. Because of the large variance in biomass between individuals and species, the current critical level is supported by the assessment of visible leaf symptoms rather than growth reduction.     

Effects of ozone on growth, yield and leaf gas exchange rates of two Bangladeshi cultivars of wheat (Triticum aestivum L.)

To clarify the effects of O₃ on crop plants cultivated in Bangladesh, two Bangladeshi wheat cultivars (Sufi and Bijoy) were grown in plastic boxes filled with Andisol and exposed daily to charcoal-filtered air or O₃ at 60 and 100 nl l⁻¹ (10:00-17:00) from 13 March to 4 June 2008. The whole-plant dry mass and grain yield per plant of the two cultivars at the final harvest were significantly reduced by the exposure to O₃. Although there was no significant effect of O₃ on stomatal diffusive conductance to H₂O of flag leaf, net photosynthetic rate of the leaf was significantly reduced by the exposure to O_3. The sensitivity of growth, yield, yield components and leaf gas exchange rates to O₃ was not significantly different between the two cultivars. The results obtained in the present study suggest that ambient levels of O₃ may detrimentally affect wheat production in Bangladesh.