Skip to main content

Advertisement

Log in

Root nitrogen acquisition strategy of trees and understory species in a subtropical pine plantation in southern China

  • Original Paper
  • Published:
European Journal of Forest Research Aims and scope Submit manuscript

Abstract

Nitrogen (N) is considered as a major factor that limits plant growth and metabolism, and absorptive roots play a critical role in plant resource acquisition. However, little is known about the roles of mycorrhizal colonization, and morphological and architectural traits of absorptive roots in N uptake rates. We examined the uptake rates for ammonium (\({\text{NH}}_{4}^{ + }\)), nitrate (\({\text{NO}}_{3}^{ - }\)) and glycine using a 15N isotope tracer technique and measured mycorrhizal colonization rates and functional traits (morphology, architecture and chemistry) of absorptive roots in a subtropical plantation during the growing season. Results showed that trees, shrubs and herbs all preferred to take up \({\text{NH}}_{4}^{ + }\) over \({\text{NO}}_{3}^{ - }\) and glycine, likely due to the dominant available N form in native soils. Species coexisting in the subtropical plantation did not show chemical niche differentiation, but there was a temporal niche separation in N acquisition across plant species. Absorptive roots with higher mycorrhizal colonization rates exhibited higher N uptake rates than those with lower colonization. In May, morphological traits (diameter and root tissue density) seemed playing important roles in N acquisition on that the absorptive roots with larger diameter and shorter specific root length (SRL) showed higher uptake rates for \({\text{NH}}_{4}^{ + }\), \({\text{NO}}_{3}^{ - }\), and glycine than those with smaller diameter and longer SRL. While in August, the architectural traits of root branching might be essential to enhance nutrient absorption on that the absorptive roots with intensive branching exhibited higher N uptake rates than those with less branching. Our findings suggested that plant species may evolve effective N acquisition strategies integrated mycorrhizal symbiosis, and root morphological and architectural traits over a temporal scale to acclimate to the changing environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arend M, Fromm J (2007) Seasonal change in the drought response of wood cell development in poplar. Tree Physiol 27:985–992

    PubMed  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260

    PubMed  Google Scholar 

  • Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641

    PubMed  Google Scholar 

  • BassiriRad H (2000) Kinetics of nutrient uptake by roots: responses to global change. New Phytol 147:155–169

    CAS  Google Scholar 

  • Bohrer KE, Friese CF, Amon JP (2004) Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats. Mycorrhiza 14:329–337

    PubMed  Google Scholar 

  • Budyko MI (1974) Climate and life. Academic Press, New York

    Google Scholar 

  • Bueno A, Greenfield L, Pristch L, Schmidt S, Simon J (2019) Responses to competition for nitrogen between subtropical native tree seedlings and exotic grasses are species-specific and mediated by soil N availability. Tree Physiol 39:404–416

    CAS  PubMed  Google Scholar 

  • Burton AJ, Pregitzer KS, Hendrick RL (2000) Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia 125:389–399

    CAS  PubMed  Google Scholar 

  • Chen W, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proc Natl Acad Sci USA 113:8741–8746

    CAS  PubMed  Google Scholar 

  • Cheng L, Chen W, Adams TS, Wei X, Li L, McCormack ML, DeForest JL, Koide RT, Eissenstat DM (2016) Mycorrhizal fungi and roots are complementary in foraging within nutrient patches. Ecology 97:2815–2823

    PubMed  Google Scholar 

  • Comas LH, Callahan HS, Midford PE (2014) Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies. Ecol Evol 4:2979–2990

    PubMed  PubMed Central  Google Scholar 

  • Cooper HD, Clarkson DT (1989) Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals - a possible mechanism integrating shoot and root in the regulation of nutrient uptake. J Exp Bot 40:753–762

    CAS  Google Scholar 

  • De Graaff MA, Jastrow JD, Six J, Wullschleger SD (2013) Variation in root architecture among switchgrass cultivars impacts decomposition rates. Soil Biol Biochem 58:198–206

    Google Scholar 

  • de Mesquita CPB, del Río CMM, Suding KN, Schmidt SK (2018) Rapid temporal changes in root colonization by arbuscular mycorrhizal fungi and fine root endophytes, not dark septate endophytes, track plant activity and environment in an alpine ecosystem. Mycorrhiza 28:717–726

    Google Scholar 

  • Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Garnier E (2016) The global spectrum of plant form and function. Nature 529:167–171

    PubMed  Google Scholar 

  • 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 208:114–124

    PubMed  Google Scholar 

  • FAO (2015) Global forest resources assessment 2015, FAO Forestry paper 163, Rome

  • Fitter AH (1991) The ecological significance of root system architecture: An economic approach. Plant root growth: an ecological perspective, 229–243

  • Fox TR (2000) Sustained productivity in intensively managed forest plantations. For Ecol Manag 138:187–202

    Google Scholar 

  • Gallet-Budynek A, Brzostek E, Rodgers VL, Talbot JM, Hyzy S, Finzi AC (2009) Intact amino acid uptake by northern hardwood and conifer trees. Oecologia 160:129–138

    PubMed  Google Scholar 

  • Gessler A, Schneider S, von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H (1998) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–285

    CAS  Google Scholar 

  • Gessler A, Kopriva S, Rennenberg H (2004) Regulation of nitrate uptake at the whole-tree level: interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiol 24:1313–1321

    CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    CAS  PubMed  Google Scholar 

  • Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008a) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683

    PubMed  Google Scholar 

  • Guo D, Mitchell RJ, Withington JM, Fan PP, Hendricks JJ (2008b) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96:737–745

    CAS  Google Scholar 

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    CAS  Google Scholar 

  • Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24

    Google Scholar 

  • Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759

    CAS  PubMed  Google Scholar 

  • Hong J, Ma X, Yan Y, Zhang X, Wang X (2018) Which root traits determine nitrogen uptake by alpine plant species on the Tibetan Plateau? Plant Soil 424:63–72

    CAS  Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EA, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104:8902–8906

    CAS  PubMed  Google Scholar 

  • James JJ, Richards JH (2005) Plant N capture from pulses: effects of pulse size, growth rate, and other soil resources. Oecologia 145:113–122

    CAS  PubMed  Google Scholar 

  • Johansen A, Finlay RD, Olsson PA (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 133:705–712

    CAS  Google Scholar 

  • Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383

    Google Scholar 

  • Kuzyakov Y, Xu XL (2013) Competition and mutualism between roots and rhizosphere microorganisms by nitrogen acquisition and their ecological consequences. New Phytol 198:656–669

    CAS  PubMed  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    PubMed  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    PubMed  Google Scholar 

  • Lee JA, Stewart GR (1978) Ecological aspects of nitrogen assimilation. Adv Bot Res 6:43

    CAS  Google Scholar 

  • Lee MH, Comas LH, Callahan HS (2014) Experimentally reduced root-microbe interactions reveal limited plasticity in functional root traits in Acer and Quercus. Ann Bot 113:513–521

    PubMed  Google Scholar 

  • Li X, Rennenberg H, Simon J (2016) Seasonal variation in n uptake strategies in the understory of a beech-dominated N-limited forest ecosystem depends on N source and species. Tree Physiol 36:589–600

    PubMed  PubMed Central  Google Scholar 

  • Li H, Liu B, McCormack ML, Ma Z, Guo D (2017) Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient. New Phytol 216:1140–1150

    PubMed  Google Scholar 

  • Liu Y, He L, An L, Helgason T, Feng H (2009) Arbuscular mycorrhizal dynamics in a chronosequence of Caragana korshinskii plantations. FEMS Microb Ecol 67:81–92

    CAS  Google Scholar 

  • Liu B, Li H, Zhu B, Koide RT, Eissenstat DM, Guo D (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136

    PubMed  Google Scholar 

  • Liu Q, Qiao N, Xu X, Xin X, Han JY, Tian Y, Ouyang H, Kuzyakov Y (2016) Nitrogen acquisition by plants and microorganisms in a temperate grassland. Sci Rep 6:22642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Li C, Xu X, Wanek W, Jiang N, Wang H, Yang X (2017) Organic and inorganic nitrogen uptake by 21 dominant tree species in temperate and tropical forests. Tree Physiol 37:1515–1526

    CAS  PubMed  Google Scholar 

  • Ma Z, Guo D, Xu X, Lu M, Bardgett RD, Eissenstat DM, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94

    CAS  PubMed  Google Scholar 

  • McCormack ML, Adams TS, Smithwick EA, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235

    PubMed  Google Scholar 

  • McFarland JW, Ruess RW, Kielland K, Pregitzer K, Hendrick R, Allen M (2010) Cross-ecosystem comparisons of in situ plant uptake of amino acid-N and NH4. Ecosystems 13:177–193

    CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    CAS  PubMed  Google Scholar 

  • Meier IC, Leuschner C (2008) Genotypic variation and phenotypic plasticity in the drought response of fine roots of European beech. Tree Physiol 28:297–309

    PubMed  Google Scholar 

  • Miller AE, Bowman WD (2002) Variation in nitrogen-15 natural abundance and nitrogen uptake traits among cooccurring alpine species, do species partition by nitrogen form? Oecologia 130:609–616

    PubMed  Google Scholar 

  • Miransari M (2011) Arbuscular mycorrhizal fungi and nitrogen uptake. Arch Microbiol 193:77–81

    CAS  PubMed  Google Scholar 

  • Montagnoli A, Dumroese RK, Terzaghi M, Onelli E, Scippa GS, Chiatante D (2019) Seasonality of fine root dynamics and activity of root and shoot vascular cambium in a Quercus ilex L. forest (Italy). For Ecol Manag 431:26–34

    Google Scholar 

  • Näsholm T, Sandberg G, Ericsson A (1987) Quantitative analysis of amino acids in conifer tissues by high-performance liquid chromatography and fluorescence detection of their 9-fluorenylmethyl chloroformate derivatives. J Chromatogr A 396:225–236

    Google Scholar 

  • Näsholm T, Ekbladm A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic N. Nature 392:914–916

    Google Scholar 

  • Nilsson LO, Baath E, Falkengren-Grerup U, Wallander H (2007) Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153:375–384

    PubMed  Google Scholar 

  • Nord EA, Lynch JP (2009) Plant phenology: a critical controller of soil resource acquisition. J Exp Bot 60:1927–1937

    CAS  PubMed  Google Scholar 

  • Nordin A, Högberg P, Näsholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132

    PubMed  Google Scholar 

  • Ostonen I, Helmisaari HS, Borken W, Tedersoo L, Kukumägi M, Bahram M, Asi E (2011) Fine root foraging strategies in Norway spruce forests across a European climate gradient. Glob Change Biol 17:3620–3632

    Google Scholar 

  • Pena R, Polle A (2014) Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress. ISME J 8:321–330

    CAS  PubMed  Google Scholar 

  • Persson J, Näsholm T (2001) Amino acid uptake: a widespread ability among boreal forest plants. Ecol Lett 4:434–438

    Google Scholar 

  • Pinno BD, Wilson SD (2013) Fine root response to soil resource heterogeneity differs between grassland and forest. Plant Ecol 214:821–829

    Google Scholar 

  • Polverigiani S, McCormack ML, Mueller CW, Eissenstat DM (2011) Growth and physiology of olive pioneer and fibrous roots exposed to soil moisture deficits. Tree Physiol 31:1228–1237

    CAS  PubMed  Google Scholar 

  • Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309

    Google Scholar 

  • Radville L, McCormack ML, Post E, Eissenstat DM (2016) Root phenology in a changing climate. J Exp Bot 67:3617–3628

    CAS  PubMed  Google Scholar 

  • Richards AE, Forrester DI, Bauhus J, Scherer-Lorenzen M (2010) The influence of mixed tree plantations on the nutrition of individual species: a review. Tree Physiol 30:1192–1208

    PubMed  Google Scholar 

  • Robinson D, Hodge A, Fitter A (2003) Constraints on the form and function of root systems. Root ecology. Springer, Berlin, Heidelberg, pp 1–31

    Google Scholar 

  • Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Stokes A (2016) Root structure–function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210:815–826

    PubMed  Google Scholar 

  • Schimann H, Ponton S, Hättenschwiler S, Ferry B, Lensi R, Domenach AM, Roggy JC (2008) Differing nitrogen use strategies of two tropical rainforest late successional tree species in French Guiana: evidence from 15N natural abundance and microbial activities. Soil Biol Biochem 40:487–494

    CAS  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Google Scholar 

  • Schmid I, Kazda M (2002) Root distribution of Norway spruce in monospecific and mixed stands on different soils. For Ecol Manag 159:37–47

    Google Scholar 

  • Shah F, Nicolás C, Bentzer J, Ellström M, Smits M, Rineau F, Braesel J (2016) Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol 209:1705–1719

    CAS  PubMed  Google Scholar 

  • Simon J, Dannenmann M, Gasche R, Holst J, Mayer H, Papen H, Rennenberg H (2011) Competition for nitrogen between adult European beech and its offspring is reduced by avoidance strategy. For Ecol Manag 262:105–114

    Google Scholar 

  • Smith SE, Read DJ (eds) (2008) Mycorrhizal symbiosis. Academic Press, London

    Google Scholar 

  • Sokolovski SG, Meharg AA, Maathuis FJM (2002) Calluna vulgaris root cells show increased capacity for amino acid uptake when colonized with the mycorrhizal fungus Hymenoscyphus ericae. New Phytol 155:525–530

    Google Scholar 

  • Templer PH, Dawson TE (2004) Nitrogen uptake by four tree species of the Catskill Mountains, New York: implications for forest N dynamics. Plant Soil 262:251–261

    CAS  Google Scholar 

  • Tibbett M, Cairney JWG (2007) The cooler side of mycorrhizas: their occurrence and functioning at low temperatures. Can J Bot 85:51–62

    Google Scholar 

  • Tiedje JM (1982) Denitrification. Methods of soil analysis: part 2 chemical and microbiological properties. American Society of Agronomy, Madison, pp 1011–1026

    Google Scholar 

  • Wang P, Shu M, Mou P, Weiner J (2018) Fine root responses to temporal nutrient heterogeneity and competition in seedlings of two tree species with different rooting strategies. Ecol Evol 8:3367–3375

    PubMed  PubMed Central  Google Scholar 

  • Warren CR (2009) Does nitrogen concentration affect relative uptake rates of nitrate, ammonium, and glycine? J Plant Nutr Soil Sci 172:224–229

    CAS  Google Scholar 

  • Warren CR, Adams PR (2007) Uptake of nitrate, ammonium and glycine by plants of Tasmanian wet eucalypt forests. Tree Physiol 27:413–419

    CAS  PubMed  Google Scholar 

  • Weemstra M, Mommer L, Visser EJ, Ruijven J, Kuyper TW, Mohren GM, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169

    CAS  PubMed  Google Scholar 

  • Wells CE, Glenn DM, Eissenstat DM (2002) Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae). Am J Bot 89:79–87

    PubMed  Google Scholar 

  • Wen XF, Yu GR, Sun XM, Li QK, Liu YF, Zhang LM, Ren CY, Fu YL, Li ZQ (2006) Soil moisture effect on the temperature dependence of ecosystem respiration in a subtropical Pinus plantation of southeastern China. Agric For Meteorol 137:166–175

    Google Scholar 

  • Whiteside MD, Garcia MO, Treseder KK (2012) Amino acid uptake in arbuscular mycorrhizal plants. PLoS ONE 7:e47643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Flexas J (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    CAS  PubMed  Google Scholar 

  • Xu X, Ouyang H, Richter A, Wanek W, Cao G, Kuzyakov Y (2011) Spatio-temporal variations determine plant–microbe competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571

    CAS  Google Scholar 

  • Yang B, Wen X, Sun X (2015) Seasonal variations in depth of water uptake for a subtropical coniferous plantation subjected to drought in an East Asian monsoon region. Agric For Meteorol 201:218–228

    Google Scholar 

  • Zadworny M, McCormack ML, Rawlik K, Jagodziński AM (2015) Seasonal variation in chemistry, but not morphology, in roots of Quercus robur growing in different soil types. Tree Physiol 35:644–652

    CAS  PubMed  Google Scholar 

  • Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat plants 1:15

    Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (31670635, 31730014). We appreciate the two anonymous reviewers for their valuable comments and suggestions on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Huimin Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Agustín Merino.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 675 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Q., Wang, H. & Xu, X. Root nitrogen acquisition strategy of trees and understory species in a subtropical pine plantation in southern China. Eur J Forest Res 139, 791–804 (2020). https://doi.org/10.1007/s10342-020-01284-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10342-020-01284-6

Keywords

Navigation