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Seasonal variations in plant nitrogen acquisition in an ectomycorrhizal alpine forest on the eastern Tibetan Plateau, China

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Abstract

Background and aims

Plant nitrogen (N) acquisition plays an important role in regulating plant growth and ecosystem functions. However, the seasonal variations in the relative contributions of different N sources to plant N uptake and how plants modify their N absorption preferences, especially in ectomycorrhizal forests, are not well understood.

Methods

We used the in situ 15N-labeling method to quantitatively estimate the relative uptake contributions of plants for three different soil N sources (nitrate, ammonium and amino acids) and plant N acquisition preferences in an ectomycorrhizal alpine forest (a 70-year-old spruce plantation on the eastern Tibetan Plateau, China) during the growing season and the nongrowing season.

Results

Across the two seasons, plants in the spruce plantation showed a greater preference for acquiring soil NH4+-N, with soil NH4+ contributing more than 50% to the total N uptake of plants (57.88% during the growing season and 52.72% during the non-growing season). Moreover, amino acids exhibited a considerable contribution to the total plant N uptake, and their contribution was significantly higher during the non-growing season (33.47%) than that during the growing season (9.86%). Accordingly, plants showed a greater preference for taking up amino acids over NO3− -N in the soil as the season changed from the growing season to the non-growing season.

Conclusions

Collectively, our data demonstrate that soil inorganic N is the predominant N source for plants in alpine forests, irrespective of seasonal variations. However, soil amino acids could also be an important supplementary N source for the plant N economy, especially during the non-growing season, when inorganic N availability is constrained. Our findings also suggest that plants in ectomycorrhizal alpine forests modify their nutrient absorption preference in response to seasonal changes.

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References

  • Andersson P, Berggren D (2005) Amino acids, total organic and inorganic nitrogen in forest floor soil solution at low and high nitrogen input. Water Air Soil Pollut 162(1–4):369–384

    CAS  Google Scholar 

  • Andresen LC, Michelsen A (2005) Off-season uptake of nitrogen in temperate heath vegetation. Oecologia 144(4):585–597

    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(11):3252–3260

    PubMed  Google Scholar 

  • Averill C, Finzi A (2011) Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δ15N. Ecology 92(4):883–891

    PubMed  Google Scholar 

  • Bennett JN, Prescott CF (2004) Organic and inorganic nitrogen nutrition of western red cedar, western hemlock and salal in mineral N-limited cedar-hemlock forests. Oecologia 141(3):468–476

    PubMed  Google Scholar 

  • Berthrong ST, Finzi AC (2006) Amino acid cycling in three cold-temperate forests of the northeastern Usa. Soil Biol Biochem 38(5):861–869

    CAS  Google Scholar 

  • Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiol 99:1294–1301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159(6):567–584

    CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2013) Ecological significance and complexity of N-source preference in plants. Ann Bot 112(6):957–963

    CAS  PubMed  PubMed Central  Google Scholar 

  • Broughton RCI, Newsham KK, Hill PW, Stott A, Jones DL (2015) Differential acquisition of amino acid and peptide enantiomers within the soil microbial community and its implications for carbon and nitrogen cycling in soil. Soil Biol Biochem 88:83–89

    CAS  Google Scholar 

  • Courty PE, Buée M, Diedhiou AG, Frey-Klett P, le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42(5):679–698

    CAS  Google Scholar 

  • Craine JM, Elmore AJ, Aidar MP et al (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183(4):980–992

    CAS  PubMed  Google Scholar 

  • D'Elia CF, Deboer JA (1978) Nutritional studies of two red algae. Ii. Kinetics of ammonium and nitrate uptake. J Phycol 14(3):266–272

    CAS  Google Scholar 

  • Dijkstra FA, Carrillo Y, Pendall E et al (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4(1):216–216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dunn RM, Mikola J, Bol R, Bardgett RD (2006) Influence of microbial activity on plant–microbial competition for organic and inorganic nitrogen. Plant Soil 289(1–2):321–334

    CAS  Google Scholar 

  • Farrell M, Hill PW, Farrar J, Bardgett RD, Jones DL (2011) Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient. Soil Biol Biochem 43(4):835–844

    CAS  Google Scholar 

  • Finzi AC, Berthrong ST (2005) The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86(12):3345–3353

    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(1):129–138

    PubMed  Google Scholar 

  • Gillespie AR (1989) Modelling nutrient flux and interspecies root competition in agroforestry interplantings. Agrofor Syst 8(3):257–265

    Google Scholar 

  • Grogan P, Michelsen A, Ambus P, Jonasson S (2004) Freeze–thaw regime effects on carbon and nitrogen dynamics in sub-arctic heath tundra mesocosms. Soil Biol Biochem 36(4):641–654

    CAS  Google Scholar 

  • Hildebrandt TM, Nunes Nesi A, Araujo WL et al (2015) Amino acid catabolism in plants. Mol Plant 8(11):1563–1579

    CAS  PubMed  Google Scholar 

  • Hofmockel KS, Schlesinger WH, Jackson RB (2007) Effects of elevated atmospheric carbon dioxide on amino acid and NH4+-N cycling in a temperate pine ecosystem. Glob Chang Biol 13(9):1950–1959

    Google Scholar 

  • Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Näsholm T, Högberg P (2010) Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytol 187(2):485–493

    PubMed  Google Scholar 

  • Hooper D, Coughlan J, Mullen M (2008) Structural equation modelling: guidelines for determining model fit. Electron J Bus Res Methods 6:53–60

    Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EA et al (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci 104(21):8902–8906

    CAS  PubMed  Google Scholar 

  • Imai R, Yoshida M, Matsumoto N (2013) Plant and microbe adaptations to cold in a changing world: proceedings from plant and microbe adaptations to cold 2012. Springer Science & Business Media

  • Joergensen RG, Mueller T, Wolters V (1996) Total carbohydrates of the soil microbial biomass in 0.5 M K2SO4 soil extracts. Soil Biol Biochem 28(9):1147–1153

    CAS  Google Scholar 

  • Jones D, Hodge A (1999) Biodegradation kinetics and sorption reactions of three differently charged amino acids in soil and their effects on plant organic nitrogen availability. Soil Biol Biochem 31(9):1331–1342

    CAS  Google Scholar 

  • Jones DL, Owen AG, Farrar JF (2002) Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem 34(12):1893–1902

    CAS  Google Scholar 

  • Kahmen A, Livesley SJ, Arndt SK (2009) High potential, but low actual, glycine uptake of dominant plant species in three Australian land-use types with intermediate N availability. Plant Soil 325(1–2):109–121

    CAS  Google Scholar 

  • Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75(8):2373–2383

    Google Scholar 

  • Kielland K, McFarland J, Olson K (2006) Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288(1–2):297–307

    CAS  Google Scholar 

  • Kieloaho AJ, Pihlatie M, Carrasco MD et al (2016) Stimulation of soil organic nitrogen pool: the effect of plant and soil organic matter degrading enzymes. Soil Biol Biochem 96:97–106

    CAS  Google Scholar 

  • Li YJ, Sun DD, Li DD, Xu Z, Zhao C, Lin H, Liu Q (2015) Effects of warming on ectomycorrhizal colonization and nitrogen nutrition of Picea asperata seedlings grown in two contrasting forest ecosystems. Sci Rep 5(1):17546–17546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liese R, Lubbe T, Albers NW et al (2018) The mycorrhizal type governs root exudation and nitrogen uptake of temperate tree species. Tree Physiol 38(1):83–95

    CAS  PubMed  Google Scholar 

  • Liu XY, Koba K, Makabe A, Li XD, Yoh M, Liu CQ (2013) Ammonium first: natural mosses prefer atmospheric ammonium but vary utilization of dissolved organic nitrogen depending on habitat and nitrogen deposition. New Phytol 199(2):407–419

    CAS  PubMed  Google Scholar 

  • Makarov MI (2019) The role of mycorrhiza in transformation of nitrogen compounds in soil and nitrogen nutrition of plants: a review. Eurasian Soil Sci 52(2):193–205

    CAS  Google Scholar 

  • Mcfarland JW, Ruess RW, Kielland K et al (2010a) Glycine mineralization in situ closely correlates with soil carbon availability across six north American forest ecosystems. Biogeochemistry 99(1–3):175–191

    CAS  Google Scholar 

  • Mcfarland JW, Ruess RW, Kielland K et al (2010b) Cross-ecosystem comparisons of in situ plant uptake of amino acid-N and NH4+. Ecosystems 13:177–193

    CAS  Google Scholar 

  • Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128

    CAS  Google Scholar 

  • Moore TR, Alfonso A, Clarkson BR (2018) Plant uptake of organic nitrogen in two peatlands. Plant Soil 433(1–2):391–400

    CAS  Google Scholar 

  • Munzarova E, Lorenzen B, Brix H, Vojtiskova L, Votrubova O (2006) Effect of NH4+/NO3− availability on nitrate reductase activity and nitrogen accumulation in wetland helophytes Phragmites australis and Glyceria maxima. Environ Exp Bot 55(1–2):49–60

    CAS  Google Scholar 

  • Näsholm T, Persson J (2001) Plant acquisition of organic nitrogen in boreal forests. Physiol Plant 111(4):419–426

    PubMed  Google Scholar 

  • Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392(6679):914–916

    Google Scholar 

  • Näsholm T, Huss-Danell K, Högberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81(4):1155–1161

    Google Scholar 

  • Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytologist 182(1):31–48

  • Neff JC, Chapin Iii FS, Vitousek PM (2003) Breaks in the cycle: dissolved organic nitrogen in terrestrial ecosystems. Front Ecol Environ 1(4):205–211

    Google Scholar 

  • Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manag 260(10):1623–1639

    Google Scholar 

  • Nilsson LO, Giesler R, Bååth E, Wallander H (2005) Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phytol 165(2):613–622

    PubMed  Google Scholar 

  • Nordin A, Schmidt IK, Shaver GR (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85(4):955–962

    Google Scholar 

  • Persson J, Gardeström P, Näsholm T (2006) Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. J Exp Bot 57(11):2651–2659

    CAS  PubMed  Google Scholar 

  • Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199(1):41–51

    CAS  PubMed  Google Scholar 

  • Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe soil interactions as drivers of plant community structure and dynamics. Ecology 84(9):2281–2291

    Google Scholar 

  • Riley WJ, Zhu Q, Tang J (2018) Weaker land–climate feedbacks from nutrient uptake during photosynthesis-inactive periods. Nat Clim Chang 8(11):1002–1006

    CAS  Google Scholar 

  • Rothstein DE (2014) In-situ root uptake and soil transformations of glycine, glutamine and ammonium in two temperate deciduous forests of contrasting N availability. Soil Biol Biochem 75:233–236

    CAS  Google Scholar 

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

    Google Scholar 

  • Schimel JP, Chapin FS (1996) Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants complete well for amino acid N. Ecology 77(7):2142–2147

    Google Scholar 

  • Schimel JP, Jackson LE, Firestone MK (1989) Spatial and temporal effects on plant-microbial competition for inorganic nitrogen in a California annual grassland. Soil Biol Biochem 21(8):1059–1066

    CAS  Google Scholar 

  • Schwarz PA, Fahey TJ, Dawson TE (1997) Seasonal air and soil temperature effects on photosynthesis in red spruce (picea rubens) saplings. Tree Physiol 3:187–194

    Google Scholar 

  • Setién I, Fuertes-Mendizabal T, González A, Aparicio-Tejo PM, González-Murua C, González-Moro MB, Estavillo JM (2013) High irradiance improves ammonium tolerance in wheat plants by increasing N assimilation. J Plant Physiol 170(8):758–771

    PubMed  Google Scholar 

  • Song FQ, Tian XJ, Yang CL et al (2006) Ectomycorrhizal infection intensity of subalpine forest ecosystems in western Sichuan, China. Acta Ecol Sin 26(12):4171–4178

    CAS  Google Scholar 

  • Song MH, Zheng LL, Suding KN, Yin TF, Yu FH (2015) Plasticity in nitrogen form uptake and preference in response to long-term nitrogen fertilization. Plant Soil 394(1–2):215–224

    CAS  Google Scholar 

  • Starr G, Oberbauer SF (2003) Photosynthesis of arctic evergreens under snow: implications for tundra ecosystem carbon balance. Ecology 84(6):1415–1420

    Google Scholar 

  • Templer P, Dawson T (2004) Nitrogen uptake by four tree species of the Catskill Mountains, New York: implications for forest N dynamics. Plant Soil 262(1–2):251–261

    CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707

    CAS  Google Scholar 

  • Wang L, Macko SA (2011) Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell Environ 34(3):525–534

    CAS  PubMed  Google Scholar 

  • Wang XL, Ye J, Gonzalez Perez P et al (2013) The impact of organic farming on the soluble organic nitrogen pool in horticultural soil under open field and greenhouse conditions: a case study. Soil Sci Plant Nutr 59(2):237–248

    CAS  Google Scholar 

  • Warren C, Adams P (2007) Uptake of nitrate, ammonium and glycine by plants of Tasmanian wet eucalypt forests. Tree Physiol 27(3):413–419

    CAS  PubMed  Google Scholar 

  • Warren CR, Taranto MT (2010) Temporal variation in pools of amino acids, inorganic and microbial N in a temperate grassland soil. Soil Biol Biochem 42(2):353–359

    CAS  Google Scholar 

  • Wei L, Chen C, Yu S (2014) Uptake of organic nitrogen and preference for inorganic nitrogen by two Australian native Araucariaceae species. Plant Ecol Divers 8(2):259–264

    Google Scholar 

  • Weih M (2000) Growth of mountain birch seedlings in early-successional patches: a year-round perspective. Plant Biol 2(4):428–436

    Google Scholar 

  • Xu XL, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant Soil 285(1–2):221–231

    CAS  Google Scholar 

  • Xu ZF, Hu R, Xiong P, Wan C, Cao G, Liu Q (2010) Initial soil responses to experimental warming in two contrasting forest ecosystems, eastern Tibetan plateau, China: nutrient availabilities, microbial properties and enzyme activities. Appl Soil Ecol 46(2):291–299

    Google Scholar 

  • Yu Z, Zhang Q, Kraus TEC, Dahlgren RA, Anastasio C, Zasoski RJ (2002) Contribution of amino compounds to dissolved organic nitrogen in forest soils. Biogeochemistry 61(2):173–198

    CAS  Google Scholar 

  • Zhang Z, Yuan Y, Zhao W, He H, Li D, He W, Liu Q, Yin H (2017) Seasonal variations in the soil amino acid pool and flux following the conversion of a natural forest to a pine plantation on the eastern Tibetan plateau, China. Soil Biol Biochem 105:1–11

    CAS  Google Scholar 

  • Zhang Z, Li N, Xiao J, Zhao C, Zou T, Li D, Liu Q, Yin H (2018) Changes in plant nitrogen acquisition strategies during the restoration of spruce plantations on the eastern Tibetan plateau, China. Soil Biol Biochem 119:50–58

    CAS  Google Scholar 

  • Zhang Z, Yuan Y, Liu Q, Yin H (2019) Plant nitrogen acquisition from inorganic and organic sources via root and mycelia pathways in ectomycorrhizal alpine forests. Soil Biol Biochem 136:107517

    CAS  Google Scholar 

  • Zhu F, Dai L, Hobbie EA, Koba K, Liu X, Gurmesa GA, Huang S, Li S, Li Y, Han S, Fang Y (2019) Uptake patterns of glycine, ammonium, and nitrate differ among four common tree species of Northeast China. Front Plant Sci 10:799

    PubMed  PubMed Central  Google Scholar 

  • Zou T, Zhang Z, Li N et al (2017) Differential uptakes of different forms of soil nitrogen among major tree species in subalpine coniferous forests of western Sichuan, China. Chin J Plant Ecol 41(10):1051–1059

    Google Scholar 

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Acknowledgements

This study was supported jointly by the Second Tibetan Plateau Scientific Expedition and Research program (STEP; 2019QZKK0301), the Frontier Science Key Research Programs of CAS (QYZDB-SSW-SMC023) and the National Natural Science Foundation of China (No. 31872700, 31670449, and 31700387). We also thank Yuanshuang Yuan, Zheng Jiang and Duoduo Zhou for their help in the field experiment.

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  1. Wanji Guo and Ziliang Zhang contributed equally to this work.

Authors and Affiliations

  1. CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, China

    Wanji Guo, Ziliang Zhang, Qing Liu & Huajun Yin

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Wanji Guo

  3. Department of Plant & Environmental Sciences, Clemson University, Clemson, SC, 29631, USA

    Ziliang Zhang

  4. College of Environmental Science and Engineering, China West Normal University, Nanchong, 637000, China

    Juan Xiao & Huajun Yin

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  1. Wanji Guo
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  2. Ziliang Zhang
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  3. Qing Liu
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  4. Juan Xiao
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Correspondence to Juan Xiao or Huajun Yin.

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Guo, W., Zhang, Z., Liu, Q. et al. Seasonal variations in plant nitrogen acquisition in an ectomycorrhizal alpine forest on the eastern Tibetan Plateau, China. Plant Soil 459, 79–91 (2021). https://doi.org/10.1007/s11104-020-04644-8

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