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Belowground responses of woody plants to nitrogen addition in a phosphorus-rich region of northeast China

  • Jing Guo
  • Yingzhi GaoEmail author
  • David M. Eissenstat
  • Chunguang HeEmail author
  • Lianxi Sheng
Original Article


Key Message

Nitrogen addition leads to large increases in shoot growth but limited increases in root growth and reductions in mycorrhizal colonization of Sorbus pohuashanensis and Acanthopanax sessiliflorus.


Soil in the cultivated fields of Changbai Mountain region of China is rich in phosphorus (P) and deficient in nitrogen (N) for most woody plants. However, currently N deposition is increasing and reducing its limitation on plant growth. How N addition shifts carbon investment among shoots, roots and arbuscular mycorrhizal (AM) fungi is not well understood, especially in woody plants growing in the field. We examine the responses of the growth, biomass partitioning and AM colonization of Sorbus pohuashanensis Hedl. and Acanthopanax sessiliflorus Seem. to low and high N fertilization in northeastern China on high-P soil over 3 years. With N addition, both plants increased shoot biomass by 20–45%, and N and P content by 13–30%, while root biomass increased only by 2.1–5.4%. The slower increase in root growth relative to shoot growth resulted in lower root mass fraction. After plant size (ontogeny) was accounted for, root mass fraction still decreased significantly with high N fertilization in both species. Mycorrhizal colonization intensity and AM-colonized root length decreased with an increase in N addition. In this P-rich site, the limited increase in root biomass and large decrease in AM colonization with N addition presumably promoted plant growth and nutrient uptake. Our results imply that the growth of these two species may be improved by increased carbon allocation to shoots, as N addition permitted sufficient nutrient uptake by roots and AM fungi to meet shoot nutrient demand without additional belowground carbon expenditure.


Arbuscular mycorrhiza Biomass partitioning Carbon investment Sorbus pohuashanensis Acanthopanax sessiliflorus 



This work was financially supported by the National Key Basic Research Program of China (2016YFC0500703, 2016YFC0500407), the National Natural Science Foundation of China (31670446, 31270444) and Human Resources and Social Security Department of Jilin Province (2016-28). We thank anonymous reviewers and editor for their comments and suggestions.

Author contribution statement

JG, YG and CH designed the experiment and performed the study. CH and LS helped to establish and maintain the experimental plots. JG analyzed the data and drafted the first version of the manuscript. JG, YG and DME helped with manuscript revisions. All authors read and approved the final version of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

468_2019_1906_MOESM1_ESM.docx (286 kb)
Table S1 Results of repeated measures ANOVA on plant growth, biomass partitioning, plant nutrient content, root length and mycorrhizal colonization traits, with species and fertilization treatment as independent variable, and years as the repeated measure. Table S2 Plant height, nutrient content, N:P ratio, root length and AM colonization (means±SE, n = 4) of two woody plants Sorbus pohuashanensis (Sopo) and Acanthopanax sessiliflorus (Acse) over three years. Differences among three fertilization treatments for each plant traits were analyzed by years. Different letters represent statistical significance (P < 0.05) among treatments. Treatments are: C, control (no additional N addition); L, low nitrogen fertilization (5 g m-2 yr-1); H, high nitrogen fertilization (15 g m-2 yr-1). Table S3 Linear regression between leaf, stem or root mass fraction (dependent variable, y axis, g g-1) and total biomass (independent variable, x axis, kg) of Sorbus pohuashanensis and Acanthopanax sessiliflorus. Treatments are: C, control (no additional N addition); L, low nitrogen fertilization (5 g m-2 yr-1); H, high nitrogen fertilization (15 g m-2 yr-1). Table S4 Analysis of covariance on biomass partitioning of Sorbus pohuashanensis and Acanthopanax sessiliflorus, with leaf, stem or root mass fraction as independent variable individually, control (no additional nitrogen addition) and low or high nitrogen fertilization treatment (NF) as fixed factor, and total biomass (TB) as covariate. Treatments are: C, control (no additional N addition); L, low nitrogen fertilization (5 g m-2 yr-1); H, high nitrogen fertilization (15 g m-2 yr-1). Table S5 Results of repeated measures ANOVA on the traits of absorptive root and mycorrhizal colonization for two woody seedlings, with species and fertilization treatment as independent variable, and years as the repeated measure. All these parameters were measured based on both unfertilized and fertilized plots in 2016 and 2017. Table S6 Traits of absorptive roots and of mycorrhizal colonization (means±SE, n = 8) for two woody seedlings. All parameters are based on both unfertilized and fertilized plots in 2016 and 2017. Table S7 Plant type, soil fertility, N addition amount, and shift in plant P demand, root amount, root fraction and AM colonization after N addition in previous studies. Fig. S1 Location of the study area in Jilin Longwan National Nature Reserve, Jinchuan town, northeastern China. Fig. S2 Pictures of Sorbus pohuashanensis and Acanthopanax sessiliflorus (DOCX 286 kb)


  1. Agüero ML, Puntieri J, Mazzarino MJ, Grosfeld J, Barroetaveña C (2014) Seedling response of Nothofagus species to N and P: linking plant architecture to N/P ratio and resorption proficiency. Trees 28:1185–1195CrossRefGoogle Scholar
  2. Axelsson E, Axelsson B (1986) Changes in carbon allocation patterns in spruce and pine trees following irrigation and fertilization. Tree Physiol 2:189–204CrossRefGoogle Scholar
  3. Ballhausen MB, de Boer W (2016) The sapro-rhizosphere: carbon flow from saprotrophic fungi into fungus-feeding bacteria. Soil Biol Biochem 102:14–17CrossRefGoogle Scholar
  4. Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn AJ, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992CrossRefGoogle Scholar
  5. Blanke V, Wagner M, Renker C, Lippert H, Michulitz M, Kuhn AJ, Buscot F (2011) Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343:379–392CrossRefGoogle Scholar
  6. Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants: an economic analogy. Annu Rev Ecol Syst 16:363–392CrossRefGoogle Scholar
  7. Bown HE, Watt MS, Clinton PW, Mason EG (2010) Influence of ammonium and nitrate supply on growth, dry matter partitioning, N uptake and photosynthetic capacity of Pinus radiata seedlings. Trees 24:1097–1107CrossRefGoogle Scholar
  8. Bremner JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. American Society of Agronomy, Madison, pp 595–608Google Scholar
  9. Brouwer R (1983) Functional equilibrium: sense or nonsense? Neth J Agric Sci 31:335–348Google Scholar
  10. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. ACIAR monograph. ACIAR, CanberraGoogle Scholar
  11. Carrara JE, Walter CA, Hawkins JS, Peterjoohn WT, Averill C, Brzostek ER (2018) Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization. Glob Change Biol 24:2721–2734CrossRefGoogle Scholar
  12. Cowden CC, Peterson CJ (2009) A multi-mutualist simulation: applying biological market models to diverse mycorrhizal communities. Ecol Model 220:1522–1533CrossRefGoogle Scholar
  13. Coyle DR, Aubrey DP, Coleman MD (2016) Growth responses of narrow or broad site adapted tree species to a range of resource availability treatments after a full harvest rotation. For Ecol Manage 362:107–119CrossRefGoogle Scholar
  14. Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60CrossRefGoogle Scholar
  15. Eissenstat DM, Graham JH, Syvertsen JP, Drouillard DL (1993) Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Ann Bot 71:1–10CrossRefGoogle Scholar
  16. Eissenstat DM, Kucharski JM, Zadworny M, Adams TS, Koide RT (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol 208:114–124CrossRefGoogle Scholar
  17. Freschet GT, Swart EM, Cornelissen JHC (2015) Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytol 206:1247–1260CrossRefGoogle Scholar
  18. Gradowski T, Thomas SC (2006) Phosphorus limitation of sugar maple growth in central Ontario. For Ecol Manage 226:104–109CrossRefGoogle Scholar
  19. Graham JH, Syvertsen JP (1985) Host determinants of mycorrhizal dependency of citrus rootstock seedlings. New Phytol 101:667–676CrossRefGoogle Scholar
  20. Grechi I, Vivin Ph, Hilbert G, Milin S, Robert T, Gaudillère J-P (2007) Effect of light and nitrogen supply on internal C:N balance and control of root-to-shoot biomass allocation in grapevine. Environ Exp Bot 59:139–149CrossRefGoogle Scholar
  21. Grman E (2012) Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711–718CrossRefGoogle Scholar
  22. Grman E, Robinson TMP (2013) Resource availability and imbalance affect plant–mycorrhizal interactions: a field test of three hypotheses. Ecology 94:62–71CrossRefGoogle Scholar
  23. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  24. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Ecol Evol Syst 5:37–61CrossRefGoogle Scholar
  25. Hasselquist NJH, Metcalfe DB, Inselsbacher E, Stangl Z, Oren R, Näsholm T, Högberg P (2016) Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecology 97:1012–1022Google Scholar
  26. Heggenstaller AH, Moore KJ, Liebman M, Anex RP (2009) Nitrogen influences biomass and nutrient partitioning by perennial, warm-season grasses. Agron J 101:1363–1371CrossRefGoogle Scholar
  27. Hertel D, Strecker T, Müller-Haubold H, Christoph Leuschner (2013) Fine root biomass and dynamics in beech forests across a precipitation gradient—is optimal resource partitioning theory applicable to water-limited mature trees? J Ecol 101:1183–1200CrossRefGoogle Scholar
  28. Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–569CrossRefGoogle Scholar
  29. Ingestad T, Ågren GI (1991) The influence of plant nutrition on biomass allocation. Ecol Appl 1:168–174CrossRefGoogle Scholar
  30. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647CrossRefGoogle Scholar
  31. Kobiela B, Biondini M, Sedivec K (2016) Comparing root and shoot responses to nutrient additions and mowing in a restored semi-arid grassland. Plant Ecol 217:303–314CrossRefGoogle Scholar
  32. Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:365–386CrossRefGoogle Scholar
  33. Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53:773–787CrossRefGoogle Scholar
  34. Li W, Jin C, Guan D, Wang Q, Wang A, Yuan F, Wu J (2015) The effects of simulated nitrogen deposition on plant root traits: a meta-analysis. Soil Biol Biochem 82:112–118CrossRefGoogle Scholar
  35. Liu B, Li H, Zhu B, Eissenstat DM, Guo D (2015) Complementarity of absorptive fine roots and arbuscular mycorrhizal fungi in nutrient foraging strategies across 14 coexisting subtropical tree species. New Phytol 208:125–136CrossRefGoogle Scholar
  36. MacLean AM, Bravo A, Harrison MJ (2017) Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. Plant Cell 29:2319–2335CrossRefGoogle Scholar
  37. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  38. McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593CrossRefGoogle Scholar
  39. Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147:131–139CrossRefGoogle Scholar
  40. Ostertag R (2001) Effects of nitrogen and phosphorus availability on fine-root dynamics in Hawaiian montane forests. Ecology 82:485–499CrossRefGoogle Scholar
  41. Ouimette A (2017) Patterns and drivers of carbon fluxes in temperate forests. Dissertation, University of New HampshireGoogle Scholar
  42. Ploschuk EL, Slafer GA, Ravetta DA (2005) Reproductive allocation of biomass and nitrogen in annual and perennial Lesquerella crops. Ann Bot 96:127–135CrossRefGoogle Scholar
  43. Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607Google Scholar
  44. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50CrossRefGoogle Scholar
  45. Reich P (2002) Root–shoot relations: optimality in acclimation and adaptation or the ‘‘Emperor’s New Clothes’’? In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 205–220CrossRefGoogle Scholar
  46. Roberts TL, Ross WJ, Norman RJ, Slaton NA, Wilson CE Jr (2011) Predicting nitrogen fertilizer needs for rice in Arkansas using alkaline hydrolyzable-nitrogen. Soil Sci Soc Am J 75:1161–1171CrossRefGoogle Scholar
  47. Ryser P, Lambers H (1995) Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant Soil 170:251–265CrossRefGoogle Scholar
  48. Rytter R-M (2013) The effect of limited availability of N or water on C allocation to fine roots and annual fine root turnover in Alnus incana and Salix viminalis. Tree Physiol 33:924–939CrossRefGoogle Scholar
  49. Schortemeyer M, Atkin OK, McFarlane N, Evans JR (1999) The impact of elevated atmospheric CO2 and nitrate supply on growth, biomass allocation, nitrogen partitioning and N2 fixation of Acacia melanoxylon. Aust J Plant Physiol 26:737–747Google Scholar
  50. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  51. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbiosis. New Phytol 182:347–358CrossRefGoogle Scholar
  52. Sugiura D, Tateno M (2011) Optimal leaf-to-root ratio and leaf nitrogen content determined by light and nitrogen availabilities. PLoS One 6:e22236CrossRefGoogle Scholar
  53. Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytol 167:493–508CrossRefGoogle Scholar
  54. Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954CrossRefGoogle Scholar
  55. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221Google Scholar
  56. Trubat R, Cortina J, Vilagrosa A (2012) Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings. Oecologia 170:899–908CrossRefGoogle Scholar
  57. Uchinomiya K, Iwasa Y (2014) Optimum resource allocation in the plant–fungus symbiosis for an exponentially growing system. Evol Ecol Res 16:363–372Google Scholar
  58. van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM (2007) Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytol 176:175–183CrossRefGoogle Scholar
  59. van Diepen LTA, Entwistle EM, Zak DR (2013) Chronic nitrogen deposition and the composition of active arbuscular mycorrhizal fungi. Appl Soil Ecol 72:62–68CrossRefGoogle Scholar
  60. Vogt KA, Grier CC, Meier CE, Edmonds RL (1982) Mycorrhizal role in net primary production and nutrient cycling in Abies amabilis ecosystems in western Washington. Ecology 63:370–380CrossRefGoogle Scholar
  61. Wang G, Fahey TJ, Xue S, Liu F (2013) Root morphology and architecture respond to N addition in Pinus tabuliformis, west China. Oecologia 171:583–590CrossRefGoogle Scholar
  62. Wang Y, Meng B, Zhong S, Wang D, Ma J, Sun W (2018) Aboveground biomass and root/shoot ratio regulated drought susceptibility of ecosystem carbon exchange in a meadow. Plant Soil 432:259–272CrossRefGoogle Scholar
  63. Wurzburger N, Wright SJ (2015) Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96:2137–2146CrossRefGoogle Scholar
  64. Zhang L, Bai Y, Han X (2004) Differential responses of N:P stoichiometry of Leymus chinensis and Carex korshinskyi to N additions in a steppe ecosystem in Nei Mongol. Acta Bot Sinica 46:259–270Google Scholar
  65. Zhang N, Guo R, Song P, Guo J, Gao Y (2013) Effects of warming and nitrogen deposition on the coupling mechanism between soil nitrogen and phosphorus in Songnen Meadow Steppe, northeastern China. Soil Biol Biochem 65:96–104CrossRefGoogle Scholar
  66. Zheng Z, Ma P, Li J, Ren L, Bai W, Tian Q, Sun W, Zhang WH (2018) Arbuscular mycorrhizal fungal communities associated with two dominant species differ in their responses to long-term nitrogen addition in temperate grasslands. Funct Ecol 32:1575–1588CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Vegetation Ecology, Institute of Grassland ScienceNortheast Normal UniversityChangchunChina
  2. 2.State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation RestorationNortheast Normal UniversityChangchunChina
  3. 3.Department of Ecosystem Science and ManagementThe Pennsylvania State UniversityUniversity ParkUSA

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