Original paper Environ. Control in Biol. 26(3), 83-89, Effect of Ozone on Stomatal Conductance in Sunflower Leaves:
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1 Original paper Environ. Control in Biol. 26(3), 83-89, 1988 Effect of Ozone on Stomatal Conductance in Sunflower Leaves: Yasumi FUJINUMA, Akio FURUKAWA* and Ichiro AIGA** Department of Engineering, National Institute for Environmental Studies, Tsukuba 305, Japan *Department of Environmental Biology, National Institute for Environmental Studies, Tsukuba 305, Japan **Faculty of Agriculture, University of Osaka Prefecture, Sakai 591, Japan (Received October 6, 1987) The effects of 03 on visible injury and stomatal conductance for water vapor transfer were determined during the leaf development of sunflower plant (Helianthus annuus L. cv. Russian Mammoth). The stomatal frequency and conductance were also measured during the leaf development. The foliar necrosis induced by the exposure to O3 was influenced by the leaf age. With increasing leaf age, the foliar necrosis increased from young to mature leaves, then decreased in senescent leaves. The effect on stomatal conductance was also influenced. The inhibition of stomatal conductance on the pretreatment value basis decreased from young to senescent leaves. The degree of foliar necrosis had no linear relationship to the calculated uptake rate of 03 suggesting that the agedependent foliar sensitivity to 03 could not be determined by the amount of O3 incorporated into leaves but by the detoxicating capacity of absorbed O3 in the leaf. INTRODUCTION Interest in the mechanism of O3 injury to plants has increased in recent years with the recognition that we are suffered from photochemical oxidants. Concerning this situation, the strict understanding of the response of stomata to air pollutants is very important, since the major pathway of gas flux, including O3, into leaf tissue occurs through stomata.1) Furthermore, plants play an important role in cleaning air by absorbing air pollutants from the atmosphere through stomata.2) Therefore, several investigators have paid their attention to the stomata for the injury with air pollutants. However, the effect of air pollutants on stomatal movement is complicated and reported results are often contradictory. Several authors reported that SO2 stimulated stomatal opening,3-5) while others reported the stomatal closure.6,7) Concerning this discrepancy, Mansfield and Majernik8) proposed that SO2 induced stomata open or close depending on the humidity conditions. Ozone has also been shown to affect the stomatal aperture. Evans and Ting9) found at 0.65 or 0.80 ppm that O3 caused a decrease in stomatal diffusive resistance, in other words the increase in stomatal opening, but Hill and Littlefield10) found that O3 decreased stomatal opening in oats. Furukawa et al.11) had a similar response with decreased opening in poplar. Concerning this discrepancy, plant age may be an influencing factor since the f oliar sensitivity to O3 depends on leaf development.12) Ting and Vol. 26, No. 3 (1988) (1) 83
2 Dugger13) reported that the age-dependent sensitivity of cotton leaves to O3 was not correlated with the diffusive resistance of stomata. A further evidence was reported by Harris and Heath14) that the resistant and sensitive cultivars of Zea mays had similar diffusive resistances of stomata. However, there are only a few studies concerning the effects of O3 on stomatal aperture of different aged leaves. The present work is therefore concerned with the age-dependent differences in responses of diffusive conductance for water vapor transfer through stomata, the antagonistic of the diffusive resistance, to O3 and the role of stomatal opening in sensitivity to O3. MATERIALS AND METHODS Plant materials Seedlings of sunflower (Helianthus annuus L. Russian Mammoth), were grown at 25 Ž and a relative humidity of 70% in a phytotron greenhouse. Plants were cultivated for 4 weeks in plastic pots (11 cm diameter, 15 cm deep) filled with a mixture of vermiculite, peatmoss, perlite, and gravel (2 : 2 : 1: 1, v/v/v/v). Each pot contained 5 g of Magamp-K (N: P2O5: K2O = 6 : 40: 5) and 15 g of magnesia lime. Potted plants were watered daily and with Hyponex (N: P2O5: K2O = 6.5: 5 : 19) solution (1 g/l) once a week. Fumigation system Plants were exposed to O3 in a controlled environment room (1.7 ~2.3 ~2.0 m high). The field air was passed in succession through the activated charcoal and MnO2 catalyst bearing filters to remove ambient air pollutants and led into the controlled environment room. This filtration system could remove 03 and sulfur dioxide almost perfectly, but a trace amount of nitrogen dioxide (below 5 ppb) was remained in the room. Ozone was generated by a silent electrical discharger (Nihon Ozone, MOT-2A) in dry oxygen and was injected through a solenoid valve into the air stream. Ozone concentration was regulated by a thermal mass-flow controller equipped with a controlling system of chemiluminescent 03 analyzer (Kimoto, Model 806). Recordings of 03 concentrations inside the room showed that on starting a fumigation, the concentration reached 90% of the fixed level within 5 min. Ozone concentrations could be regulated within ± 1 % of the desired levels. Illumination system was consisted of twenty four 400 W stannous halide lamps (Toshiba, Yoko Lamp D400-NN). The light was filtered through heat absorbing glass filter, which removed radiation above 800 nm. The quantum flux density at the top of plants was 500 ƒêmol m-2 Es-1 measured with a quantum flux sensor (LI-COR, LI-185A). Prior to the fumigation, the plant was illuminated for more than one hour to open stomata. Estimation of stomatal conductance For the experiments on the effects of O3, stomatal conductance was estimated using the data of transpiration rate and leaf temperature.15) The transpiration rate was determined by the gravimetric method using an electronic top-loading balance (Mettler, PL-3000) at 28 }0.5 Ž, 75% RH. Pot was enclosed in a plastic bag to prevent evaporation of water from pot surface. Leaf area was determined with a photo-electric area meter (LI-COR, LI-3100). 84 (2) Environ. Control in Biol.
3 For other experiments, stomatal conductance was determined using a null balance diffusion porometer (LI-COR, LI-1600). Stomatal frequency The impressions were made on the abaxial and adaxial epidermis using thin films of cellulose acetate and the stomatal frequency was determined under a light microscope. Foliar necrosis Symptoms of O3 injury were generally not visible immediately after the exposure, and therefore the degree of foliar necrosis was determined in adopting six grades (0: no visible injury to 5: visible injury developed on whole area of a leaf) of necrosis on a leaf area basis at a day after the exposure. RESULTS Ontogenetic changes in stomatal frequency and stomatal conductance The ontogenetic changes in stomatal frequency and stomatal conductance are shown in Fig. 1 and Fig. 2 respectively. The abaxial stomatal frequency and stomatal conductance were higher than the adaxial at any leaf age. The stomatal frequency on both leaf surfaces decreased with increasing leaf age. But, the stomatal conductance increased from 7 days old leaves (young) to 10 days old leaves, then slowly decreased in 25 days old leaves (senescent). Ontogenetic changes in foliar necrosis To demonstrate the age-dependent sensitivity to O3, sunflower plants were exposed to 0.3 ppm O3 for 4 h and the degree of foliar necrosis was measured in the course of leaf ontogenetis (Fig. 3). The foliar necrosis in 8 days old leaves (young) was low and Fig. 1 Stomatal frequency on abaxial ( œ) and adaxial ( ) leaf surface during the ontogeny of the 3rd (counted from the bottom of plant) sunflower leaves. Each point represents the average of eight or more leaves ; bars represent } standard errors of the mean. Fig. 2 stomatal conductance on abaxial ( œ) and adaxial ( ) leaf surface during the ontogeny of the 3rd (counted from the bottom of plant) sunflower leaves. Each point represents the average of eight or more leaves; bars represent } standard errors of the mean. Vol. 26, No. 3 (1988) (3) 85
4 Fig. 3 Ontogenetic changes in 03-induced foliar necrosis appeared on the 3rd sunflower leaves. The degree of foliar necrosis was rated from 0 (no injury) to 5 (full necrosis). The foliar necrosis was determined a day after the exposure to 0.3 ppm O3 for 4 h and each leaf was assigned to one of these levels. Each point represents the average of three or more leaves; bars represent } standard errors of the mean. Fig. 4 Effect of 4 h exposure to 0.4 ppm O3 on stomatal conductance of the 3rd sunflower leaves during the leaf ontogenesis. The relative stomatal conductance is expressed as a percent of the respective rate prior to O3 exposure. The stomatal conductance was determined from transpiration rate and leaf temperature. The transpiration rate was determined by the gravimetric method using an electronic top-loading balance at 28 }0.5 Ž, 75% RH. Each point represents the average of three or more leaves; bars represent ± standard errors of the mean. the degree was 0.7. With increasing leaf age, the degree of foliar necrosis increased to the maximum value of 2.4 in 16 days old leaves. After this age, the foliar necrosis slowly decreased to the degree of 1.0 in 24 days old leaves (senescent). Effect of 03 on stomatal conductance Figure 4 represents the effect of 4 h exposure to 0.3 ppm O3 on the relative stomatal conductance of the different aged leaves. The percent of stomatal conductance shown in a figure is the representative value of the pre-treatment value. The stomatal conductance of 8 days old leaves (young) was not reduced to 85%, while that of 24 days old leaves (senescent) declined to 60% of the pre-treatment value. Relationship between foliar necrosis and O3 intake Figure 5 shows the relationship between the foliar necrosis appeared on various aged leaves and the total uptake of O3. The uptake rate of O3 was estimated by converting the stomatal conductance into the uptake rate using the diffusion coefficient of 03.16) The total uptake rate was obtained by integrating the calculated rate for the treatment periods (4 h). The results shown in this figure demonstrated that ontogenetic differences in foliar sensitivity to O3 did not have any relationship (r2 = 0.04) with the total uptake rate of O3. 86 (4) Environ. Control in Biol.
5 Fig. 5 The relationship between the degree of foliar necrosis and the total uptake of O3 in the 3rd sunflower leaves. The total uptake of O3 was estimated by the calculation using stomatal conductance and the ratio of diffusive conductance of O3 to water vapor. Data were the mean values shown in Figs. 3 and 4. DISCUSSION In the present experiment, we treated different aged sunflower leaves with O3 and determined the stomatal aperture to elucidate the ontogenetic changes in responses of plants to O3. The present results have shown that sensitivity to O3 differed markedly among different aged-leaves. Environmental factors, e.g. light,17) temperature,17) time of day,18) water availability,19) humidity,20) potassium nutrition21) affect the sensitivity of plants to O3. Such factors could be influencing stomatal aperture and the rate of diffusion of O3 into the leaves, since the main pathway of O3 for the entry into the leaf is stomata.1) Thus it is easily recognizable that the variability in O3 sensitivity between differently aged leaves could be based on differences in stomatal frequency or stomatal conductance. Some investigators22) reported that the foliar injury caused by O3 was correlated with the stomatal opening. However, others13,14) found no significant correlation between stomatal frequency or stomatal diffusive resistance and the specific differences in sensitivity to O3. Furthermore, Omasa et al.23) demonstrated using an image instrumentation method that stomatal response to O3 varied randomly at different sites on a single leaf. We have reached the same conclusion as described below. Despite the age-dependent decrease in stomatal frequency or the increase in degree of inhibition of stomatal conductance by O3, the ontogenetic changes in stomatal conductance and foliar necrosis were quite different. Mature leaves were more sensitive to O3 than young and senescent leaves in respect of stomatal conductance or foliar necrosis. But the leaf ages in which stomatal conductance and foliar necrosis reached the maximum value were different. These results may suggest that the ontogenetic changes in foliar sensitivity to O3 is not a reflection of stomatal frequency, stomatal conductance or O3-induced stomatal closure. Furthermore, as clearly shown in Fig. 5, the ontogenetic changes in foliar sensitivity was not the result of the magnitude of total uptake rate of O3. These results may suggest that O3 stimulates stomatal closure, but the relationship of these effects on ontogenetic changes in sensitivity to O3 is not related. There is the possibility that the rate of absorption of O3 is limited by a barrier after the stomata,24) and this internal barrier may be different between the different aged leaves. This speculation and those findings in the present study indicate the Vol. 26, No. 3 (1988) (5) 87
6 probable existence of a metabolically based resistance to O3 which is developmentally controlled. REFERENCES 1) BENNETT, J.H., A.C. HILL, and D.M. GATES A model for gaseous pollutant sorption by leaves. J. Air Pollut. Cont. Assoc. 23: ) HILL, A.C Vegetation: A sink for atmospheric pollutants. J. Air Pollut. Cont. Assoc. 21: ) UNSWORTH, M.H., P.V. BISCOE, and H.R. PINCKNEY Stomatal responses to sulphur dioxide. Nature 239: ) MAJERNIK, O., and T.A. MANSFIELD Direct effect of SO2 pollution on the degree of opening of stomata. Nature 227: ) BISCOE, P.V., M.H. UNSWORTH, and H.R. PINCKNEY The effects of low concentrations of sulphur dioxide on stomatal behavior in Vicia faba. New Phytol. 72: ) FURUKAWA, A.,O. ISODA, H. IWAKI, and T. TOTSUKA Interspecific differences in responses of transpiration to SO2. Environ. Control in Biol. 17: ) MENSER, H.A., and H.E. HEGGESTAD Ozone and sulfur dioxide synergism. Injury to tobacco plants. Science 153: ) MANSFIELD, T.A., and O. MAJERNIK Can stomata play a part in protecting plants against air pollutants? Environ. Pollut. 1: ) EVANS, L. S., and I. P. TING Ozone sensitivity of leaves: Relationship to leaf water content, gas transfer resistance, and anatomical characteristics. Am. J. Bot. 61: ) HILL, A.C., and N. LITTLEFIELD Ozone. Effect on apparent photosynthesis, rate of transpiration, and stomatal closure in plants. Environ. Sci. Tech. 3: ) FURUKAWA, A.,M. KATASE, T. USHIJIMA, and T. TOTSUKA Inhibition of photosynthesis of poplar species by ozone. J. Jap. For. Soc. 65: ) MENSER, H.A., H.E. HEGGESTAD, and O.E. STREET Response of plants to air pollutants. II. Effects of ozone concentration and leaf maturity on injury to Nicotiana tabaccum. phytopathology 53: ) TING, I.P., and W.M. DUGGER, Jr Factors affecting ozone sensitivity and susceptibility of cotton plants. J. Air Pollut. Control Assoc. 18: ) HARRIS, M.J., and R.L. HEATH Ozone sensitivity in sweet corn (Zea mays L.) plants: a possible relationship to water balance. Plant Physiol. 68: ) NOVEL, P.S Leaf anatomy and water use efficiency. In gadaptations of Plants to Water and High Temperature Stress h(eds. by Turner, N.C., and P.J. Kramer) 43-55, Wiley, New York. 16) OMASA, K., F. ABO, T. NATORI, and T. TOTSUKA Analysis of air pollutant sorption by plants. (3) Sorption under fumigation with NO2, O3 or NO2+O3. Res. Rep. Natl. Inst. Environ. Stud.11: ) MENSER, H.A., H.E. HEGGESTAD, O.E. STREET, and R.N. JEFFREY Response of plants to air pollutants. I. Effects of ozone on tobacco plants preconditioned by light and temperature. Plant Physiol. 38: ) HECK, W.W., and J.A. DUNNING The effects of ozone on tobacco and pinto bean as conditioned by several ecological factors. J. Air Pollut. Control Assoc. 17: ) TING, I.P., and W.M. DUGGER, Jr Ozone resistance in tobacco plants: A possible relationship to water balance. Atoms. Environ. 5: ) OTTO, H.W., and R.H. DAINES Plant injury by air pollutants: Influence of humidity on stomatal apertures and plant response to ozone. Science 163: ) LEONE, I.A Response of potassium-deficient tomato plants to atmospheric ozone. Phytopathology 66: ) LEE, T.T Sugar content and stomatal width as related to ozone injury in tobacco 88 (6) Environ. Control in Biol.
7 leaves. Can. J. Bot. 43: ) OMASA, K., Y. HASHIMOTO, and I. ALGA A quantitative analysis of the relationship between O3 sorption and its effects on leaves: Using image instrumentation. Environ. Control in Biol. 19: ) TINGEY, D.T., and G.E. TAYLOR, Jr Variation in plant response to ozone: A conceptual model of physiological events. In geffects of Gaseous Air Pollution in Agriculture and Horticulture h(eds. by Unsworth, M.H. and D.P. Ormrod) , Butterworth Scientific, London.
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