Plant and Soil

, Volume 221, Issue 1, pp 95–102 | Cite as

Physiological regulation of plant-atmosphere ammonia exchange

  • Jan K. Schjoerring
  • Søren Husted
  • Gisela Mäck
  • Kent Høier Nielsen
  • Jørgen Finnemann
  • Marie Mattsson
Article

Abstract

Plants have a compensation point for NH3 which ranges from 0.1 to 20 nmol mol-1, and may be several-fold higher or lower than naturally occurring atmospheric NH3 concentrations. This implies that NH3 fluxes over vegetated surfaces are bi-directional and that ammonia exchange with the atmosphere in many cases contributes significantly to the nitrogen economy of vegetation. Physiological regulation of plant–atmosphere NH3 fluxes is mediated via processes involved in nitrogen uptake, transport and metabolism. A rapid turnover of NH3+ in plant leaves leads to the establishment of a finite NH3+ concentration in the leaf apoplastic solution. This concentration determines, together with that of H+, the size of the NH3 compensation point. Barley and oilseed rape plants with access to NH3+ in the root medium have higher apoplastic NH3+ concentrations than plants absorbing NO3-. Furthermore, the apoplastic NH3+ concentration increases with the external NH3+ concentration. Inhibition of GS leads to a rapid and substantial increase in apoplastic NH3+ and barley mutants with reduced GS activity have higher apoplastic NH3+ than wild-type plants. Increasing rates of photorespiration do not affect the steady-state NH3+ or H+ concentration in tissue or apoplast of oilseed rape, indicating that the NH3+ produced is assimilated efficiently. Nevertheless, NH3 emission increases due to a temperature-mediated displacement of the chemical equilibrium between gaseous and aqueous NH3 in the apoplast. Sugarbeet plants grown with NO3- seem to be temporarily C-limited in the light due to a repression of respiration. As a consequence, the activity of chloroplastic GS declines during the day causing a major part of NH3+ liberated in photorespiration to be assimilated during darkness when 2-oxoglutarate is supplied in high rates by respiration.

ammonia exchange apoplast atmosphere glutamine synthetase nitrogen photorespiration 

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References

  1. Asman W A H 1994 Emission and deposition of ammonia and ammonium. Nova Acta Leopoldina 70, 263–297.Google Scholar
  2. Atkin O K, Westbeek MH M, Cambridge ML, Lambers H and Pons T L 1997 Leaf respiration in light and darkness. Plant Physiol. 113, 961–965.PubMedGoogle Scholar
  3. Brooks A and Farquhar G D 1995 Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406.CrossRefGoogle Scholar
  4. Dannel F, Pfeffer H and Marschner H 1995 Isolation of apoplasmic fluid from sunflower leaves and its use for studies on influence of nitrogen supply on apoplasmic pH. J. Plant Physiol. 146, 273–278.Google Scholar
  5. Dentener F J and Crutzen P J 1994 A three dimensional model of the global ammonia cycle. J. Atmos. Chem. 19, 331–369.CrossRefGoogle Scholar
  6. Duyzer J H, Verhagen H L M, Westrate J H, Bosveld F C and Vermetten A W M 1994 The dry deposition of ammonia onto a douglas fir forest in the Netherlands. Atmos. Environ. 28, 1241–1258.CrossRefGoogle Scholar
  7. Farquhar G D, Firth P M, Wetselaar R and Weir B 1980 On the gaseous exchange of ammonia between leaves and the environment: determination of the ammonia compensation point. Plant Physiol. 66, 710–714.PubMedCrossRefGoogle Scholar
  8. Finnemann J and Schjoerring J K 1999 Translocation of NH4+ in oilseed rape plants in relation to glutamine synthetase isogene expression and activity. Physiol. Plant. 105, 469–477.CrossRefGoogle Scholar
  9. Glass A D M, Erner Y, Kronzucker H, Schjoerring J K, Siddiqi M Y and Wang M-Y 1997 Ammonium fluxes into plant roots: energetics, kinetics and regulation. J. Plant Nutr. Soil Sci. 160, 261–268.Google Scholar
  10. Häusler R E, Blackwell R D, Lea P J and Leegood R C 1994 Control of photosynthesis in barley leaves with reduced activities of glutamine synthetase or glutamate synthase. I. Plant characteristics and change of nitrate, ammonium and amino acids. Planta 194, 406–417.Google Scholar
  11. Hoffmann B, Planker R and Mengel K 1992 Measurements of pH in the apoplast of sunflower leaves by means of fluorescence. Physiol. Plant 84, 146–153.CrossRefGoogle Scholar
  12. Husted S and Schjoerring J K 1995 Apoplastic pH and ammonium concentration in leaves of Brassica napus L. Plant Physiol. 109, 1453–1460.PubMedGoogle Scholar
  13. Husted S and Schjoerring J K 1996 Ammonia flux between oilseed rape plants and the atmosphere in response to changes in leaf temperature, light intensity and relative air humidity. Interactions with stomatal conductance and apoplastic NH4+ and H+ concentrations. Plant Physiol. 112, 67–74.PubMedGoogle Scholar
  14. Husted S, Mattsson M and Schjoerring J K 1996 Ammonia compensation points in two cultivars of Hordeum vulgare L. during vegetative and generative growth. Plant Cell Environ. 19, 1299–1306.CrossRefGoogle Scholar
  15. Joy K W 1988 Ammonia, glutamine, and asparagine: a carbonnitrogen interface. Can. J. Bot. 66, 2103–2109.Google Scholar
  16. Krömer S 1995 Respiration during photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 45–70.CrossRefGoogle Scholar
  17. Langford A O and Fehsenfeld F C 1992 Natural vegetation as a source or sink for atmospheric ammonia: a case study. Science 255, 581–583.PubMedGoogle Scholar
  18. Lea P J, Blackwell R B and Joy KW1992 Ammonia assimilation in higher plants. In Nitrogen Metabolism of Plants. Eds K Mengel and D J Pilbeam. pp 153–186. Oxford Scientific Publishers, New York.Google Scholar
  19. Leegood R C, Lea P J, Adcock M D and Häusler R E 1995 The regulation and control of photorespiration. J. Exp. Bot. 46, 1397–1414.Google Scholar
  20. Ludwig R A 1991 Plants shuttle CO2 equivalents as carbamoyl phosphate from mitochondria to chloroplasts. In Molecular Approaches to Compartmentation and Metabolic Regulation. Eds H C Huang and L Taiz. pp 99–112. American Society Plant Physiologists, Rockville.Google Scholar
  21. Ludwig R A 1993 Arabidopsis chloroplasts dissimilate L-arginine and L-citrulline for use as N source. Plant Physiol. 101, 429–434.PubMedCrossRefGoogle Scholar
  22. Mattsson M and Schjoerring J K 1996 Ammonia emission from young barley plants: influence of N source, light/dark cycles, and inhibition of glutamine synthetase. J. Exp. Bot. 47, 477–484.Google Scholar
  23. Mattsson M, Lundborg T and Larsson C-M 1993 Nitrogen utilization in N-limited barley during vegetative and generative growth. IV. Translocation and remobilization of nitrogen. J. Exp. Bot. 44, 537–546.Google Scholar
  24. Mattsson M, Häusler R E, Leegood R C, Lea P and Schjoerring J K 1997 Leaf-atmosphere ammonia exchange in barley mutants with reduced activities of glutamine synthetase. Plant Physiol. 114, 1307–1312.PubMedGoogle Scholar
  25. Mattsson M, Husted S and Schjoerring J K 1998 Influence of nitrogen nutrition and metabolism on ammonia emission from plant leaves. Nutr. Cycling Agroecosyst. 51, 35–40.CrossRefGoogle Scholar
  26. Mühling K H and Sattelmacher B 1995 Apoplastic ion concentration of intact leaves of field bean (Vicia faba) as influenced by ammonium and nitrate nutrition. J. Plant Physiol. 147, 81–86.Google Scholar
  27. Nielsen K H and Schjoerring J K 1998 Regulation of apoplastic ammonium concentration in leaves of oilseed rape. Plant Physiol. 118, 1361–1368.PubMedCrossRefGoogle Scholar
  28. Ninnemann O, Jauniaux J-C and Frommer W B 1994 Identification of a high affinity NH4+ transporter from plants. EMBO J. 13, 3464–3471.PubMedGoogle Scholar
  29. Oaks A 1994 Primary nitrogen assimilation in higher plants and its regulation. Can. J. Bot. 72, 739–750.Google Scholar
  30. O'Deen W A 1989 Wheat volatilized ammonia and resulting nitrogen isotopic fractionation. Agron. J. 81, 980–985.CrossRefGoogle Scholar
  31. O'Deen W A and Porter L K 1986 Continuous flow system for collecting volatile ammonia and amines from senescing wheat. Agron. J. 78, 746–749.CrossRefGoogle Scholar
  32. Olsen C, Mattsson M and Schjoerring J K 1995 Ammonia volatilization in relation to nitrogen nutrition of young Brassica napus plants growing with controlled nitrogen supply. J. Plant Physiol. 147, 306–312.Google Scholar
  33. Parton W J, Morgan J A, Altenhofen J M and Harper L A 1988 Ammonia volatilization from spring wheat plants. Agron. J. 80, 419–425.CrossRefGoogle Scholar
  34. Pitcairn C E R, Fowler D and Grace J 1995 Deposition of fixed atmospheric nitrogen and foliar nitrogen content of bryophytes and Calluna vulgaris (L.) Hull. Environ. Pollut. 88, 193–205.PubMedCrossRefGoogle Scholar
  35. Schjoerring J K 1991 Ammonia emission from the foliage of growing plants. In Trace Gas Emissions by Plants. Eds T D Sharkey, H A Mooney and E A Holland. pp 267–292. Academic Press, New York.Google Scholar
  36. Schjoerring J K 1997 Plant-atmosphere ammonia exchange. Quantification, physiological regulation and interactions with environmental factors. D.Sc. Thesis, 55 pp. DSR Publishers, Copenhagen.Google Scholar
  37. Schlesinger W H and Hartley A E 1992 A global budget for atmospheric NH3. Biogeochemistry 15, 191–211.CrossRefGoogle Scholar
  38. Sutton M A, Moncrieff J B and Fowler D 1992 Deposition of atmospheric ammonia to moorlands. Environ. Pollut. 75, 15–24.PubMedCrossRefGoogle Scholar
  39. Sutton M A, Fowler D and Moncrieff J B 1993 The exchange of atmospheric ammonia with vegetated surfaces. I: Unfertilized vegetation. Q. J. R. Meteorol. Soc. 119, 1023–1045.CrossRefGoogle Scholar
  40. Sutton M A, Asman W A H and Schjoerring J K 1994 Dry deposition of reduced nitrogen. Tellus 46, 255–273.CrossRefGoogle Scholar
  41. Sutton M A, Schjoerring J K and Wyers P 1995 Plant-atmosphere exchange of ammonia. Phil. Trans. R. Soc. London 351, 261–278.Google Scholar
  42. Söderlund R and Svensson B H 1976 The global nitrogen cycle. Ecol. Bull. (Stockholm) 22, 23–73.Google Scholar
  43. Wallsgrove R M, Keys A J, Lea P J and Miflin B J 1983 Photosynthesis, photorespiration and nitrogen metabolism. Plant Cell Environ. 6, 301–309.Google Scholar
  44. Wyers G P, Vermeulen A T and Slanina J 1992 Measurements of dry deposition of ammonia on a forest. Environ. Pollut. 75, 25–28.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Jan K. Schjoerring
  • Søren Husted
  • Gisela Mäck
  • Kent Høier Nielsen
  • Jørgen Finnemann
  • Marie Mattsson

There are no affiliations available

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