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Physiology of ecotypic plant response to sulfur dioxide in Geranium carolinianum L.

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Summary

Populations of Geranium carolinianum, a winter annual plant common in disturbed habitats, vary in their foliar response to sulfur dioxide, and pollution resistance is characteristic of populations sampled from areas in which SO2 has been a prominent stress. The physiological basis of this ecotypic response was investigated using a whole-plant gaseous exchange system in which leaf resistance to H2O efflux and SO2 influx were concurrently monitored. Individual plants of distinct SO2 susceptibility were exposed to pollutant concentrations of either 0.4, 0.6 or 0.8 μl 1-1 in both the dark and light. Total SO2 flux (μg cm-2 h-1) to the plant, which is the sum of leaf adsorptive and absorptive loss, varied as an inverse function of leaf resistance (s cm-1), and the relationship was modeled using linear regression techniques. Total SO2 flux was partitioned to leaf surface and internal fractions using estimation procedures with the regression analysis. SO2 flux into the leaf interior, the pollutant fraction responsible for causing foliar injury, was strikingly similar for resistant and sensitive plants at each concentration. Resistant plants must absorb 30% more SO2 than their sensitive counterparts in order to exhibit comparable levels of foliar injury. Therefore, in G. carolinianum the predominant explantation for genetically controlled and quantitatively inherited differences in plant résponse to SO2 is not variable pollutant flux but rather disparate physiological-biochemical processes affecting pollutant toxicity, cellular perturbation and repair. This conclusion is relevant to understanding how populations of G. carolinianum respond over time to elevated levels of SO2 and may explain the inherent susceptibility of this species compared with plants with which it co-exists.

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References

  • Ashenden TW (1979) The effects of long-term exposures to SO2 and NO2 pollution on the growth of Dactylus glomerata L. and Poa pratensis L. Environ Pollut 18:249–258

    Google Scholar 

  • Barton JR, McLaughlin SB, McConathy RK (1980) The effects of SO2 on components of leaf resistance to gas exchange. Environ Pollut Ser A 21:255–265

    Google Scholar 

  • Bell JNB, Mudd CH (1976) Sulphur dioxide resistance in plants: a case study of Lolium perenne. In: Mansfield TA (ed) Effects of Air Pollutants on Plants. Cambridge Univ Press, New York

    Google Scholar 

  • Bell JNB, Clough WS (1973) Depression of yield in ryegrass exposed to sulphur dioxide. Nature 241:47–49

    Google Scholar 

  • Black CR, Black VJ (1979) The effects of low concentrations of sulphur dioxide on stomatal conductance and epidermal cell survival in field bean (Vicia faba L.). J exp Bot 30:291–298

    Google Scholar 

  • Bonte J, Bonte C, de Cormis L, Louguet P (1977) Contribution à l'étude des caractères de resistance de Pelargonium à un pollutant atmospherique, le dioxyde de soufre. Physiol vég 15:15–27

    Google Scholar 

  • Bonte J, Louguet P (1975) Interrelations entre la pollution par le dioxyde de soufre et le mouvement des stomates chez le Pelargonium x hortorum: effects de l'humidité relative et de la teneur en gaz carbonique de l'air. Physiol vég 13:527–537

    Google Scholar 

  • Börtitz S (1968) Physiologische und biochemische Beiträge zur Rauchschadensforschung. 8. Mitt. Physiologische Untersuchungen über die Wirkung von SO2 auf den Stoffwechsel von Koniferennadeln in Winter. Biol Abl 87:489–506

    Google Scholar 

  • Braun G (1977) Über die Ursachen und Kriterien der Immissionsresistenz bei Fichte, Picea abies (L.) Karst. II. Reflektorische Immissionsresistenz. Eur J For Path 7:129–152

    Google Scholar 

  • Bressan RA, Wilson LG, Filner P (1978) Mechanisms of resistance to sulfur dioxide in the Cucurbitaceae. Plant Physiol 61:761–767

    Google Scholar 

  • Caput C, Belot Y, Auclair D, Decourt N (1978) Absorption of sulphur dioxide by pine seedlings leading to acute injury. Environ Pollut 16:3–15

    Google Scholar 

  • Catcheside DG (1975) Chemicals, radiation, and heredity. Search 6:23–28

    Google Scholar 

  • Craker LE, Starbuck JS (1973) Leaf age and air pollutant susceptibility: uptake of ozone and sulfur dioxide. Environ Res 6:91–94

    Google Scholar 

  • Davies T (1980) Grasses more sensitive to SO2 pollution in conditions of low irradiance and short days. Nature 284:483–485

    Google Scholar 

  • de Cormis L, Bonte J (1970) Étude du degagement d'hydrogène sulfuré par des feuilles de plantes avant reçu du dioxyde de soufre. CR Acad Sc Paris, t 277:2078–2080

    Google Scholar 

  • Downs RJ, Hellmers H (1975) Evironment and the Experimental Control of Plant Growth. Academic Press, New York

    Google Scholar 

  • Dunn DB (1959) Some effects of air pollution on Lupinus in the Los Angeles area. Ecology 40:621–625

    Google Scholar 

  • Elkiey T, Ormrod DP (1980) Sorption of ozone and sulfur dioxide by Petunia leaves. J Environ Quality 9:93–95

    Google Scholar 

  • Esterbauer H (1976) Biochemischer Wirkungsmechanismus von Abgasen. Umschau 76:349–350

    Google Scholar 

  • Fried M (1948) The absorption of sulfur dioxide by plants as shown by the use of radioactive sulfur. Proc Soil Sci of Amer 13:135–138

    Google Scholar 

  • Garsed SG, Read DJ (1977) The uptake and metabolism of 35SO2 in plants of differing sensitivity to sulphur dioxide. Environ Pollut 13:173–187

    Google Scholar 

  • Gaastra P (1959) Photosynthesis of crop plants as influences by light, carbon dioxide, temperature and stomatal resistance. Meded Landbowhoogesch Wageningen 13:1–68

    Google Scholar 

  • Gressel J, Segel LA (1978) The paucicity of plants evolving genetic resistance to herbicides: possible reasons and implications. J theor Biol. 75:349–371

    Google Scholar 

  • Grill D (1972) Pufferkapazität gesunder und rauchgeschädigter Fichtennadeln. Pflkrankh 10:612–622

    Google Scholar 

  • Grill O, Härtel O (1972) Zellphysiologische und biochemische Untersuchungen an SO2-begasten Fichtennadeln. Resistenz und Pufferkapazität. Mitt Forstl Bundes-Vers-Anst Wien 97:367–384

    Google Scholar 

  • Härtel O, Miklau-Grassl S (1974) Über den Einfluß von SO2 auf Pflanzenzellen. Phyton 16:81–99

    Google Scholar 

  • Hocking D, Hocking MB (1977) Equilibrium solubility of trace atmospheric sulphur dioxide in water and its bearing on air pollution injury to plants. Environ Pollut 13:57–64

    Google Scholar 

  • Horsman DC, Wellburn AR (1977) Effect of SO2 polluted air upon enzyme activity in plants originating from areas with different annual mean atmospheric SO2 concentration. Environ Pollut 13:33–39

    Google Scholar 

  • Horsman DC, Roberts FM, Bradshaw AD (1979) Studies on the effect of sulphur dioxide on perennial ryegrass (Lolium perenne L.). II. Evolution of sulphur dioxide tolerance. J exp Bot 30:495–501

    Google Scholar 

  • Jäger HJ (1975) Wirkung von SO2-Begasung auf die Aktivität von Enzymen des Aminosäurestoffwechsels und den Gehalt freier Aminosäuren in unterschiedlich resistenten Pflanzen. Z Pflkrankh Pflschutz 82:139–148

    Google Scholar 

  • Jensen KF, Kozlowski TT (1975) Absorption and translocation of sulfur dioxide in seedlings of four forest tree species. J Environ Qual 4:379–382

    Google Scholar 

  • Juhren M, Noble W, Went FW (1957) The standardization of Poa annua as an indicator of smog concentrations. I. Effects of temperature, photoperiod, and light intensity during growth of test plants. Plant Physiol. 32:576–586

    Google Scholar 

  • Keller T (1978) Wintertime atmospheric pollutants — do they affect performance of deciduous trees in the ensuing growing season. Environ Pollut 16:243–247

    Google Scholar 

  • Klein H, Jäger HJ, Domes W, Wong CH (1978) Mechanisms contributing to differential sensitivities of plants to SO2. Oecologia (Berl) 33:203–208

    Google Scholar 

  • Klepper LA (1979) Author's reply. Atmosph Environ 13:1475

    Google Scholar 

  • Kondo H, Sugahara K (1978) Changes in transpiration rate of SO2-resistant and sensitive plants with SO2 fumigation and the participation of abscisic acid. Plant and Cell Physiol 19:365–373

    Google Scholar 

  • Lange OL (1965) Leaf temperatures and methods of measurement. In: methodology of Plant Ecophysiology, Proceedings of the Montpellier Symposium (F Eckardt) (ed) UNESCO. pp 203–209

  • Levitt J (1972) Responses of Plants to Environmental Stresses. Academic Press, New York

    Google Scholar 

  • Lüttge U, Osmond CB, Ball E, Brinckmann E, Kinze G (1972) Bisulfite compounds as metabolic inhibitors: nonspecific effects on membranes. Plant and Cell Physiol. 13:505–514

    Google Scholar 

  • Malhotra SS, Hocking D (1976) Biochemical and cytological effects of sulphur dioxide on plant metabolism. New Phytol 76:227–237

    Google Scholar 

  • Malhotra SS (1976) Effects of sulphur dioxide on biochemical activity and ultrastructural organization of pine needle chloroplasts. New Phytol 76:239–245

    Google Scholar 

  • Mansfield TA (1973) The role of stomata in determining the responses of plants to air pollutants. In: Smith H (ed) Current Advances in Plant Sciences. Pergamon Press, New York, pp 13–22

    Google Scholar 

  • McLaughlin SB Jr (1972) Botanical studies in the vicinity of Johnsonville steam plant: Results of surveys conducted in 1972. Tennessee opment, Muscle Shoals, Alabama, EBB-72-5

    Google Scholar 

  • Meidner H (1975) Water supply, evaporation, and vapour diffusion in leaves. J exp Bot 26:666–673

    Google Scholar 

  • Miller JE, Xerikos PB (1979) Residence time of sulphite in SO2 ‘sensitive’ and ‘tolerant’ soybean cultivars. Environ Pollut 18:259–264

    Google Scholar 

  • Mudd JB (1975) Sulfur dioxide. In: Mudd JB and Kozlowski TT (eds) Responses of Plants to Air Pollution. Academic Press, New York, pp 8–22

    Google Scholar 

  • Murdy WH (1979) Effect of SO2 on sexual reproduction in Lepidium virginicum L. originating from regions with different SO2 concentrations. Bot Gaz 140:299–303

    Google Scholar 

  • Nobel PS (1974) Introduction to Biophysical Plant Physiology. WH Freeman and Co, San Francisco

    Google Scholar 

  • Noland TL, Kozlowski TT (1979) Effect of SO2 on stomatal aperture and sulfur uptake of woody angiosperm seedlings. Can J For Res 9:57–62

    Google Scholar 

  • Pahlich E (1973) Über den Hemm-Mechanismus mitochondrialer Glutamat-Oxalacetat-Transaminase in SO2-begasten Erbsen. Planta 110:267–278

    Google Scholar 

  • Priebe A, Klein H, Jäger HJ (1978) Role of polyamines in SO2-polluted pea plants. J exp Bot 29:1045–1050

    Google Scholar 

  • Puckett KJ, Tomassini FD, Nieboer E, Richardson DNS (1977) Potassium efflux by lichen thalli following exposure to aqueous sulphur dioxide. New Phytol 79:135–145

    Google Scholar 

  • Rosen PM, Musselman RC, Kender WJ (1978) Relationship of stomatal resistance to sulfur dioxide and ozone injury in grapevines. Scientia Hort 8:137–142

    Google Scholar 

  • Schindlbeck WE (1977) Biochemische Beiträge zur Immissionsforschung. Forstwiss Central Ct 96:67–71

    Google Scholar 

  • Sestak Z, Catsky J, Jarvis PG (1971) Plant Photosynthetic Production. Manual of methods. Dr W Junk N U Publ, The Hague

    Google Scholar 

  • Silvius JE, Ingle M, Baer CH (1975) Sulfur dioxide inhibition of photosynthesis in isolated spinach chloroplasts. Plant Physiol 56:434–437

    Google Scholar 

  • Silvius JE, Baer CH, Dodrill S, Patrick H (1976) Photoreduction of sulfur dioxide by spinach leaves and isolated spinach chloroplasts. Plant Physiol 27:799–801

    Google Scholar 

  • Sokolowski AW (1976) Zjawisko selekeji pod wplywem prezemyslowych zanieczyszcen powietrza. Pr Inst Badaw Lesn 478/482:181–185

    Google Scholar 

  • Snedecor GW, Cochran WG (1967) Statistical Methods 6th Edition. The Iowa State University Press, Ames Iowa

    Google Scholar 

  • Soldatini GF, Ziegler I, Ziegler H (1978) Sulfite: preferential sulfur source and modifier of CO2 fixation in Chlorella vulgaris. Planta 143:231–2551

    Google Scholar 

  • Taylor GE Jr, Murdy WH (1975) Population differentiation of an annual plant species, Geranium carolinianum L., in response to sulfur dioxide. Bot Gaz 136:212–215

    Google Scholar 

  • Taylor GE Jr (1976) The evolutionary process of population differentiation of an annual plant species, Geranium carolinianum L., in response to sulfur dioxide. PhD Dissertation, Emory University, Atlanta Georgia, pp 172

    Google Scholar 

  • Taylor GE Jr (1978a) Genetic analysis of ecotypic differentiation within an annual plant species, Geranium carolinianum L., in response to sulfur dioxide. Bot Gaz 139:362–368

    Google Scholar 

  • Taylor GE Jr (1978b) Plant and leaf resistance to gaseous air pollution stress. New Phytol 80:523–534

    Google Scholar 

  • Taylor GE Jr, Tingey DT (1979) A gas-exchange system for assessing plant performance in response to environmental stress. U.S. Environmental Protection Agency, Corvallis Environmental Research Laboratory, Corvallis Oregon EPA-600/3-79-108

  • Tingey DT, Manning M, Grothaus LC, Burns WF (1979) The influence of light and temperature on isoprene emission rates from live oak. Physiol Plant 47:112–118

    Google Scholar 

  • Unsworth MH, Biscoe PU, Black V (1976) Analysis of gas exchange between plants and polluted atmospheres. In: Mansfield TA (ed) Effects of Air Pollutants on Plants. Cambridge Univ Press, New York

    Google Scholar 

  • Winner WE, Mooney HA (1980a) Ecology of SO2 resistance: I. Effects of fumigations on gas exchange of deciduous and evergreen shrubs. Oecologia (Berl) 44:290–295

    Google Scholar 

  • Winner WE, Mooney HA (1980b) Ecology of SO2 resistance: II. Photosynthetic changes of shrubs in relation to SO2 absorption and stomatal behavior. Oecologia (Berl). 44:296–302

    Google Scholar 

  • Winner WE, Mooney HA Ecology of SO2 resistance: III. Metabolic changes of C3 and C4 Atriplex species due to SO2 fumigation. Oecologia (Berl) (in press)

  • Ziegler I (1972) The effect of SO 32 on the activity of ribulose 1,5 diphosphate carboxylase in isolated spinach chloroplasts. Planta 103:155–163

    Google Scholar 

  • Ziegler I (1975) The effect of SO 32 pollution on plant metabolism. In: Gunther FA and Gunther JD (eds) Residue Reviews. Vol 56:79–106

  • Ziegler I (1977) Subcellular distribution of 35S-sulfur in spinach leaves after application of 35SO 2-4 and 35SO2. Planta 135:25–32

    Google Scholar 

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  1. G. E. Taylor Jr.

    Present address: Terrestrial Division, Corvallis Environmental Research Laboratory, U.S. Environmental Protection Agency, 97330, Corvallis, Oregon, USA

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  1. Environmental Sciences Division, Oak Ridge National Laboratory, 37830, Oak Ridge, Tennessee, USA

    G. E. Taylor Jr. & D. T. Tingey

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Taylor, G.E., Tingey, D.T. Physiology of ecotypic plant response to sulfur dioxide in Geranium carolinianum L.. Oecologia 49, 76–82 (1981). https://doi.org/10.1007/BF00376901

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