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Seasonal variation in ammonia compensation point and nitrogen pools in beech leaves (Fagus sylvatica)

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Abstract

Ammonia (NH3) fluxes between beech leaves (Fagus sylvatica) and the atmosphere were investigated in a 90-year-old forest canopy and related to leaf nitrogen (N) pools and glutamine synthetase (GS) activities. The stomatal ammonia compensation point, χNH3, was measured by both a twig cuvette and bioassay techniques involving measurements of pH and ammonium (NH +4 ) concentration in the leaf apoplastic solution. The χNH3 determined on the basis of the gas exchange measurements followed a seasonal variation with early-season peaks during leaf expansion (9.6 nmol NH3 mol−1 air) and late-season peaks during leaf senescence (7.3 nmol NH3 mol−1 air). In the mid-season, the χNH3 of mature green leaves was much lower (around 3 nmol NH3 mol−1 air) and dropped below the NH3 concentration in the ambient atmosphere. For comparison, χNH3 obtained by the apoplastic bioassay were 7.0, 3.7 and 6.4 nmol NH3 mol−1 air in early-, mid-, and late -season, thus agreeing reasonably well with χNH3 values derived from the gas exchange measurements. Potential NH3 emission fluxes during early and late season were 1.31 and 0.51 nmol m−2 leaf surface area s−1, respectively, while leaves were a sink for NH3 during mid-season. During leaf establishment and senescence, both apoplastic and bulk tissue NH +4 concentrations were relatively high coinciding with low activities of glutamine synthetase, which is a key enzyme in leaf N metabolism. In conclusion, the exchange of NH3 between beech leaves and the atmosphere followed a seasonal variation with NH3 emission peaks being related to N mobilization during early leaf establishment and remobilization during late leaf senescence.

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References

  • Andersen HV, Hovmand MF, Hummelshøj P, Jensen NO (1993) Measurements of ammonia flux to a spruce stand in Denmark. Atmos Environ Gen Topics 27:189–202

    Article  Google Scholar 

  • Asman W (1992) Ammonia emission in Europe: updated emission and emission variations. Rep. No. 228471008. RIVM, Bilthoven, The Netherlands

  • Beier C, Rasmussen L, Pilegaard K, Ambus P, Mikkelsen T, Jensen NO, Kjøller A, Priemé A, Ladekarl UL (2001) Fluxes of NO 3 , NH +4 , NO, NO2, and N2O in an old Danish beech forest. Water Air Soil Pollut Focus 1:187–195

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cole DW, Rapp M (1981) Element cycling in forest ecosystems. In: Reichle DE (ed) Dynamic properties of forest ecosystems. Cambridge University Press, Cambridge, pp 341–409

    Google Scholar 

  • Duyzer JH, Verhagen HLM, Weststrate JH (1992) Measurement of dry deposition flux of NH3 on to coniferous forest. Environ Pollut 75:3–13

    Article  PubMed  CAS  Google Scholar 

  • Duyzer JH, Verhagen HLM, Weststrate JH, Bosveld FC, Vermetten AWM (1994) Dry deposition of ammonia onto a douglas fir forest in the Netherlands. Atmos Environ 28:1241–1253

    Article  CAS  Google Scholar 

  • Farquhar GD, Wetselaar R, Weir B (1983) Gaseous nitrogen losses from plants. In: Freney JR, Simpson JR (eds) Gaseous nitrogen losses from plant-soil systems. Nijhoff, Hague, pp 159–180

    Google Scholar 

  • Field CB, Ball JT, Berry JA (1996) Photosynthesis: principles and field techniques. In: Pearcy RW, Ehleringer J, Mooney HA, Rundel PW (eds) Plant physiological ecology. Chapman and Hall, London, pp 209–248

    Google Scholar 

  • Finnemann J, Schjoerring JK (1999) Translocation of NH +4 in oilseed rape plants in relation to glutamine synthetase isogene expression and activity. Physiol Plant 105:469–477

    Article  CAS  Google Scholar 

  • Geβler A, Rennenberg H (1998) Atmospheric ammonia: mechanisms of uptake and impacts on N metabolism of Plants. In: Kok LD, Stulen I (eds) Responses of plant metabolism to air pollution and global changes. Backhuys, The Netherlands, pp 81–94

    Google Scholar 

  • Geβler A, Rienks M, Rennenberg H (2000) NH3 and NO2 fluxes between beech trees and the atmosphere—correlation with climatic and physiological parameters. New Phytol 147:539–560

    Article  Google Scholar 

  • Geβler A, Rienks M, Rennenberg H (2003) Stomatal uptake and cuticular adsorption contribute to dry deposition of NH3 and NO2 to needles of adult spruce (Picea abies) trees. New Phytol 156:179–194

    Google Scholar 

  • Glavac V, Jochheim H (1993) A contribution to understanding the internal nitrogen budget of beech (Fagus silvatica L.). Trees 7:237–241

    Article  Google Scholar 

  • Hanstein S, Mattsson M, Jaeger HJ, Schjoerring JK (1999) Uptake and utilization of atmospheric ammonia in three native poaceae species: leaf conductances, composition of apoplastic solution and interactions with root nitrogen supply. New Phytol 141:71–83

    Article  Google Scholar 

  • Herrmann B, Mattsson M, Fuhrer J, Schjoerring JK (2002) Leaf-atmosphere NH3 exchange of white clover (Trifolium repens L.) in relation to mineral N nutrition and symbiotic N2 fixation. J Exp Bot 53:139–146

    Article  PubMed  CAS  Google Scholar 

  • Hill PW, Raven JA, Loubet B, Fowler D, Sutton MA (2001) Comparison of gas exchange and bioassay determinations of the ammonia compensation point in Luzula sylvatica (Huds.) Gaud. Plant Physiol 125:476–487

    Article  PubMed  CAS  Google Scholar 

  • Husted S, Schjoerring JK (1995) Apoplastic pH and ammonium concentration in leaves of Brassica napus L. Plant Physiol 109:1453–1460

    PubMed  CAS  Google Scholar 

  • Husted S, Schjoerring JK (1996) Ammonia flux between oilseed rape plant and the atmosphere in response to changes in leaf temperature, light intensity and air humidity. Plant Physiol 112:67–74

    PubMed  CAS  Google Scholar 

  • Husted S, Mattsson M, Schjoerring JK (1996) Ammonia compensation points in two cultivars of Hordeum vulgare L. during vegetative and generative growth. Plant Cell Environ 19:1299–1306

    Article  Google Scholar 

  • Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000a) A critical evaluation of methods for determination of NH +4 in plant tissue, xylem sap and apoplastic fluid. Physiol Plant 109:167–179

    Article  CAS  Google Scholar 

  • Husted S, Schjoerring JK, Nielsen KH, Nemitz E, Sutton MA (2000b) Stomatal compensation points for ammonia in oilseed rape plants under field conditions. Agric For Meteorol 105:371–383

    Article  Google Scholar 

  • Katahata S, Naramoto M, Kakubari Y, Mukai Y (2007) Seasonal changes in photosynthesis and nitrogen allocation in leaves of different ages in evergreen understory shrub Daphniphyllum humile. Trees 21:619–629

    Article  CAS  Google Scholar 

  • Kesselmeier J, Meck L, Bliefernicht M, Helas G (1993) Trace gas exchange between terrestrial plants and atmosphere: carbon dioxide, carbonyl sulfide and ammonia under the rule of the compensation point. In: Slanina J, Angeletti G, Bielke S (eds) General Assessment of biogenic emission and deposition of nitrogen compounds, sulfur compounds and oxidants in Europe. Air Pollution Research Report 47, CEC, Brussels, pp 71–80

  • Koyama L, Tokuchi N, Fukushima K, Terai M, Yamamoto Y (2008) Seasonal changes in nitrate use by three woody species: the importance of the leaf-expansion period. Trees 22:851–859

    Article  CAS  Google Scholar 

  • Langford A, Fehsenfeld FC (1992) Natural vegetation as a source or sink for atmospheric ammonia—a case study. Science 255:581–583

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • Massad RS, Loubet B, Tuzet A, Cellier P (2008) Relationship between ammonia stomatal compensation point and nitrogen metabolism in arable crops: Current status of knowledge and potential modelling approaches. Environ Pollut 154:390–403

    Article  PubMed  CAS  Google Scholar 

  • Massad RS, Loubet B, Tuzet A, Autret H, Cellier P (2009) Ammonia stomatal compensation point of young oilseed rape leaves during dark/light cycles under various nitrogen nutritions. Agric Ecosyst Environ 133:170–182

    Article  CAS  Google Scholar 

  • Mattsson M, Schjoerring JK (2002) Dynamic and steady state responses of inorganic nitrogen pools and NH3 exchange in leaves of Lolium perenne and Bromus erectus to changes in root N supply. Plant Physiol 128:742–750

    Article  PubMed  CAS  Google Scholar 

  • Mattsson M, Schjoerring JK (2003) Senescence-induced changes in apoplastic and bulk tissue ammonia concentrations of rye-grass leaves. New Phytol 160:489–499

    Article  Google Scholar 

  • Mattsson M, Häusler RE, Leegood RC, Lea P, Schjoerring JK (1997) Leaf-atmosphere ammonia exchange in barley mutants with reduced activities of glutamine synthetase. Plant Physiol 114:1307–1312

    PubMed  CAS  Google Scholar 

  • Mattsson M, Husted S, Schjoerring JK (1998) Influence of nitrogen nutrition and metabolism on ammonia emission from plant leaves. Nutr Cycl Agroecosys 51:35–40

    Article  CAS  Google Scholar 

  • Mattsson M, Herrmann B, David M, Loubet B, Riedo M, Theobald MR, Sutton MA, Bruhn D, Neftel A, Schjoerring JK (2009) Temporal variability in bioassays of the stomatal ammonia compensation point in relation to plant and soil nitrogen parameters in intensively managed grassland. Biogeosciences 6:15–23

    Article  Google Scholar 

  • Nahm M, Matzarakis A, Rennenberg H, Geßler A (2007) Seasonal courses of key parameters of nitrogen, carbon and water balance in European beech (Fagus sylvatica L.) grown on four different study sites along a European North–South climate gradient during the 2003 drought. Trees 21:79–92

    Article  CAS  Google Scholar 

  • Neirynck J, Ceulemans R (2008) Bidirectional ammonia exchange above a mixed coniferous forest. Environ Pollut 154:424–438

    Article  PubMed  CAS  Google Scholar 

  • Neirynck J, Kowalski AS, Carrara A, Ceulemans R (2005) Driving forces for ammonia fluxes over mixed forest subjected to high deposition loads. Atmos Environ 39:5013–5024

    Article  CAS  Google Scholar 

  • Nielsen KH, Schjoerring JK (1998) Regulation of apoplastic ammonium concentration in leaves of oilseed rape. Plant Physiol 118:1361–1368

    Article  PubMed  CAS  Google Scholar 

  • Nielsen KH, Schjoerring JK, Erisman JW, Pearson J (2002) Ammonia exchange at the tree-atmosphere interface. In: Gasche R, Papen H, Rennenberg H (eds) Trace gas exchange in forest ecosystems. Kluwer Academic, The Netherlands, pp 159–173

    Google Scholar 

  • Nord-Larsen T, Johannsen VK, Jørgensen BB, Bastrup-Birk A (2008) Forests and plantations 2006 (Danish text). Forestry and Landscape, Hoersholm 2008, 185 pp. ISBN 978-87-7903-369-6 (internet)

  • Pearson J, Ji YM (1994) Seasonal-variation of leaf glutamine-synthetase isoforms in temperate deciduous trees strongly suggests different functions for the enzymes. Plant Cell Environ 17:1331–1337

    Article  CAS  Google Scholar 

  • Pearson J, Stewart G (1993) The deposition of atmospheric ammonia and its effect on plants. New Phytol 125:283–305

    Article  CAS  Google Scholar 

  • Pearson J, Woodall J, Clough ECM, Nielsen KH, Schjoerring JK (2002) Production and consumption of NH3 in trees. In: Gasche R, Papen H, Rennenberg H (eds) Trace gas exchange in forest ecosystems. Kluwer Academic, The Netherlands, pp 53–77

    Google Scholar 

  • Pepin S, Livingston NJ (1997) Rates of stomatal opening in conifer seedlings in relation to air temperature and daily carbon gain. Plant Cell Environ 20:1462–1472

    Article  Google Scholar 

  • Pilegaard K, Hummelshøj B, Jensenb NO, Chen Z (2001) Two years of continuous CO2 eddy-flux measurements over a Danish beech forest. Agric For Meteorol 107:29–41

    Article  Google Scholar 

  • Pilegaard K, Mikkelsen TN, Beier C, Jensen NO, Ambus P, Ro-Poulsen H (2003) Field measurement of atmosphere-biosphere interactions in a Danish beech forest. Boreal Environ Res 8:315–333

    CAS  Google Scholar 

  • Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

    Article  PubMed  Google Scholar 

  • Rennenberg H, Kreutzer K, Papen H, Weber P (1998) Consequences of high loads of nitrogen for spruce (Picea abies) and beech (Fagus sylvatica) forests. New Phytol 139:71–86

    Article  CAS  Google Scholar 

  • Schjoerring JK, Husted S (1997) Measurement of ammonia gas emission from plants. In: Linskens HK, Jackson JF (eds) Modern methods in plant analysis. Springer Verlag, Berlin, pp 73–95

    Google Scholar 

  • Schjoerring JK, Husted S, Mattsson M (1998a) Physiological parameters controlling plant-atmosphere ammonia exchange. Atmos Environ 32:491–498

    Article  CAS  Google Scholar 

  • Schjoerring JK, Husted S, Poulsen M (1998b) Soil-plant-atmosphere NH3 exchange associated with Calluna vulgaris and Deschampsia flexuosa. Atmos Environ 32:507–512

    Article  CAS  Google Scholar 

  • Schjoerring JK, Husted S, Mäck G, Nielsen KH, Finnemann J, Mattsson M (2000) Physiological regulation of plant-atmosphere ammonia exchange. Plant Soil 221:95–102

    Article  CAS  Google Scholar 

  • Schneider S, Geβler A, Weber P, von Sengbusch D, Hanemann U, Rennenberg H (1996) Soluble N compounds in trees exposed high loads of N: a comparison of spruce (Picea abis) and beech (Fagus sylvatica) grown under field conditions. New Phytol 134:103–114

    Article  CAS  Google Scholar 

  • Soares A, Ming JY, Pearson J (1995) Physiological indicators and susceptibility of plants to acidifying atmospheric pollution: a multivariate approach. Environ Pollut 87:159–166

    Article  PubMed  CAS  Google Scholar 

  • Sutton MA, Fowler D, Moncrieff JB (1993) The exchange of atmospheric ammonia with vegetated surfaces. I: Unfertilized vegetation. Q J R Meteorol Soc 119:1023–1045

    Article  Google Scholar 

  • van Hove LWA (1989) The mechanism of NH3 and SO2 uptake by leaves and its physiological effects. Ph.D. Thesis, Wageningen Agricultural University, The Netherlands

  • Wyers GP, Erisman JW (1998) Ammonia exchange over a coniferous forest. Atmos Environ 32:441–451

    Article  CAS  Google Scholar 

  • Wyers GP, Vermeulen AT, Slanina J (1992) Measurement of dry deposition of ammonia on a forest. Environ Pollut 75:25–28

    Article  PubMed  CAS  Google Scholar 

  • Wyers GP, Otjes R, Slanina J (1993) A continuous-flow denuder for the measurement of ambient concentrations and surface exchange fluxes of ammonia. Atmos Environ 27:2085–2090

    Google Scholar 

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Acknowledgements

The work was supported financially by the European Union Framework Programme 6 as part of the Integrated Project NitroEurope (www.nitroeurope.eu). The assistance of Dr. Kent Høier Nielsen with the gas exchange measurements and manuscript preparation is gratefully acknowledged.

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Correspondence to Jan Kofod Schjoerring.

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Responsible Editor: Per Ambus.

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Wang, L., Xu, Y. & Schjoerring, J.K. Seasonal variation in ammonia compensation point and nitrogen pools in beech leaves (Fagus sylvatica). Plant Soil 343, 51–66 (2011). https://doi.org/10.1007/s11104-010-0693-7

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