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Forest Ecosystems 2022, 9(6): 100071 https://doi.org/10.1016/j.fecs.2022.100071
Research Article | Open Access | Issue | Published: 03 November 2022

How do nitrogen-limited alpine coniferous forests acquire nitrogen? A rhizosphere perspective

Show Author's Information Huajun Yina,b,  Bartosz Adamczykc,  Qitong Wanga,  Biao Zhud,  Wanji Guoa,  Xiaomin Zhua,  Qing Liua,  Ziliang Zhanga,e,*( )
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
China-Croatia "Belt and Road" Joint Laboratory on Biodiversity and Ecosystem Services, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, China
Natural Resources Institute Finland, PL 2, 00791, Helsinki, Finland
Institute of Ecology, College of Urban and Environmental Sciences, and Key Laboratory for Earth Surface Processes of the Ministry of Education, Peking University, Beijing, 100871, China
Institute for Sustainability, Energy, and Environment, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

* Corresponding author. 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.

Keywords:
Rhizosphere, Plant nitrogen acquisition, Root-soil interaction, Alpine coniferous forests, Nitrogen limitation
Cite this article:
Yin H, Adamczyk B, Wang Q, et al. How do nitrogen-limited alpine coniferous forests acquire nitrogen? A rhizosphere perspective. Forest Ecosystems, 2022, 9(6): 100071. https://doi.org/10.1016/j.fecs.2022.100071
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Abstract Full text About this article
Background

Alpine coniferous forest ecosystems dominated by ectomycorrhizal (ECM) tree species are generally characterized by low soil nitrogen (N) availability but stabilized plant productivity. Thus, elucidating potential mechanisms by which plants maintain efficient N acquisition is crucial for formulating optimized management practices in these ecosystems.

Methods

We summarize empirical studies conducted at a long-term field monitoring station in the alpine coniferous forests on the eastern Tibetan Plateau, China. We propose a root-soil interaction-based framework encompassing key components including soil N supply, microbial N transformation, and root N uptake in the rhizosphere.

Results

We highlight that, (ⅰ) a considerable size of soil dissolved organic N pool mitigates plant dependence on inorganic N supply; (ⅱ) ectomycorrhizal roots regulate soil N transformations through both rhizosphere and hyphosphere effects, providing a driving force for scavenging soil N; (ⅲ) a complementary pattern of plant uptake of different soil N forms via root- and mycorrhizal mycelium-pathways enables efficient N acquisitions in response to changing soil N availability.

Conclusions

Multiple rhizosphere processes abovementioned collaboratively contribute to efficient plant N acquisition in alpine coniferous forests. Finally, we identify several research outlooks and directions to improve the understanding and prediction of ecosystem functions in alpine coniferous forests under on-going global changes.


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Abstract
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About this article

How do nitrogen-limited alpine coniferous forests acquire nitrogen? A rhizosphere perspective

Show Author's information Huajun Yina,b, Bartosz Adamczykc, Qitong Wanga, Biao Zhud, Wanji Guoa, Xiaomin Zhua, Qing Liua, Ziliang Zhanga,e,*( )
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
China-Croatia "Belt and Road" Joint Laboratory on Biodiversity and Ecosystem Services, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, China
Natural Resources Institute Finland, PL 2, 00791, Helsinki, Finland
Institute of Ecology, College of Urban and Environmental Sciences, and Key Laboratory for Earth Surface Processes of the Ministry of Education, Peking University, Beijing, 100871, China
Institute for Sustainability, Energy, and Environment, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

* Corresponding author. 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.

Abstract

Background

Alpine coniferous forest ecosystems dominated by ectomycorrhizal (ECM) tree species are generally characterized by low soil nitrogen (N) availability but stabilized plant productivity. Thus, elucidating potential mechanisms by which plants maintain efficient N acquisition is crucial for formulating optimized management practices in these ecosystems.

Methods

We summarize empirical studies conducted at a long-term field monitoring station in the alpine coniferous forests on the eastern Tibetan Plateau, China. We propose a root-soil interaction-based framework encompassing key components including soil N supply, microbial N transformation, and root N uptake in the rhizosphere.

Results

We highlight that, (ⅰ) a considerable size of soil dissolved organic N pool mitigates plant dependence on inorganic N supply; (ⅱ) ectomycorrhizal roots regulate soil N transformations through both rhizosphere and hyphosphere effects, providing a driving force for scavenging soil N; (ⅲ) a complementary pattern of plant uptake of different soil N forms via root- and mycorrhizal mycelium-pathways enables efficient N acquisitions in response to changing soil N availability.

Conclusions

Multiple rhizosphere processes abovementioned collaboratively contribute to efficient plant N acquisition in alpine coniferous forests. Finally, we identify several research outlooks and directions to improve the understanding and prediction of ecosystem functions in alpine coniferous forests under on-going global changes.

Keywords: Rhizosphere, Plant nitrogen acquisition, Root-soil interaction, Alpine coniferous forests, Nitrogen limitation

References(123)

Adamczyk, B., Sietiö, O.M., Straková, P., Prommer, J., Wild, B., Hagner, M., Pihlatie, M., Fritze, H., Richter, A., Heinonsalo, J., 2019. Plant roots increase both decomposition and stable organic matter formation in boreal forest soil. Nat. Commun. 10, 3982. https://doi.org/10.1038/s41467-019-11993-1.
DOI Google Scholar

Adamczyk, B., Smolander, A., Kitunen, V., Godlewski, M., 2010. Proteins as nitrogen source for plants: a short story about exudation of proteases by plant roots. Plant Signal Behav. 5, 817-819. https://doi.org/10.4161/psb.5.7.11699.
DOI Google Scholar

Ågren, G.I., Wetterstedt, J.M., Billberger, M.F., 2012. Nutrient limitation on terrestrial plant growth–modeling the interaction between nitrogen and phosphorus. New Phytol. 194, 953-960. https://doi.org/10.1111/j.1469-8137.2012.04116.x.
DOI Google Scholar

Akselsson, C., Westling, O., Alveteg, M., Thelin, G., Fransson, A.M., Hellsten, S., 2008. The influence of N load and harvest intensity on the risk of P limitation in Swedish forest soils. Sci. Total Environ. 404(2-3), 284-289. https://doi.org/10.1016/j.scitotenv.2007.11.017.
DOI Google Scholar

Arvieu, J.C., Leprince, F., Plassard, C., 2003. Release of oxalate and protons by ectomycorrhizal fungi in response to P-deficiency and calcium carbonate in nutrient solution. Ann. For. Sci. 60(8), 815-821. https://doi.org/10.1051/forest:2003076.
DOI Google Scholar

Ashton, I.W., Miller, A.E., Bowman, W.D., Suding, K.N., 2010. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91(11), 3252-3260. https://doi.org/10.1890/09-1849.1.
DOI Google Scholar

Averill, C., Turner, B.L., Finzi, A.C., 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505(7484), 543-545. https://doi.org/10.1038/nature12901.
DOI Google Scholar

Bardgett, R.D., Streeter, T.C., Bol, R., 2003. Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84(5), 1277-1287. https://doi.org/10.1890/0012-9658(2003)084[1277:smcewp]2.0.co;2.
DOI Google Scholar

Baribault, T.W., Kobe, R.K., Finley, A.O., 2012. Tropical tree growth is correlated with soil phosphorus, potassium, and calcium, though not for legumes. Ecol. Monogr. 82(2), 189-203. https://doi.org/10.2307/41739364.
DOI Google Scholar

Bergmann, J., Weigelt, A., Van der Plas, F., Laughlin, D.C., Kuyper, T.W., Guerrero-Ramirez, N., Valverde-Barrantes, O.J., Bruelheide, H., Freschet, G.T., Iversen, C.M., Kattge, J., McCormack, M.L., Meier, I.C., Rillig, M.C., Roumet, C., Semchenko, M., Sweeney, C.J., Van Ruijven, J., York, L.M., Mommer, L., 2020. The fungal collaboration gradient dominates the root economics space in plants. Sci. Adv. 6(27), eaba3756. https://doi.org/10.1126/sciadv.aba3756.
DOI Google Scholar

Berthrong, S.T., Finzi, A.C., 2006. Amino acid cycling in three cold temperate forests of the northeastern USA. Soil Biol. Biochem. 38(5), 861-869. https://doi.org/10.1016/j.soilbio.2005.08.002.
DOI Google Scholar

Broughton, R.C.I., Newsham, K.K., Hill, P.W., Stott, A., Jones, D.L., 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. https://doi.org/10.1016/j.soilbio.2015.05.003.
DOI Google Scholar

Brzostek, E.R., Greco, A., Drake, J.E., Finzi, A.C., 2013. Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115(1), 65-76. https://doi.org/10.1007/s10533-012-9818-9.
DOI Google Scholar

Bücking, H., Kaflfle, A., 2015. Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5(4), 587-612. https://doi.org/10.3390/agronomy5040587.
DOI Google Scholar

Burton, J., Chen, C., Xu, Z., Ghadiri, H., 2007a. Gross nitrogen transformations in adjacent native and plantation forests of subtropical Australia. Soil Biol. Biochem. 39(2), 426-433. https://doi.org/10.1016/j.soilbio.2006.08.011.
DOI Google Scholar

Burton, J., Chen, C., Xu, Z., Ghadiri, H., 2007b. Soluble organic nitrogen pools in adjacent native and plantation forests of subtropical Australia. Soil Biol. Biochem. 39(11), 2723-2734. https://doi.org/10.1016/j.soilbio.2007.05.021.
DOI Google Scholar

Cairney, J.W.G., 2012. Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biol. Biochem. 47, 198-208. https://doi.org/10.1061/j-soilbio.2011.12.029.
DOI Google Scholar

Carmosinia, N., Devitob, K.J., Prepasc, E.E., 2002. Gross nitrogen transformations in harvested and mature aspen-conifer mixed forest soils from the Boreal Plain. Soil Biol. Biochem. 34(12), 1949-1951. https://doi.org/10.1016/S0038-0717(02)00172-4.
DOI Google Scholar

Chapin, F.S., Moilanen, L., Kielland, K., 1993. Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361(6408), 150-153. https://doi.org/10.1038/361150a0.
DOI Google Scholar

Chaturvedi, O.P., Singh, J.S., 1987. The structure and function of pine forest in Central Himalaya. I. Dry matter dynamics. Ann. Bot. 60(3), 237-252. https://doi.org/10.1093/oxfordjournals.aob.a087442.
DOI Google Scholar

Cheng, W., Parton, W.J., Gonzalez-Meler, M.A., Phillips, R., Asao, S., McNickle, G.G., Brzostek, E., Jastrow, J.D., 2014. Synthesis and modeling perspectives of rhizosphere priming. New Phytol. 201(1), 31-44. https://doi.org/10.1111/nph.12440.
DOI Google Scholar

Cheng, X., Euliss, A., Baumgartner, K., 2008. Nitrogen capture by grapevine roots and arbuscular mycorrhizal fungi from legume cover-crop residues under low rates of mineral fertilization. Biol. Fertil. Soils 44(7), 965-973. https://doi.org/10.1007/s00374-008-0281-7.
DOI Google Scholar

Corre, M.D., Brumme, R., Veldkamp, E., Beese, F.O., 2007. Changes in nitrogen cycling and retention processes in soils under spruce forests along a nitrogen enrichment gradient in Germany. Glob. Change Biol. 13(7), 1509-1527. https://doi.org/10.1111/j.1365-2486.2007.01371.x.
DOI Google Scholar

Courty, P.E., Buee, M., Diedhiou, A.G., Frey-Klett, P., Le Tacon, F., Rineau, F., Turpault, M.P., 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. https://doi.org/10.1016/j.soilbio.2009.12.006.
DOI Google Scholar

Craine, J.M., Elmore, A.J., Aidar, M.P.M., Bustamante, M., Dawson, T.E., Hobbie, E.A., Kahmen, A., Mack, M.C., McLauchlan, K.K., Michelsen, A., Nardoto, G.B., Pardo, L.H., Penuelas, J., Reich, P.B., Schuur, E.A.G., Stock, W.D., Templer, P.H., Virginia, R.A., Welker, J.M., Wright, I.J., 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. https://doi.org/10.1111/j.1469-8137.2009.02917.x.
DOI Google Scholar

Cui, Y., Bing, H., Fang, L., Jiang, M., Shen, G., Yu, J., Wang, X., Zhu, H., Wu, Y., Zhang, X., 2019. Extracellular enzyme stoichiometry reveals the carbon and phosphorus limitations of microbial metabolisms in the rhizosphere and bulk soils in alpine ecosystems. Plant Soil 458(1), 7-20. https://doi.org/10.1007/s11104-019-04159-x.
DOI Google Scholar

Daly, A.B., Jilling, A., Bowles, T.M., Buchkowski, R.W., Frey, S.D., Kallenbach, C.M., Keiluweit, M., Mooshammer, M., Schimel, J.P., Grandy, A.S., 2021. A holistic framework integrating plant-microbe-mineral regulation of soil bioavailable nitrogen. Biogeochemistry 154(2), 211-229. https://doi.org/10.1007/s10533-021-00793-9.
DOI Google Scholar

Davidson, E.A., Hart, S.C., Firestone, M.K., 1992. Internal cycling of nitrate in soils of a mature coniferous forest. Ecology 73(4), 1148-1156. https://doi.org/10.2307/1940665.
DOI Google Scholar

Ding, J., Kong, D., Zhang, Z., Cai, Q., Xiao, J., Liu, Q., Yin, H., 2020. Climate and soil nutrients differentially drive multidimensional fine root traits in ectomycorrhizal-dominated alpine coniferous forests. J. Ecol. 108(6), 2544-2556. https://doi.org/10.1111/1365-2745.13407.
DOI Google Scholar

Du, E., Terrer, C., Pellegrini, A.F., Ahlstrom, A., Van-Lissa, C.J., Zhao, X., Xia, N., Wu, X., Jackson, R.B., 2020. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13(3), 221-226. https://doi.org/10.1038/s41561-019-0530-4.
DOI Google Scholar

Elser, J.J., Bracken, M.E.S., Cleland, E.E., Gruner, D.S., Harpole, W.S., Hillebrand, H., Ngai, J.T., Seabloom, E.W., Shurin, J.B., Smith, J.E., 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10(12), 1135-1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x.
DOI Google Scholar

Emmett, B.D., Buckley, D.H., Drinkwater, L.E., 2020. Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field. New Phytol. 225(2), 960-973. https://doi.org/10.1111/nph.16171.
DOI Google Scholar

Erktan, A., Roumet, C., Bouchet, D., Stokes, A., Pailler, F., Munoz, F., 2018. Two dimensions define the variation of fine root traits across plant communities under the joint influence of ecological succession and annual mowing. J. Ecol. 106(5), 2031-2042. https://doi.org/10.1111/1365-2745.12953.
DOI Google Scholar

Fagotti, D.S.L., Miyauchi, M.Y.H., Oliveira, A.G., Santinoni, I.A., Eberhardt, D.N., Nimtz, A., Ribeiro, R.A., Paula, A.M., Queiroz, C.A.S., Andrade, G., Zangaro, W., Nogueira, M.A., 2012. Gradients in N-cycling attributes along forestry and agricultural land-use systems are indicative of soil capacity for N supply. Soil Use. Manage. 28(3), 292-298. https://doi.org/10.1111/j.14752743.2012.00418.x.
DOI Google Scholar

Fang, Y., Yoh, M., Koba, K., 2011. Nitrogen deposition and forest nitrogen cycling along an urban–rural transect in southern China. Global Change Biol. 17(2), 872-885. https://doi.org/10.1111/j.13652486.2010.02283.x.
DOI Google Scholar

Finzi, A.C., Berthrong, S.T., 2005. The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86(12), 3345-3353. https://doi.org/10.1890/04-1460.
DOI Google Scholar

Finzi, A.C., Schlesinger, W.H., 2003. Soil-nitrogen cycling in a pine forest exposed to 5 years of elevated carbon dioxide. Ecosystems 6(5), 444-456. https://doi.org/10.1007/s10021-003-0205-1.
DOI Google Scholar

Finzi, A.C., Abramoff, R.Z., Spiller, K.S., Brzostek, E.R., Darby, B.A., Kramer, M.A., Phillips, R.P., 2015. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biol. 21(5), 2082-2094. https://doi.org/10.1111/gcb.12816.
DOI Google Scholar

Frank, D.A., Groffman, P.M., 2009. Plant rhizospheric N processes: what we don't know and why we should care. Ecology 90(6), 1512-1519. https://doi.org/10.1890/08-0789.1.
DOI Google Scholar

Gan, D., Zeng, H., Zhu, B., 2022. The rhizosphere effect on soil gross nitrogen mineralization: a meta-analysis. Soil Ecol. Lett. 4(2), 144-154. https://doi.org/10.1007/s42832-021-0098-y.
DOI Google Scholar

Gao, J., Yi, M., Xu, X., Zhang, X., Yu, F., 2014. Spatiotemporal variations affect uptake of inorganic and organic nitrogen by dominant plant species in an alpine wetland. Plant Soil 381(1), 271-278. https://doi.org/10.1007/s11104-014-2130-9.
DOI Google Scholar

Grace, E.J., Cotsaftis, O., Tester, M., Smith, F.A., Smith, S.E., 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytol. 181(4), 938-949. https://doi.org/10.1111/j.1469-8137.2008.02720.x.
DOI Google Scholar

Greaver, T.L., Clark, C.M., Compton, J.E., Vallano, D., Talhelm, A.F., Weaver, C.P., Band, L.E., Baron, J.S., Davidson, E.A., Tague, C.L., Felker-Quinn, E., Lynch, J.A., Herrick, J.D., Liu, L., Goodale, C.L., Novak, K.J., Haeuber, R.A., 2016. Key ecological responses to nitrogen are altered by climate change. Nat. Clim. Change 6(9), 836-843. https://doi.org/10.1038/NCLIMATE3088.
DOI Google Scholar

Guo, W., Ding, J., Wang, Q., Yin, M., Zhu, X., Liu, Q., Zhang, Z., Yin, H., 2021a. Soil fertility controls ectomycorrhizal mycelial traits in alpine forests receiving nitrogen deposition. Soil Biol. Biochem. 161, 108386. https://doi.org/10.1016/j.soilbio.2021.108386.
DOI Google Scholar

Guo, W., Zhang, Z., Liu, Q., Xiao, J., Yin, H., 2021b. Seasonal variations in plant nitrogen acquisition in an ectomycorrhizal alpine forest on the eastern Tibetan Plateau, China. Plant Soil 459(1), 79-91. https://doi.org/10.1016/j.soilbio.2021.108386.
DOI Google Scholar

Han, M., Chen, Y., Li, R., Yu, M., Fu, L., Li, S., Su, J., Zhu, B., 2022. Root phosphatase activity aligns with the collaboration gradient of the root economics space. New Phytol. 234(3), 773-775. https://doi.org/10.1111/nph.17906.
DOI Google Scholar

Henneron, L., Cros, C., Picon-Cochard, C., Rahimian, V., Fontaine, S., 2020a. Plant economic strategies of grassland species control soil carbon dynamics through rhizodeposition. J. Ecol. 108(2), 528-545. https://doi.org/10.1111/1365-2745.13276.
DOI Google Scholar

Henneron, L., Kardol, P., Wardle, D.A., Cros, C., Fontaine, S., 2020b. Rhizosphere control of soil nitrogen cycling: a key component of plant economic strategies. New Phytol. 228(4), 1269-1282. https://doi.org/10.1111/nph.16760.
DOI Google Scholar

Hildebrandt, T.M., Nunes, A.N., Araujo, W.L., Braun, H.P., 2015. Amino acid catabolism in plants. Mol. Plant 8(11), 1563-1579. https://doi.org/10.1016/j.molp.2015.09.005.
DOI Google Scholar

Hobbie, E.A., Hobbie, J.E., 2008. Natural abundance of 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11(5), 815-830. https://doi.org/10.1077/s10021-008-9159-7.
DOI Google Scholar

Hobbie, J.E., Hobbie, E.A., 2006. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87(4), 816-822..https://doi.org/10.1890/0012-9658(2006)87[816:NISFAP]2.0CO;2.
DOI Google Scholar

Houlton, B.Z., Sigman, D.M., Schuur, E.A., Hedin, L.O., 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc. Natl. Acad. Sci. USA 104(21), 8902-8906. https://doi.org/10.1073/pnas.0609935104.
DOI Google Scholar

Hu, L., Robert, C.A.M., Cadot, S., Zhang, X., Ye, M., Li, B., Manzo, D., Chervet, N., Steinger, T., van der Heijden, M.G.A., Schlaeppi, K., Erb, M., 2018. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738. https://doi.org/10.1038/s41467-018-05122-7.
DOI Google Scholar

Isobe, K., Oka, H., Watanabe, T., Tateno, R., Urakawa, R., Liang, C., Senoo, K., Shibata, H., 2018. High soil microbial activity in the winter season enhances nitrogen cycling in a cool-temperate deciduous forest. Soil Biol. Biochem. 124, 90-100. https://doi.org/10.1016/j.soilbio.2018.05.028.
DOI Google Scholar

Jia, X., Huang, F., Hui, D., 2020. Nitrogen uptake by two plants in response to plant competition as regulated by neighbor density. Front. Plant Sci. 11, 584370. https://doi.org/10.3389/FPLS.2020.584370.
DOI Google Scholar

Jiang, J., Moore, J.A., Priyadarshi, A., Classen, A.T., 2017. Plant-mycorrhizal interactions mediate plant community coexistence by altering resource demand. Ecology 98(1), 187-197. https://doi.org/187-197.10.1002/ecy.1630.
DOI Google Scholar

Jones, D.L., Healey, J.R., Willett, V.B., Farrar, J.F., Hodge, A., 2005. Dissolved organic nitrogen uptake by plants-an important N uptake pathway? Soil Biol. Biochem. 37(3), 413-423. https://doi.org/10.1016/j.soilbio.2004.08.008.
DOI Google Scholar

Kaiser, C., Kilburn, M.R., Clode, P.L., Fuchslueger, L., Koranda, M., Cliff, J.B., Solaiman, Z.M., Murphy, D.V., 2015. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol. 205(4), 1537-1551. https://doi.org/10.1111/nph.13138.
DOI Google Scholar

Kielland, K., McFarland, J., Olson, K., 2006. Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288(1), 297-307. https://doi.org/10.1007/s11104-006-9117-0.
DOI Google Scholar

Koranda, M., Schnecker, J., Kaiser, C., Fuchslueger, L., Kitzler, B., Stange, C.F., Sessitsch, A., Zechmeister-Boltenstern, S., Richter, A., 2011. Microbial processes and community composition in the rhizosphere of European beech-the influence of plant C exudates. Soil Biol. Biochem. 43(3), 551-558. https://doi.org/10.1016/j.soilbio.2010.11.022.
DOI Google Scholar

Kuang, X., Jiao, J., 2016. Review on climate change on the Tibetan Plateau during the last half century. J. Geophys. Res. Atmos. 121(8), 3979-4007. https://doi.org/10.1002/2015jd024728.
DOI Google Scholar

Kuzyakov, Y., Xu, X., 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol. 198(3), 656-669. https://doi.org/10.1111/nph.12235.
DOI Google Scholar

Laliberté, E., 2017. Below-ground frontiers in trait-based plant ecology. New Phytol. 213(4), 1597-1603. https://doi.org/10.1111/nph.14247.
DOI Google Scholar

Lambers, H., Mougel, C., Jaillard, B., Hinsinger, P., 2009. Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321(1), 83-115. https://doi.org/10.1007/s11104-009-0042-x.
DOI Google Scholar

LeBauer, D., Treseder, K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystem is globally distributed. Ecology 89(2), 371-379. https://doi.org/10.1890/06-2057.1.
DOI Google Scholar

Li, M., Zhou, X., Zhang, Q., Cheng, X., 2014. Consequences of afforestation for soil nitrogen dynamics in central China. Agric. Ecosyst. Environ. 183, 40-46. https://doi.org/10.1016/j.agee.2013.10.018.
DOI Google Scholar

Li, Y., Sun, D., Li, D., 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, 17546. https://doi.org/10.1038/srep17546.
DOI Google Scholar

Liu, Y., Wang, L., He, R., Chen, Y., Xu, Z., Tan, B., Zhang, L., Xiao, J., Zhu, P., Chen, L., Guo, L., Zhang, J., 2019. Higher soil fauna abundance accelerates litter carbon release across an alpine forest-tundra ecotone. Sci. Rep. 9, 10561. https://doi.org/10.1038/s41598-019-47072-0.
DOI Google Scholar

Ma, L., Xu, X., Zhang, C., Lv, Y., Liu, G., Zhang, Q., Feng, J., Wang, R., 2021. Strong non-growing season N uptake by deciduous trees in a temperate forest: a 15N isotopic experiment. J. Ecol. 109(11), 3752-3766. https://doi.org/10.1111/1365-2745.13754.
DOI Google Scholar

McKane, R.B., Johnson, L.C., Shaver, G.R., Nadelhoffer, K.J., Rastetter, E.B., Fry, B., Giblin, A.E., Kielland, K., Kwiatkowski, B.L., Laundre, J.A., Murray, G., 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415, 68-71. https://doi.org/10.1038/415068a.
DOI Google Scholar

Meier, I.C., Pritchard, S.G., Brzostek, E.R., McCormack, M.L., Phillips, R.P., 2015. The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. New Phytol. 205(3), 1164-1174. https://doi.org/10.1111/nph.13122.
DOI Google Scholar

Moreau, D., Bardgett, R.D., Finlay, R.D., Jones, D.L., Philippot, L., Power, S., 2019. A plant perspective on nitrogen cycling in the rhizosphere. Funct. Ecol. 33(4), 540-552. https://doi.org/10.1111/1365-2435.13303.
DOI Google Scholar

Mouginot, C., Kawamura, R., Matulich, K.L., Berlemont, R., Allison, S.D., Amend, A.S., Martiny, A.C., 2014. Elemental stoichiometry of fungi and bacteria strains from grassland leaf litter. Soil Biol. Biochem. 76, 278-285. https://doi.org/10.1016/j. soilbio.2014.05.011.
DOI 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. https://doi.org/10.1016/j.envexpbot.2004.09.011.
DOI Google Scholar

Mwafulirwa, L.D., Baggs, E.M., Russell, J., Morley, N., Sim, A., Paterson, E., 2017. Combined effects of rhizodeposit C and crop residues on SOM priming, residue mineralization and N supply in soil. Soil Biol. Biochem. 113, 35-44. https://doi.org/10.1016/j.soilbio.2017.05.026.
DOI Google Scholar

Nordin, A., Schmidt, I.K., Shaver, G.R., 2004. Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85(4), 955-962. https://doi.org/10.1890/03-0084.
DOI Google Scholar

Nӓsholm, T., Ekblad, A., Nordin, A., Giesler, R., Högberg, M., Högberg, P., 1998. Boreal forest plants take up organic nitrogen. Nature 392(6679), 914-916. https://doi.org/10.1038/31921.
DOI Google Scholar

Nӓsholm, T., Kielland, K., Ganeteg, U., 2009. Uptake of organic nitrogen by plants. New Phytol. 182(1), 31-48. https://doi.org/10.1111/j.1469-8137.2008.02751.x.
DOI Google Scholar

Parker, A.J., Peet, R.K., 1984. Size and age structure of conifers forests. Ecology 65(5), 1685-1689. https://doi.org/10.2307/1939148.
DOI Google Scholar

Persson, J., Gardeström, P., Nasholm, T., 2006. Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. J. Exp. Bot. 57(11), 2651-2659. https://doi.org/10.1093/jxb/erl028.
DOI Google Scholar

Phillips, R.P., Brzostek, E., Midgley, M.G., 2013. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol. 199(1), 41-51. https://doi.org/10.1111/nph.12221.
DOI Google Scholar

Phillips, R.P., Finzi, A.C., Bernhardt, E.S., 2011. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol. Lett. 14(2), 187-194. https://doi.org/10.1111/j.1461-0248.2010.01570.x.
DOI Google Scholar

Phillips, R.P., Meier, I.C., Bernhardt, E.S., Grandy, A.S., Wickings, K., Finzi, A.C., 2012. Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol. Lett. 15(9), 1042-1049. https://doi.org/10.1111/j.1461-0248.2012.01827.x.
DOI Google Scholar

Read, D.J., Perez-Moreno, J., 2003. Mycorrhizas and nutrient cycling in ecosystems-a journey towards relevance? New Phytol. 157(3), 475-492. https://doi.org/10.1046/j.1469-8137.2003.00704.x.
DOI Google Scholar

Reich, P.B., Wright, I.J., Cavender-Bares, J., Craine, J.M., Oleksyn, J., Westoby, M., Walters, M.B., 2003. The evolution of plant functional variation: traits, spectra, and strategies. Int. J. Plant Sci. 164(S3), S143-S164. https://doi.org/10.1086/374368.
DOI Google Scholar

Riley, W.J., Zhu, Q., Tang, J., 2018. Weaker land–climate feedbacks from nutrient uptake during photosynthesis-inactive periods. Nat. Clim. Change 8(11), 1002-1006. https://doi.org/10.1038/s41558-018-0325-4.
DOI Google Scholar

Rosswall, T., 1982. Microbiological regulation of the biogeochemical nitrogen cycle. Plant Soil 67(1), 15-34. https://doi.org/10.1007/bf02182752.
DOI Google Scholar

Rothstein, D.E., 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. https://doi.org/10.1016/j.soilbio.2014.04.004.
DOI Google Scholar

Rumpf, S.B., Hulber, K., Klonner, G., Moser, D., Schutz, M., Wessely, J., Willner, W., Zimmermann, N.E., Dullinger, S., 2018. Range dynamics of mountain plants decrease with elevation. Proc. Natl. Acad. Sci. USA 115(8), 1848-1853. https://doi.org/10.1073/pnas.1713936115.
DOI Google Scholar

Saito, M.A., Goepfert, T.J., Ritt, J.T., 2008. Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnol. Oceanogr. 53(1), 276-290. https://doi.org/10.4319/LO.2008.53.1.0276.
DOI Google Scholar

Schimel, J.P., Chapin, F.S., 1996. Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants complete well for amino acid N. Ecology 77(7), 2142-2147. https://doi.org/10.2307/2265708.
DOI Google Scholar

Schleuss, P.M., Heitkamp, F., Sun, Y., Miehe, G., Xu, X., Kuzyakov, Y., 2015. Nitrogen uptake in an alpine Kobresia pasture on the Tibetan Plateau: localization by 15N labeling and implications for a vulnerable ecosystem. Ecosystems 18(6), 946-957. https://doi.org/10.1007/s10021-015-9874-9.
DOI Google Scholar

Shahzad, T., Chenu, C., Genet, P., Barot, S., Perveen, N., Mougin, C., Fontaine, S., 2015. Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol. Biochem. 80, 146-155. https://doi.org/10.1016/j.soilbio.2014.09.023.
DOI Google Scholar
Simard, S.W., Jones, M.D., Durall, D.M., 2003. Carbon and nutrient fluxes within and between mycorrhizal plants. In: van der Heijden, M.G.A., Sanders, I.R. (Eds. ), Mycorrhizal Ecology. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 33–74. https://doi.org/10.1007/978-3-540-38364-2_2.
DOI
Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis, third ed. Academic Press, London, UK. https://doi.org/10.2136/sssaj2008.0015br.
DOI

Smithwick, E.A.H., Lucash, M.S., McCormack, M.L., Sivandran, G., 2014. Improving the representation of roots in terrestrial models. Ecol. Model. 291, 193-204. https://doi.org/10.1016/j.ecolmodel.2014.07.023.
DOI Google Scholar

Song, F., Tian, X., Yang, C., He, X., Chen, B., Zhu, J., Hao, J., 2006. Ectomycorrhizal infection intensity of subalpine forest ecosystems in western Sichuan, China. Acta Ecol. Sin. 26, 4171-4178 (in Chinese). https://doi.org/10.3321/j.issn:1000-0933.2006.12.033.
DOI Google Scholar

Stefanie, V.F., Andrew, H., Nina, B., Niklaus, P.A., Bernhard, S., Michael, S.L., 2009. Belowground nitrogen partitioning in experimental grassland plant communities of varying species richness. Ecology 90(5), 1389-1399. https://doi.org/10.1890/08-0802.1.
DOI Google Scholar

Stuart, E.K., Plett, K.L., 2020. Digging deeper: in search of the mechanisms of carbon and nitrogen exchange in ectomycorrhizal symbioses. Front. Plant Sci. 10, 1658. https://doi.org/10.3389/fpls.2019.01658.
DOI Google Scholar

Talbot, J.M., Treseder, K.K., 2010. Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53(3), 169-179. https://doi.org/10.1016/j.pedobi.2009.12.001.
DOI Google Scholar

Talbot, J.M., Bruns, T.D., Smith, D.P., Branco, S., Glassman, S.I., Erlandson, S., Vilgalys, R., Peay, K.G., 2013. Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol. Biochem. 57, 282-291. https://doi.org/10.1016/j.soilbio.2012.10.004.
DOI Google Scholar

Tarvainen, L., Lutz, M., Räntfors, M., Näsholm, T., Wallin, G., 2016. Increased needle nitrogen contents did not improve shoot photosynthetic performance of mature nitrogen-poor Scots pine trees. Front. Plant Sci. 7, 1051. https://doi.org/10.3389/fpls.2016.01051.
DOI Google Scholar

van Dam, N.M., Bouwmeester, H.J., 2016. Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci. 21(3), 256-265. https://doi.org/10.1016/j.tplants.2016.01.008.
DOI Google Scholar

van der Heijden, M.G.A., Martin, F.M., Selosse, M.A., Sanders, I.R., 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205(4), 1406-1423. https://doi.org/10.1111/nph.13288.
DOI Google Scholar

Wallander, H., Ekblad, A., Godbold, D.L., Johnson, D., Bahr, A., Baldrian, P., Bjork, R.G., Kieliszewska-Rokicka, B., Kjoller, R., Kraigher, H., Plassard, C., Rudawska, M., 2013. Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils-a review. Soil Biol. Biochem. 57, 1034-1047. https://dx.doi.org/10.1016/j-soilbio.2012.08.027.
DOI Google Scholar

Wang, C., Wang, N., Zhu, J., Liu, Y., Xu, X., Niu, S., Yu, G., Han, X., He, N., 2018. Soil gross N ammonification and nitrification from tropical to temperate forests in eastern China. Funct. Ecol. 32(1), 83-94. https://doi.org/10.1111/1365-2435.13024.
DOI Google Scholar

Wang, L., Shen, J., 2019. Root/rhizosphere management for improving phosphorus use efficiency and crop productivity. Better Crops Plant Food 103(1), 36-39. https://doi.org/10.24047/BC103136.
DOI Google Scholar

Wang, Q., Xiao, J., Ding, J., Zhou, T., Zhang, Z., Liu, Q., Yin, H., 2021. Differences in root exudate inputs and rhizosphere effects on soil N transformation between deciduous and evergreen trees. Plant Soil 458(1), 277-289. https://doi.org/10.1007/s11104-019-04156-0.
DOI 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. https://doi.org/10.1093/treephys/27.3.413.
DOI Google Scholar

Wen, Z., White, P.J., Shen, J., Lambers, H., 2022. Linking root exudation to belowground economic traits for resource acquisition. New Phytol. 233(4), 1620-1635. https://doi.org/10.1111/nph.17854.
DOI Google Scholar

Wilkinson, A., Hill, P.W., Farrar, J.F., Jones, D.L., Bardgett, R.D., 2014. Rapid microbial uptake and mineralization of amino acids and peptides along a grassland productivity gradient. Soil Biol. Biochem. 72, 75-83. https://doi.org/10.1016/j.soilbio.2014.01.026.
DOI Google Scholar

Xu, Z., 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. https://doi.org/10.1016/j.apsoil.2010.07.005.
DOI Google Scholar

Xu, Z., Yin, H., Xiong, P., Wan, C., Liu, Q., 2012. Short-term responses of Picea Asperata seedlings of different ages grown in two contrasting forest ecosystems to experimental warming. Environ. Exp. Bot. 77, 1-11. https://doi.org/10.1016/j.envexpbot.2011.10.011.
DOI Google Scholar

Yin, H., Wheeler, E., Phillips, R.P., 2014. Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol. Biochem. 78, 213-221. https://doi.org/10.1016/j.soilbio.2014.07.022.
DOI Google Scholar

Zhang, F., Shen, J., Zhang, J., Zuo, Y., Li, L., Chen, X., 2010. Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Adv. Agr. 107, 1-32. https://doi.org/10.1016/S0065-2113(10)07001-X.
DOI Google Scholar

Zhang, Z., Li, N., Xiao, J., Zhao, C., Zou, T., Li, D., Liu, Q., Yin, H., 2018a. Changes in plant nitrogen acquisition strategies during the restoration of spruce plantations on the eastern Tibetan Plateau, China. Soil Biol. Biochem. 119, 50-58. https://doi.org/10.1016/j.soilbio.2018.01.002.
DOI Google Scholar

Zhang, Z., Phillips, R.P., Zhao, W., Yuan, Y., Liu, Q., Yin, H., 2019a. Mycelia-derived C contributes more to nitrogen cycling than root-derived C in ectomycorrhizal alpine forests. Funct. Ecol. 33(2), 346-359. https://doi.org/10.1111/1365-2435.13236.
DOI Google Scholar

Zhang, Z., Xiao, J., Yuan, Y., Zhao, C., Liu, Q., Yin, H., 2018b. Mycelium- and root-derived C inputs differ in their impacts on soil organic C pools and decomposition in forests. Soil Biol. Biochem. 123, 257-265. https://doi.org/10.1016/j.soilbio.2018.05.015.
DOI Google Scholar

Zhang, Z., Yuan, Y., Liu, Q., Yin, H.J., 2019b. Plant nitrogen acquisition from inorganic and organic sources via root and mycelia pathways in ectomycorrhizal alpine forests. Soil Biol. Biochem. 136, 107517. https://doi.org/10.1016/j.soilbio.2019.06.013.
DOI Google Scholar

Zhang, Z., Yuan, Y., Zhao, W., He, H., Li, D., 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. https://doi.org/10.1016/j.soilbio.2016.11.002.
DOI Google Scholar

Zhu, F., Dai, L., Hobbie, E.A., Koba, K., Liu, X., Gurmesa, G.A., 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. https://doi.org/10.3389/fpls.2019.00799.
DOI Google Scholar

Zhu, X., Liu, D., Yin, H., 2021. Roots regulate microbial N processes to achieve an efficient NH4+ supply in the rhizosphere of alpine coniferous forests. Biogeochemistry 155(1), 39-57. https://doi.org/10.1007/s10533-021-00811-w.
DOI Google Scholar

Zhu, X., Zhang, Z., Wang, Q., Peñuelas, J., Sardans, J., Lambers, H., Liu, Z., Yin, H., 2022. More soil organic carbon is sequestered through the mycelium-pathway than through the root-pathway under nitrogen enrichment in an alpine forest. Global Change Biol. 28(16), 4947-4961. https://doi.org/10.1111/gcb.16263.
DOI Google Scholar
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Publication history

Received: 16 September 2022
Revised: 22 October 2022
Accepted: 23 October 2022
Published: 03 November 2022
Issue date: December 2022

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© 2022 The Authors.

Acknowledgements

Acknowledgements

This study was supported jointly by the Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (No. 2019QZKK0301), the Chinese Academy of Sciences (CAS) Interdisciplinary Innovation Team (No. xbzg-zysys-202112), and the National Natural Science Foundation of China (Nos. 32171757, 31872700). Moreover, Bartosz Adamczyk acknowledges the Academy of Finland (No. 330136).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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