Photosynthesis and growth responses of Fraxinus mandshurica Rupr. seedlings to a gradient of simulated nitrogen deposition

  • Miao Wang
  • Wei-Wei Zhang
  • Na Li
  • Yan-Yan Liu
  • Xing-Bo Zheng
  • Guang-You Hao
Original Paper


Key message

During an N-deposition simulation experiment, we showed that low to medium addition of N had beneficial effects on growth and photosynthetic rates of Fraxinus mandshurica Rupr. seedlings, while beyond a threshold of 80 kg N ha −1  year −1 , performance plateaued and even declined at higher immissions.


Temperate forests are shifting from naturally N-limited toward N-saturated status with increasing N deposition. Yet, our knowledge regarding how seedling growth and physiology respond to excessive N input in temperate tree species remains very limited.


The objective of this study was to examine growth and photosynthetic responses of F. mandshurica seedlings to a gradient of simulated N deposition.


We conducted a 4-year study to investigate growth and photosynthetic responses of F. mandshurica seedlings to a large gradient of simulated N deposition (0, 20, 40, 60, 80, 100, and 120 kg N ha−1 year−1). Biomass accumulation and allocation, photosynthetic gas exchange, expression, and activities of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in leaves were determined during the fourth growing season. Soil biochemical properties were measured to link them to the alterations in growth and photosynthetic traits across the N addition gradient.


Seedling growth and photosynthesis were dependent upon the rates of N deposition. The maximum rate of carboxylation (V c,max) and the net photosynthetic rate under saturating light (A sat) reached a maximum under 60 kg N ha−1 year−1. By contrast, high-level N inputs (100 and 120 kg N ha−1 year−1) resulted in suboptimal values in biomass and photosynthetic activity. Nitrogen deposition also modulated the activity and expression of Rubisco in leaves with a maximum around 80–100 kg N ha−1 year−1. Redundancy analysis (RDA) showed that the changes of seedling growth and photosynthesis along the gradient of N deposition were mostly attributed to the variations of soil pH and total N content.


Our data suggest that the threshold of N deposition is about 80 kg N ha−1 year−1 for F. mandshurica seedlings in this region. Excessive N input decreased performance on the seedling growth and photosynthesis.


Fraxinus mandshurica Photosynthetic response Nitrogen deposition Rubisco Biomass production 



We thank the staff from CBFERS for their assistance in collecting field data.

Data availability

Some metadata are available at

Funding information

This work was funded by the National Natural Science Foundation of China (31722013, 31500222, 31670412) the key project of Ministry of Science and Technology of China (2016YFA0600803), the project QYZDJ-SSW-DQC027 and the Hundred Talents Program from the Chinese Academy of Sciences.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.


  1. Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems: hypotheses revisited. Bioscience 48(11):921–934. CrossRefGoogle Scholar
  2. Aber JD, Goodale CL, Ollinger SV, Smith ML, Magill AH, Martin ME, Hallett RA, Stoddard JL (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? Bio Science 53:375–389Google Scholar
  3. Azuchi F, Kinose Y, Matsumura T, Kanomata T, Uehara Y, Kobayashi A, Yamaguchi M, Izuta T (2014) Modeling stomatal conductance and ozone uptake of Fagus crenata grown under different nitrogen loads. Environ Pollut 184:481–487. CrossRefPubMedGoogle Scholar
  4. BassiriRad H (2015) Consequences of atmospheric nitrogen deposition in terrestrial ecosystems: old questions, new perspectives. Oecologia 177(1):1–3. CrossRefPubMedGoogle Scholar
  5. Blancojuan A, Wei X, Jiang H, Jie C, Xin Z (2012) Impacts of enhanced nitrogen deposition and soil acidification on biomass production and nitrogen leaching in Chinese fir plantations. Can J For Res 42(3):437–450. CrossRefGoogle Scholar
  6. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20(1):30–59. CrossRefPubMedGoogle Scholar
  7. Boxman AW, Blanck K, Brandrud TE, Emmett BA, Gundersen P, Hogervorst RF, Kjonaas OJ, Persson H, Timmermann V (1998) Vegetation nd soil biota response to experimentally-changed nitrogen inputs in coniferous forest ecosystems of the NITREX project. For Ecol Manag 101(1-3):65–79. CrossRefGoogle Scholar
  8. Braun S, Thomas VFD, Quiring R, Fluckiger W (2010) Does nitrogen deposition increase forest production? The role of phosphorus. Environ Pollut 158(6):2043–2052. CrossRefPubMedGoogle Scholar
  9. Brown KR, Thompson WA, Camm EL, Hawkins BJ, Guy RD (1996) Effects of N addition rates on the productivity of Picea Sitchensis, Thuja plicata, and Tsuga heterophylla seedlings: II. Photosynthesis, 13C discrimination and N partitioning in foliage. Trees 10:198–205CrossRefGoogle Scholar
  10. Bubier JL, Smith R, Juutinen S, Moore TR, Minocha R, Long S, Minocha S (2011) Effects of nutrient addition on leaf chemistry, morphology, and photosynthetic capacity of three bog shrubs. Oecologia 167(2):355–368. CrossRefPubMedGoogle Scholar
  11. Carroll JA, Caporn SJM, Johnson D, Morecroft MD, Lee JA (2003) The interactions between plant growth, vegetation structure and soil processes in semi–natural acidic and calcareous grasslands receiving long–term inputs of simulated pollutant nitrogen deposition. Environ Pollution 21:363–376CrossRefGoogle Scholar
  12. Chen H, Gurmesa GA, Zhang W, Zhu X, Zheng M, Mao Q, Mo J (2015) Nitrogen saturation in humid tropical forests after 6 years of nitrogen and phosphorus addition: hypothesis testing. Funct Ecol 30:305–313CrossRefGoogle Scholar
  13. Cheng L, Fuchigami LH (2000) Rubisco activation state decreases with increasing nitrogen content in apple leaves. J Exp Bot 51(351):1687–1694. CrossRefPubMedGoogle Scholar
  14. Diaz-Alvarez EA, Lindig-Cisneros R, de la Barrera E (2015) Responses to simulated nitrogen deposition by the neotropical epiphytic orchid Laelia speciosa. Peer J 3:e1021. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ethier GJ, Livingston NJ, Harrison DL, Black TA, Moran JA (2006) Low stomatal and internal conductance to CO2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves. Plant Cell Environ 29(12):2168–2184. CrossRefPubMedGoogle Scholar
  16. Fang Y, Yoh M, Koba K, Zhu W, Takebayashi YU, Xiao Y, Lei C, Mo JM, Zhang W, Lu X (2011) Nitrogen deposition and forest nitrogen cycling along an urban–rural transect in southern China. Glob Chang Biol 17(2):872–885. CrossRefGoogle Scholar
  17. Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly AD, McNulty SG, Ryan DF, Stottlemyer R (1998) Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8(3):706–733.[0706:NEINAE]2.0.CO;2 CrossRefGoogle Scholar
  18. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878):889–892. CrossRefPubMedGoogle Scholar
  19. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53(4):341–356.[0341:TNC]2.0.CO;2 CrossRefGoogle Scholar
  20. Hungate BA, Dukes JS, Shaw MR, Luo YQ (2003) Field CB nitrogen and climate change. Science 302(5650):1512–1513. CrossRefPubMedGoogle Scholar
  21. Hyvönen R, Agren GI, Linder S, Persson T, Cotrufo MF, Ekblad A, Freeman M, Grelle A, Janssens IA, Jarvis PG, Kellomäki S, Lindroth A, Loustau D, Lundmark T, Norby RJ, Oren R, Pilegaard K, Ryan MG, Sigurdsson BD, Strömgren M, van Oijen M, Wallin G (2007) The likely impact of elevated (CO2), nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol 173(3):463–480. CrossRefPubMedGoogle Scholar
  22. Hättenschwiler S, Körner C (1998) Biomass allocation and canopy development in spruce model ecosystems under elevated CO2 and increased N deposition. Oecologia 113:104–114CrossRefGoogle Scholar
  23. Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117(6):481–494. CrossRefPubMedGoogle Scholar
  24. Högberg P, Fan H, Quist M, Binkley D, Tamm CO (2006) Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob Chang Biol 112:489–499CrossRefGoogle Scholar
  25. Jiang Y, Zhang WT, Wang MC, Kang MY, Dong MY (2014) Radial growth of two dominant montane conifer tree species in response to climate change in North–central China. PLoS One 13:e112537CrossRefGoogle Scholar
  26. Kinose Y, Azuchi F, Uehara Y, Kanomata T, Kobayashi A, Yamaguchi M, Izuta T (2014) Modeling of stomatal conductance to estimate stomatal ozone uptake by Fagus crenata, Quercus serrata, Quercus mongolica var. crispula and Betula platyphylla. Environ Pollut 194:235–245. CrossRefPubMedGoogle Scholar
  27. Kinose Y, Fukamachi Y, Okabe S, Hiroshima H, Watanabe M, Izuta T (2017) Photosynthetic responses to ozone of upper and lower canopy leaves of Fagus crenata Blume seedlings grown under different soil nutrient conditions. Environ Pollut 223:213–222. CrossRefPubMedGoogle Scholar
  28. Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer Verlag, New York 540, DOI:
  29. Latham RE (1992) Co–occurring tree species change rank in seedling performance with resources varied experimentally. Ecology 73(6):2129–2144. CrossRefGoogle Scholar
  30. Li D, Mo J, Fang Y, Cai X, Xue J, Xu G (2004) Effects of simulated nitrogen deposition on growth and photosynthesis of Schima superba, Castanopsis chinensis and Cryptocarya concinna seedlings. Acta Ecol Sin 24:876–882Google Scholar
  31. Liao YC, Fan HB, Li YY, Liu WF, Yuan YH (2010) Effects of simulated nitrogen deposition on growth and photosynthesis of 1-year-old Chinese fir (Cunninghamia lanceolata) seedlings. Acta Ecol Sin 30(3):150–154. CrossRefGoogle Scholar
  32. Liu X, Duan L, Mo J, Du E, Shen J, Lu X, Zhang Y, Zhou X, He C, Zhang F (2011) Nitrogen deposition and its ecological impacts in China: an overview. Environ Pollut 159(10):2251–2264. CrossRefPubMedGoogle Scholar
  33. Liu X, Fan Y, Long J, Wei R, Kjelgren R, Gong C, Zhao J (2013b) Effects of soil water and nitrogen availability on photosynthesis and water use efficiency of Robiniap seudoacacia seedlings. J Environ Sci 25(3):585–595. CrossRefGoogle Scholar
  34. Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013a) Enhanced nitrogen deposition over China. Nature 494(7438):459–462. CrossRefPubMedGoogle Scholar
  35. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54(392):2393–2401. CrossRefPubMedGoogle Scholar
  36. Lu X, Mo J, Gilliam FS, Yu G, Zhang W, Fang Y, Huang J (2010) Effects of experimental nitrogen additions on plant diversity in an old–growth tropical forest. Glob Chang Biol 16(10):2688–2700. CrossRefGoogle Scholar
  37. Manter DK, Kavanagh KL, Rose CL (2005) Growth response of Douglas-fir seedlings to nitrogen fertilization: importance of Rubisco activation state and respiration rates. Tree Physiol 25(8):1015–1021. CrossRefPubMedGoogle Scholar
  38. Mitchell A, Hinckley T (1993) Effects of foliar nitrogen concentration on photosynthesis and water used efficiency in Douglas-fir. Tree Physiol 12(4):403–410. CrossRefPubMedGoogle Scholar
  39. Mohren GM, Ilvesniemi H (1995) Modelling effects of soil acidification on tree growth and nutrient status. Ecol Model 83(1-2):263–272. CrossRefGoogle Scholar
  40. Nakaji T, Fukami M, Dokiya Y, Izuta T (2001) Effects of high nitrogen load on growth, photosynthesis and nutrient status of Cryptomeria japonica and Pinus densiflora seedlings. Tree Str Funct 15:453–461Google Scholar
  41. Pons TL, Poorter H (2014) The effect of irradiance on the carbon balance and tissue characteristics of five herbaceous species differing in shade-tolerance. Front Plant Sci 5:12. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Shangguan Z, Shao MA, Dyckmans J (2000) Nitrogen nutrition and water stress effects on leaf photosynthetic gas exchange and water use efficiency in winter wheat. Environ Exp Bot 44(2):141–149. CrossRefPubMedGoogle Scholar
  43. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30(9):1035–1040. CrossRefPubMedGoogle Scholar
  44. Shipley B, Lechowiczm MJ, Wright I, Reich PB (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87(3):535–541. CrossRefPubMedGoogle Scholar
  45. Stitt M, Schulze ED (1994) Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant Cell Environ 17(5):465–487. CrossRefGoogle Scholar
  46. Templer PH, Pinder RW, Goodale CL (2012) Effects of nitrogen deposition on greenhouse-gas fluxes for forests and grasslands of North America. Frontiers in Ecology and Environment 10(10):547–553. CrossRefGoogle Scholar
  47. Tetteh R, Yamaguchi M, Wada Y, Funada R, Izuta T (2015) Effects of ozone on growth, net photosynthesis and yield of two African varieties of Vigna unguiculata. Environ Pollut 196:230–238. CrossRefPubMedGoogle Scholar
  48. Wang M, Shi S, Lin F, Hao Z, Jiang P, Dai G (2012) Effects of soil water and nitrogen on growth and photosynthetic response of Manchurian ash (Fraxinus mandshurica) seedlings in northeastern China. PLoS One 7(2):e30754. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wang AY, Wang M, Yang D, Song J, Zhang WW, Han SJ, Hao GY (2016) Responses of hydraulics at the whole-plant level to simulated nitrogen deposition of different levels in Fraxinus mandshurica. Tree Physiol 36(8):1045–1055. CrossRefPubMedGoogle Scholar
  50. Warren CR, Dreyer E, Adams MA (2003) Photosynthesis-Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores. Trees 17:359–366Google Scholar
  51. Wortman E, Tomaszewski T, Waldner P, Schleppi P, Thimonier A, Eugster W, Buchmann N, Sievering H (2012) Atmospheric nitrogen deposition and canopy retention influences on photosynthetic performance at two high nitrogen deposition Swiss forests. Tellus B 64(1):17216. CrossRefGoogle Scholar
  52. Zhang M, Guan DX, Han SJ, Wu J, Zhang J, Jin M, Dai G (2005) Climatic dynamics of broadleaved Korean pine forest in Changbai Mountain during the last 22 years. Chin J Ecol 24:1007–1012Google Scholar
  53. Zhou WM, Guo Y, Zhu BK, Wang XY, Zhou L, Yu DP, Dai L (2015) Seasonal variations of nitrogen flux and composition in a wet deposition forest ecosystem on Changbai Mountain. Acta Ecol Sin 35:158–164Google Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.Key Laboratory of Environment Change and Resources Use in Beibu Gulf (Guangxi Teachers Education University)Ministry of EducationNanningChina

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