, Volume 54, Issue 4, pp 598–610 | Cite as

Ecophysiological responses of Cunninghamia lanceolata to nongrowing-season warming, nitrogen deposition, and their combination

  • L. Yu
  • T. F. Dong
  • Y. B. Lu
  • M. Y. Song
  • B. L. Duan
Original papers


Warming winter and atmospheric nitrogen (N) deposition are expected to have effects on net primary production (NPP) of Chinese fir (Cunninghamia lanceolata) plantation and implications for plantation carbon sequestration. The effects of nongrowing-season warming on plant morphological and physiological traits were investigated in a greenhouse experiment with two-year-old C. lanceolata seedlings. Elevated temperature (ET) during the nongrowing season significantly increased the net photosynthetic characteristics. The strongest effects occurred during warming period from 1 December 2014 to 1 February 2015 (W1). Moreover, the carbohydrate concentration was elevated due to the warming during W1, but it declined during four months of the warming (from 1 December 2014 to 1 April 2015, W2). The seedlings kept under N deposition (CN) showed a positive effect in all the above-mentioned parameters except δ13C. Significant interactions between ET and N deposition were observed in most parameters tested. At the end of the experiment (W2), the seedlings exposed to a combined ET and N deposition treatment exhibited the highest carbon contents. Our results showed that N deposition might ameliorate the negative effects of the winter warming on the carbon content.

Additional key words

chlorophyll fluorescence fructose gas exchange malondialdehyde reactive oxygen species starch 



ambient temperature


control (ambient temperature and 0 g N deposition)




intercellular CO2 concentration


control + nitrogen deposition (+1 g N)


dry mass


elevated temperature


nitrogen deposition (+1 g N) + elevated temperature (+2°C)


fresh mass


maximal quantum yield of PSII photochemistry


stomatal conductance




net photosynthetic rate


dark respiration


reactive oxygen species


two months of warming treatment


four months of warming treatment


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aiken R.M., Smucker A.J.M.: Root system regulation of whole plant growth.–Annu. Rev. Phytopathol. 34: 325–346, 1996.CrossRefPubMedGoogle Scholar
  2. Andresen L.C., Michelsen A.: Off-season uptake of nitrogen in temperate heath vegetation.–Oecologia 144: 585–597, 2005.CrossRefPubMedGoogle Scholar
  3. Bingham I.J., Rees R.M.: Senescence and N release from clover roots following permanent excision of the shoot.–Plant Soil 303: 229–240, 2008.CrossRefGoogle Scholar
  4. Bokhorst S., Bjerke J.W., Davey M.P. et al.: Impacts of extreme winter warming events on plant physiology in a sub-Arctic heath community.–Physiol. Plantarum 140: 128–140, 2010.CrossRefGoogle Scholar
  5. Bowler C., Montagu M.V., Inze D.: Superoxide dismutase and stress tolerance.–Annu. Rev. Plant Phys. 43: 83–116, 1992.CrossRefGoogle Scholar
  6. Chen J., Dong T.F., Duan B.L. et al.: Sex competition and N supply interactively affect the dimorphism and competiveness of opposite sexes in Populus cathayana.–Plant Cell Environ. 38: 1285–1298, 2015.CrossRefPubMedGoogle Scholar
  7. Danby R.K., Hik D.S.: Variability, contingency and rapid change in recent subarctic alpine tree line dynamics.–J. Ecol. 95: 352–363, 2007.CrossRefGoogle Scholar
  8. Dong T.F., Zhang Y.X., Zhang Y.B. et al.: Continuous planting under a high density enhances the competition for nutrients among young Cunninghamia lanceolata saplings.–Ann. For. Sci. 73: 331–339, 2015.CrossRefGoogle Scholar
  9. Easterling D.R., Horton B., Jones P.D. et al.: Maximum and minimum temperature trends for the globe.–Science 277: 364–367, 1997.CrossRefGoogle Scholar
  10. Elser J.J., Kyle M., Steger L. et al.: Nutrient availability and phytoplankton nutrient limitation across a gradient of atmospheric nitrogen deposition.–Ecology 90: 3062–3073, 2009.CrossRefPubMedGoogle Scholar
  11. Fazeli F., Ghorbanli M., Niknam V.: Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two sesame cultivars.–Biol. Plantarum 51: 98–103, 2007.CrossRefGoogle Scholar
  12. Gandin A., Gutjahr S., Dizengremel P. et al.: Source-sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum.–J. Exp. Bot. 62: 3467–3479, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gruber N., Galloway J.N.: An Earth-system perspective of the global nitrogen cycle.–Nature 451: 293–296, 2008.CrossRefPubMedGoogle Scholar
  14. Günthardt-Goerg M.S., Vollenweider P.: Linking stress with macroscopic and microscopic leaf response in trees: new diagnostic perspectives.–Environ. Pollut. 147: 467–488, 2007.CrossRefPubMedGoogle Scholar
  15. Hudson J.M.G., Henry G.H.R.: Increased plant biomass in a High Arctic heath community from 1981 to 2008.–Ecology 90: 2657–2663, 2009.CrossRefPubMedGoogle Scholar
  16. Körner C.: Carbon limitation in trees.–J. Ecol. 91: 4–17, 2003.CrossRefGoogle Scholar
  17. Li J.Y., Dong T.F., Guo Q.X. et al.: Populus deltoides females are more selective in nitrogen assimilation than males under different nitrogen forms supply.–Trees 29: 143–159, 2015.CrossRefGoogle Scholar
  18. Li Y., Zhang X.L., Yang Y.Q. et al.: Soil cadmium toxicity and nitrogen deposition differently affect growth and physiology in Toxicodendron vernicifluum seedlings.–Acta. Physiol. Plant. 35: 529–540, 2013.CrossRefGoogle Scholar
  19. Li Y., Zhao H.X., Duan B.L. et al.: Effect of drought and ABA on growth, photosynthesis and antioxidant system of Cotinus coggygria seedlings under two different light conditions.–Environ. Exp. Bot. 71: 107–113, 2011.CrossRefGoogle Scholar
  20. Lichtenthaler H.K.: Chlorophyll and carotenoids: pigments of photosynthetic biomembranes.–Methods Enzymol. 148: 350–382, 1987.CrossRefGoogle Scholar
  21. Livingston N.J., Guy R.D., Sun Z.J. et al.: The effects of nitrogen stress on the stable carbon isotope composition, productivity and water use efficiency of white spruce (Picea glauca (Moench) Voss) seedlings.–Plant Cell Environ. 22: 281–289, 1999.CrossRefGoogle Scholar
  22. Masia A.: Physiological effects of oxidative stress in relation to ethylene in postharvest produce.–In: Hodges, D.M. (ed.): Post harvest Oxidative Stress in Horticultural Crops. Pp. 165–197. Food Products Press, New York 2003.Google Scholar
  23. Matson P., Lohse K.A., Hall S.J.: The globalization of nitrogen deposition: Consequences for terrestrial ecosystems.–AMBIO 31: 113–119, 2002.CrossRefPubMedGoogle Scholar
  24. Mitchell A.K.: Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade.–Tree Physiol. 18: 749–757, 1998.CrossRefPubMedGoogle Scholar
  25. Murata T.: Enzymic mechanism of starch breakdown in germinating rice seeds I. An analytical study.–Plant Physiol. 43: 1899–1905, 1968.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nakaji T., Fukami M., Dokiya Y. et al.: Effects of high nitrogen load on growth, photosynthesis and nutrient status of Cryptomeria japonica and Pinus densiflora seedlings.–Trees 15: 453–461, 2001.Google Scholar
  27. Naudts K., van den Berge J., Janssens I.A. et al.: Does an extreme drought event alter the response of grassland communities to a changing climate?–Environ. Exp. Bot. 70: 151–157, 2011.CrossRefGoogle Scholar
  28. Naudts K., van den Berge J., Janssens I.A. et al.: Combined effects of warming and elevated CO2 on the impact of drought in grassland species.–Plant Soil. 369: 497–507, 2013.CrossRefGoogle Scholar
  29. Nelson D.W., Sommers L.E.: Total carbon, organic carbon, organic matter.–In: Dinauer R.C. (ed.): Methods of Soil Analysis. Part 2. Pp. 539–579. Am. Soc. Agron., Inc., and Soil Sci. Soc. Am., Inc., Madison 1982.Google Scholar
  30. Ogaya R., Peñuelas J.: Species-specific drought effects on flower and fruit production in a Mediterranean holm oak forest.–Forestry 80: 351–357, 2007.CrossRefGoogle Scholar
  31. Olszyk D.M., Johnson M.G., Tingey D.T. et al.: Whole-seedling biomass allocation, leaf area, and tissue chemistry for Douglasfir exposed to elevated CO2 and temperature for 4 years.–Can. J. Forest Res. 33: 269–278, 2003.CrossRefGoogle Scholar
  32. Porra R.J., Thompson W.A., Kriedemann P.E.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.–BBA-Bioenergetics 975: 384–394, 1989.CrossRefGoogle Scholar
  33. Reich P.B., Walters M.B., Ellsworth D.S., Uhl C.: Photosynthesis- nitrogen relations in Amazonian tree species. I. Patterns among species and communities.–Oecologia 97: 62–72, 1994.CrossRefGoogle Scholar
  34. Sardans J., Peñuelas J., Estiarte M.: Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland.–Plant Soil 289: 227–238, 2006.CrossRefGoogle Scholar
  35. Saxe H., Cannell M.G.R., Johnsen Ø. et al.: Tree and forest functioning in response to global warming.–New Phytol. 149: 369–400, 2001.CrossRefGoogle Scholar
  36. Schreiber U., Schliwa U., Bilger W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.–Photosynth. Res. 10: 51–62, 1986.CrossRefPubMedGoogle Scholar
  37. Shi C.G., Silva L.C.R., Zhang H.X. et al.: Climate warming alters nitrogen dynamics and total non-structural carbohydrate accumulations of perennial herbs of distinctive functional groups during the plant senescence in autumn in an alpine meadow of the Tibetan Plateau, China.–Agr. Forest Meteorol. 200: 21–29, 2015.CrossRefGoogle Scholar
  38. Stefanowska M., Kuras M., Kacperska A.: Low temperatureinduced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L. var. oleifera L.) leaves.–Ann. Bot.-London 90: 637–645, 2002.CrossRefGoogle Scholar
  39. Ti C.P., Yan X.Y.: [Estimation of atmospheric nitrogen wet deposition in China mainland from based on N emission data.]–J. Agroenviron. Sci. 29: 1606–1611, 2010. [In Chinese]Google Scholar
  40. Tripodi A.D., Sievering H.: The photosynthetic response of a high-altitude spruce forest to nitrogen amendments with implications for gross primary productivity.–Tellus B 62: 59–68, 2010.CrossRefGoogle Scholar
  41. Vollenweider P., Cosio C., Günthardt-Goerg M.S. et al.: Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.).–Environ. Exp. Bot. 58: 25–40, 2006.CrossRefGoogle Scholar
  42. Wu Z.L.: [Chinese Fir.] Pp. 583. China For. Press, Beijing 1984. [In Chinese]Google Scholar
  43. Xie H.H., Gong Q.W., Wu C.Z. et al.: [Effects of nitrogen and sulfur deposition on photosynthetic characteristics of Eucalyptus urophylla × Eucalyptus grandis and Cunninghamia lanceolata seedlings under simulated experimental condition.]–J. Appl. Environ. Biol. 21: 555–562, 2015. [In Chinese]Google Scholar
  44. Yao L.H., Kang W.X., Zhao Z.H. et al.: [Carbon fixed characteristics of plant of Chinese fir (Cunninghamia lanceolata) plantation at different growth stages in Huitong.]–Acta Ecol. Sin. 35: 1187–1197, 2015. [In Chinese]Google Scholar
  45. Yemm E.W., Willis A.J.: The estimation of carbohydrates in plant extracts by anthrone.–Biochem. J. 57: 508–514, 1954.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Zhang J.H., Huang W.D., Liu Y.P., Pan Q.H.: Effects of temperature acclimation pretreatment on the ultrastructure of mesophyll cells in young grape plants (Vitis vinifera L. cv. Jingxiu) under cross-temperature stresses.–J. Integr. Plant Biol. 47: 959–970, 2005.CrossRefGoogle Scholar
  47. Zhao H.X., Xu X., Zhang Y.B. et al.: Nitrogen deposition limits photosynthetic response to elevated CO2 differentially in a dioecious species.–Oecologia 165: 41–54, 2011.CrossRefPubMedGoogle Scholar
  48. Zhou G.Y., Yan J.H.: [The influences of regional atmospheric precipitation characteristics and its element inputs on the existence and development of Dinghushan forest ecosystems.]–Acta Ecol. Sin. 21: 2002–2012, 2001. [In Chinese]Google Scholar

Copyright information

© The Institute of Experimental Botany 2016

Authors and Affiliations

  • L. Yu
    • 1
    • 3
  • T. F. Dong
    • 2
  • Y. B. Lu
    • 1
    • 3
  • M. Y. Song
    • 1
    • 3
  • B. L. Duan
    • 1
  1. 1.Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and EnvironmentChinese Academy of SciencesChengduChina
  2. 2.Key Laboratory of Southwest China Wildlife Resources Conservation of Ministry of Education and College of Life Sciences of China West Normal UniversityNanchong, SichuanChina
  3. 3.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations