Plant and Soil

, Volume 131, Issue 2, pp 235–245 | Cite as

Long-term effects of SO2 on plants, SO2 metabolism and regulation of intracellular pH

  • M. J. Kropff
Article
Received:

Abstract

The impact of SO2 on the ionic balance of plants and its implications for intracellular pH regulation was studied to find explanations for long-term effects of SO2. When sulphur, taken up as SO2 by the shoots of plants, is not assimilated in organic compounds, but stored as sulphate, an equivalent amount of H+ is produced. These H+ ions are not buffered chemically, but removed by metabolic processes.

On the basis of knowledge on metabolic buffering mechanisms a conceptual model is proposed for the removal of shoot-generated H+ by (i) OH- ions, produced in the leaves when sulphate and nitrate are assimilated in organic compounds and/or by (ii) OH- ions produced by decarboxylation of organic anions (a biochemical pH stat mechanism). The form in which nitrogen is supplied largely determines the potential of the plant to neutralize H+ in the leaves during SO2 uptake by the proposed mechanisms.

In field experiments with N2 fixing Vicia faba L. crops, the increase of sulphate in the shoots of SO2-exposed plants was equivalent in charge to the decrease of organic anion content, calculated as the difference between inorganic cation content (C) and inorganic anion content (A), indicating that H+ ions produced in the leaves following SO2 uptake were partly removed by OH- from sulphate reduction and partly by decarboxylation of organic anions.

The appearance of chronic SO2 injury (leaf damage) in the field experiment at the end of the growing period is discussed in relation to the impact of SO2 on the processes involved in regulation of intracellular pH. It is proposed that the metabolic buffering capacity of leaf cells is related to the rates of sulphate and nitrate reduction and the import rate of organic anions, rather than to the organic anion content in the vacuoles of the leaf cells.

Key words

anions cations chronic injury nutrition open-air fumigation senescence yield Vicia faba L. 
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References

  1. Allen S and Raven J A 1987 Intracellular pH regulation in Ricinus communis grown with ammonium or nitrate as N source: The role of long-distance transport. J. Exp. Bot. 38, 580–596.Google Scholar
  2. Alscher R, Bower J L and Zipfel W 1987 The basis for different sensitivities of photosynthesis to SO2 in two cultivars of pea. J. Exp. Bot. 38, 99–108.Google Scholar
  3. Anbazhagan M, Krishnamurthy R and Bhagwart K A 1988 Proline: An enigmatic indicator of air pollution tolerance in rice cultivars. J. Plant Physiol. 133, 122–123.Google Scholar
  4. Arnon D I 1939 Effect of ammonium and nitrate nitrogen on the mineral composition and sap characteristics of barley. Soil Sci. 48, 295–307.Google Scholar
  5. Ashenden T W and Mansfield T A 1978 Extreme pollution sensitivity of grasses when SO2 and NO2 are present in the atmosphere together. Nature 273, 142–143.CrossRefPubMedGoogle Scholar
  6. Baker C K, Colls J J, Fullwood A E and Seaton G G R 1986 Depression of growth and yield in winter barley exposed to sulphur dioxide in the field. New Phytol. 104, 233–241.Google Scholar
  7. Bell J N B and Clough W S 1973 Depression of yield in ryegrass exposed to sulphur dioxide. Nature 241, 47–49.CrossRefGoogle Scholar
  8. Ben Zioni A, Vaadia Y and Lips S H 1971 Nitrate uptake by roots as regulated by nitrate reduction products of the shoot. Physiol. Plant. 24, 288–290.Google Scholar
  9. Beusichem M Lvan 1981 Nutrient absorption by pea plants during nitrogen fixation. I. Comparison with nitrate nutrition. Neth. J. Agric. Sci. 30, 317–33.Google Scholar
  10. Beusichem M Lvan 1983 Xylary charge distribution and nitrogen transport in Pisum sativum L. during dinitrogen fixation or nitrate nutrition. Z. Pflanzenfysiol. 109, 449–458.Google Scholar
  11. Beusichem M L van 1984 Non-ionic Nitrogen Nutrition of Plants. Ph.D. thesis Agricultural University Wageningen. 141 p.Google Scholar
  12. Beusichem M Lvan, Kirkby E A and Baas R 1988a Influence of nitrate and ammonium nutrition on the uptake, assimilation and distribution of nutients in Ricinus communis. Plant Physiol. 86, 914–921.Google Scholar
  13. Beusichem M Lvan, Nelemans J A and Bienfait H F 1988b Interrelationships between trans-plasma membrane electron/proton transfer stoichiometry, organic acid metabolism, and nitrate reduction in Dwarf Bean (Phaseolus vulgaris). Plant Physiol. 87, 269–273.Google Scholar
  14. Brunold C, Landolt W and Lavanchy P 1983 SO2 and assimilatory sulfate reduction in beech leaves. Physiol. Plant. 59, 313–318.Google Scholar
  15. Bytnerowycz A, Olszyk D M, Kats G, Dawson P J, Wolf J and Thompson C R 1987 Effects of SO2 on physiology, elemental content and injury development of winter wheat. Agr. Ecosyst. Environ. 20, 37–47.CrossRefGoogle Scholar
  16. Coleman R G and Richards F J 1956 Physiological studies in plant nutrition. XVIII. Some aspects of nitrogen metabolism in barley and other plants in relation to potassium deficiency. Ann. Bot. 20, 393–409.Google Scholar
  17. Colvill K E, Horsman D C, Roose M L, Roberts T M and Bradshaw A D 1985 Field trials on the influence of air pollutants, and sulphur dioxide in particular, on the growth of ryegrass (Lolium perenne L.). Environ. Pollut. Ser. A 39, 235–266.CrossRefGoogle Scholar
  18. Cowling D W and Bristow A W 1979 Effects of SO2 on sulphur and nitrogen fractions and on free amino acids in perennial ryegrass. J. Sci. F. Agric. 30, 354–360.Google Scholar
  19. Darrall N M and Jäger H-J 1984 Biochemical diagnostic tests for the effect of air pollution on plants. In Gaseous Air Pollutants and Plant Metabolism. Eds. M L Koziol and F R Whatley. pp. 333–349. Butterworths, London, Wellington.Google Scholar
  20. Davies D D 1973 Metabolic control in higher plants In Biosynthesis and Its Control in Plants. Ed. B V Milborrow pp 1–20. Academic Press, New York.Google Scholar
  21. Davies D D 1986 The fine control of cytosolic pH. Physiol. Plant. 67, 702–706.Google Scholar
  22. Davies T 1980 Grasses more sensitive to SO2 pollution in conditions of low irradiance and short days. Nature 284, 483–485.CrossRefGoogle Scholar
  23. Dijkshoorn W 1962 Metabolic regulation of the alkaline effect of nitrate utilization in plants. Nature 194, 165–167.Google Scholar
  24. Eaton F, Olmstead W R and Taylor O C 1971 Salt injury to plants with special reference to cations versus anions and ion activities. Plant and Soil 35, 533–547.Google Scholar
  25. Faller N, Herwig K and Kuhn H 1970 Die Aufnahme von Schwefeldioxid aus der Luft. 1. Einfluss auf den pflanzlichen Ertrag. Plant and Soil 33, 177–191.Google Scholar
  26. Flores H E and Galston A W 1984 Osmotic stress-induced polyamine accumulation in cereal leaves. Plant Physiol. 75, 102–109.Google Scholar
  27. Gasch G, Grünhage L, Jäger H-J and Wentzel K-F 1988 Das Verhältnis der Schwefelfractionen in Fichtennadeln als Indikator für Immissionsbelastungen durch Schwefeldioxid. Angew. Bot. 62, 73–84.Google Scholar
  28. Grill D 1971 Die Pufferkapazität gesunder und rauchgeschädigter Fichtennadeln. Z. Pflanzenkr. Pflanzensch. 78, 612–622.Google Scholar
  29. Grill D, Esterbauer H and Klotsch U 1979 Effect of sulfur dioxide on glutathione in leaves of plants. Environ. Pollut. Ser. A 19, 187–194.Google Scholar
  30. Hållgren J-E and Fredriksson S 1982 Emission of hydrogen sulfide from sulfur dioxide fumigated pine trees. Plant Physiol. 70, 456–459.Google Scholar
  31. Hållgren J-E, Linder S, Richter A, Troeng E and Granat L 1982 Uptake of SO2 in shoots of scots pine: Field measurements of net flux of sulphur in relation to stomatal conductance. Plant Cell Environ. 5, 75–83.Google Scholar
  32. Houba V F G, vanEgmond F and Wittich E M 1971 Changes in production of organic nitrogen and carboxylates (C-A) in young sugarbeet plants grown in nutrient solutions of different nitrogen composition. Neth. J. Agric. Sci. 19, 39–47.Google Scholar
  33. Irving P M and Miller J E 1984 Synergistic effect on field-grown soybeans from combinations of sulfur dioxide and nitrogen dioxide. Can. J. Bot. 62, 840–846.Google Scholar
  34. Israel D W and Jackson W A 1982 Ion balance, uptake, and transport processes in N2-fixing and nitrate- and urea-dependent soybean plants. Plant Physiol. 69, 171–178.Google Scholar
  35. Jäger H-J and Klein H 1976 Modellversuche zum Einfluss der Nährstoffversorgung auf die SO2-Empfindlichkeit von Pflanzen. Eur. J. For. Pathol. 6, 347–354.Google Scholar
  36. Jäger H-J and Klein H 1977 Biochemical and physiological detection of sulfur dioxide injury to pea plants (Pisum sativum). J. Air Pollut. Control Assoc. 27, 464–466.Google Scholar
  37. Jäger H-J and Klein H 1980 Biochemical and physiological effects of SO2 on plants. Angew. Bot. 54, 337–348.Google Scholar
  38. Jäger H-J, Bender J and Grünhage L 1985 Metabolic responses of plants differing in SO2 sensitivity towards SO2 fumigation. Environ. Pollut. Ser. A 39, 317–335.CrossRefGoogle Scholar
  39. Jones T and Mansfield T A 1982 Studies on dry matter partitioning and distribution of 14C-labelled assimilates in plants of Phleum pratense exposed to SO2 pollution. Environ. Pollut. Ser. A 28, 199–207.CrossRefGoogle Scholar
  40. Klein H and Jäger H-J 1976 Einfluss der Nährstoffversorgung auf die SO2-Empfindlichkeit von Erbsenpflanzen. Z. Pflanzenkr. Pflanzensch. 83, 555–568.Google Scholar
  41. Kropff M J 1990 The effects of long-term SO2 exposure on a field crop of broad bean (Vicia faba L.). I. Quantitative analysis of damage components. New Phytol. 115, 357–365.Google Scholar
  42. Kropff M J 1989 Modeling short term effects of sulphur dioxide. I. A model for the flux of SO2 into leaves and effects on leaf photosynthesis. Neth. J. Plant Pathol. 95, 195–213.CrossRefGoogle Scholar
  43. Kropff M J and Goudriaan J 1989 Modelling short-term effects of sulphur dioxide. III. The effect of SO2 on photosynthesis of leaf canopies. Neth. J. Pl. Pathol. 95, 265–280.CrossRefGoogle Scholar
  44. Kropff M J, Mooi J, Goudriaan J, Smeets W, Leemans A, Kliffen C and van derZalm A J A 1989a The effects of long-term SO2 exposure on a field crop of broad bean (Vicia faba L.). I. Depression of growth and yield. New Phytol. 113 337–344.Google Scholar
  45. Kropff M J, Mooi J, Goudriaan J, Smeets W, Leemans A, Kliffen C 1989b The effects of long-term SO2 exposure on a field crop of broad bean (Vicia faba L.). II. Effects on growth components leaf area development and elemental composition. New Phytol. 113, 345–351.Google Scholar
  46. Laisk A, Pfanz H, Schramm M J and Heber U 1988a Sulphur-dioxide fluxes into different cellular compartments of leaves photosynthesizing in a polluted atmosphere. I. Computer analysis. Planta 173, 230–240.CrossRefGoogle Scholar
  47. Laisk A, Pfanz H and Heber U 1988b Sulphur-dioxide fluxes into different cellular compartments of leaves photosynthesizing in a polluted atmosphere. II. Consequences of SO2 uptake as revealed by computer analysis. Planta 173, 241–252.CrossRefGoogle Scholar
  48. Legge A H, Bogner J C and Krupa S V 1988 Foliar sulphur species in Pine, a new indicator of a forest ecosystem under air pollution stress. Environ. Pollut. Ser. A 55, 15–27.Google Scholar
  49. Linzon S N 1978 Effects of airborne sulphur pollutants on plants. In Sulphur in the Environment, Part II: Ecological Impacts. Ed. I O Nriagu. pp 109–162. Wiley, New York.Google Scholar
  50. Maas F A 1987 Responses of Plants to Sulfur Containing Air Pollutants (H2S and SO2). Ph.D. thesis. University Groningen. 110 p.Google Scholar
  51. Olsen R A 1957 Absorption of sulfur dioxide from the atmosphere by cotton plants. Soil Sci. 84, 107–111.Google Scholar
  52. Pierre M and Queiroz O 1982 Modulation by leaf age and SO2 concentration of the enzymic response to subnecrotic SO2 pollution. Environ. Pollut. Ser. A 28, 209–212.CrossRefGoogle Scholar
  53. Priebe A, Klein H and Jäger H-J 1978 Role of polyamines in SO2-polluted pea plants. J. Exp. Bot. 29, 1045–1050.Google Scholar
  54. Raven J A 1986 Biochemical disposal of excess H+ in growing plants. New Phytol. 104, 175–206.Google Scholar
  55. Raven J A 1988 Acquisition of nitrogen by the shoots of land plants: Its occurrence and implications for acid-base regulation. New Phytol. 109, 1–20.Google Scholar
  56. Raven J A and Smith F A 1976 Nitrogen assimilation and transpiration in vascular land plants in relation to intracellular pH regulation. New Phytol. 76, 415–431.Google Scholar
  57. Rennenberg H 1984 The fate of excess sulfur in higher plants. Annu. Rev. Plant Physiol. 35, 121–153.CrossRefGoogle Scholar
  58. Sakai T and Kondo N 1985 Inhibition of photosynthesis by sulfite in mesophyll protoplasts isolated from Vicia faba L. in relation to intracellular sulfite accumulation. Plant Cell Physiol. 26, 1045–1055.Google Scholar
  59. Sekiya J, Schmidt A, Rennenberg H, Wilson L G and Filner P 1982 Hydrogen sulfide emission by cucumber leaves in response to sulfate in light and dark. Phytochemistry 23, 2173–2178.CrossRefGoogle Scholar
  60. Smith F A and Raven J A 1979 Intracellular pH and its regulation. Annu. Rev. Plant Physiol. 30, 289–311.CrossRefGoogle Scholar
  61. Taylor H J and Bell J N B 1988 Studies on the tolerance to SO2 of grass populations in polluted areas. V. Investigations into the development of tolerance to SO2 and NO2 in combination and NO2 alone. New Phytol. 110, 327–338.Google Scholar
  62. Thomas M D, Hendricks H R, Collier G R and Hill G R 1943 The utilization of sulfate and sulphur dioxide for the nutrition of alfalfa. Plant Physiol. 18, 345–371.Google Scholar
  63. Thomas M D Hendricks H R and Hill G R 1944 Some chemical reactions of sulfur dioxide after absorption by alfalfa and sugarbeets. Plant Physiol. 19, 212–226.Google Scholar
  64. Whitmore M E and Mansfield T A 1983 Effects of long-term exposures to SO2 and NO2, on Poa pratensis and other grasses. Environ. Pollut. Ser. A 31, 217–235.CrossRefGoogle Scholar
  65. Wilson L G, Bressan R A and Filner P 1978 Light-dependent emission of hydrogen sulfide from plants. Plant Physiol. 61, 184–189.Google Scholar
  66. Wit C T de, Dijkshoorn W and Noggle J C 1963 Ionic balance and growth of plants. Versl. Landbouwk. Onderz. 69–15, Wageningen.Google Scholar
  67. Young N D and Galston A W 1983 Putrescine and acid stress. Plant Physiol. 71, 767–771.Google Scholar
  68. Zeevaart A J 1976 Some effects of fumigating plants for short periods with NO2 Environ. Pollut. Ser. A 11, 97–108.Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • M. J. Kropff
    • 1
  1. 1.Department of Theoretical Production EcologyAgricultural University WageningenWageningenThe Netherlands

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