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Research Articles

Plasticity in nitrogen form uptake and preference in response to long-term nitrogen addition of the main tree species in a temperate old growth forest

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Pages 127-137 | Received 27 Sep 2023, Accepted 21 Dec 2023, Published online: 30 Dec 2023

References

  • Andersen KM, Turner BL. 2013. Preferences or plasticity in nitrogen acquisition by understorey palms in a tropical montane forest. J Ecol. 101(3):819–825. doi:10.1111/1365-2745.12070.
  • Andrews M, Raven JA, Lea PJ. 2013. Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Ann Appl Biol. 163(2):174–199. doi:10.1111/aab.12045.
  • Arora K, Srivastava A. 2013. Nitrogen losses due to nitrification: plant based remedial prospects. Int J Bioassays. 2(7):984–991.
  • Bassirirad H. 2000. Kinetics of nutrient uptake by roots: responses to global change. New Phytol. 147:155–169. doi:10.1046/j.1469-8137.2000.00682.x.
  • Bowsher AW, Miller BJ, Donovan LA. 2015. Evolutionary divergences in root system morphology, allocation, and nitrogen uptake in species from high-versus low-fertility soils. Funct Plant Biol. 43(2):129–140. doi:10.1071/FP15162.
  • Breteler H, Siegerist M. 1984. Effect of ammonium on nitrate utilization by root of dwarf bean. Plant Physiol. 75:1099–1103. doi:10.1104/pp.75.4.1099.
  • Britto DT, Kronzucker HJ. 2002. NH4+ toxicity in higher plants: a critical review. J Plant Physiol. 159(6):567–584. doi:10.1078/0176-1617-0774.
  • Britto DT, Kronzucker HJ. 2013. Ecological significance and complexity of N-source preference in plants. Ann Bot. 112(6):957–963. doi:10.1093/aob/mct157.
  • Cao J, Yang L, Pang S, Yang J, Hu Y, Li Y, Li L, Wang Q. 2021. Convergent nitrogen uptake patterns and divergent nitrogen acquisition strategies of coexisting plant species in response to long-term nitrogen enrichment in a temperate grassland. Environ Exp Bot. 185:104412. doi:10.1016/j.envexpbot.2021.104412.
  • Chalk P, Smith C. 2021. On inorganic N uptake by vascular plants: can 15N tracer techniques resolve the NH4+ versus NO3− “preference” conundrum? Eur J Soil Sci. 72(4):1762–1779. doi:10.1111/ejss.13069.
  • Chalot M, Brun A. 1998. Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev. 22(1):21–44. doi:10.1111/j.1574-6976.1998.tb00359.x.
  • Chen GT, Tu LH, Peng Y, Hu HL, Hu TX, Xu ZF, Liu L, Tang Y. 2016. Effect of nitrogen additions on root morphology and chemistry in a subtropical bamboo forest. Plant Soil. 412:441–451. doi:10.1007/s11104-016-3074-z.
  • Colmer TD, Bloom AJ. 1998. A comparison of NH4+ and NO3− net fluxes along roots of rice and maize. Plant Cell Environ. 21(2):240–246. doi:10.1046/j.1365-3040.1998.00261.x.
  • Coskun D, Britto DT, Li M, Becker A, Kronzucker HJ. 2013. Rapid ammonia gas transport accounts for futile transmembrane cycling under NO3−/NH4+ toxicity in plant roots. Plant Physiol. 163(4):1859–1867. doi:10.1104/pp.113.225961.
  • Crawford NM, Glass AD. 1998. Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci. 3(10):389–395. doi:10.1016/S1360-1385(98)01311-9.
  • Cui J, Yu C, Qiao N, Xu X, Tian Y, Ouyang H. 2017. Plant preference for NH4+ versus NO3− at different growth stages in an alpine agroecosystem. Field Crops Res. 201:192–199. doi:10.1016/j.fcr.2016.11.009.
  • Diekmann M, Lawesson JE. 1999. Shifts in ecological behaviour of herbaceous forest species along a transect from northern central to north Europe. Folia Geobot. 34:127–141. doi:10.1007/BF02803080.
  • Finlay RD, Ek H, Odham G, Süderström B. 1989. Uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium and nitrate sources by intact ectomycorrhizal systems of Fagus sylvatica infected with Paxillus involutus. New Phytol. 113(1):47–55. doi:10.1111/j.1469-8137.1989.tb02394.x.
  • Fitter AH, Stickland TR. 1992. Architectural analysis of plant root systems: III. Studies on plants under field conditions. New Phytol. 121(2):243–248. doi:10.1111/j.1469-8137.1992.tb01110.x.
  • Gao L, Cui X, Hill PW, Guo Y. 2020. Uptake of various nitrogen forms by co-existing plant species in temperate and cold-temperate forests in northeast China. Appl Soil Ecol. 147:103398. doi:10.1016/j.apsoil.2019.103398.
  • Greaver TL, Clark CM, Compton JE, Vallano D, Talhelm AF, Weaver CP, Band LE, Baron JS, Davidson EA, Tague CL, et al. 2016. Key ecological responses to nitrogen are altered by climate change. Nat Clim Change. 6(9):836–843. doi:10.1038/nclimate3088.
  • Guo DL, Mitchell RJ, Hendricks JJ. 2004. Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia. 140:450–457. doi:10.1007/s00442-004-1596-1.
  • Guo P, Yang L, Kong D, Zhao H. 2022. Differential effects of ammonium and nitrate addition on soil microbial biomass, enzymatic activities, and organic carbon in a temperate forest in north China. Plant Soil. 481(1-2):595–606. doi:10.1007/s11104-022-05663-3.
  • Gurmesa GA, Wang A, Li S, Peng S, de Vries W, Gundersen P, Ciais P, Phillips OL, Hobbie EA, Zhu W, et al. 2022. Retention of deposited ammonium and nitrate and its impact on the global forest carbon sink. Nat Commun. 13(1):880. doi:10.1038/s41467-022-28345-1.
  • He X, Chi Q, Meng L, Zhao C, He M, Dan X, Huang X, Zhao J, Cai Z, Zhang J, et al. 2022. Plants with nitrate preference can regulate nitrification to meet their nitrate demand. Soil Biol Biochem. 165:108516. doi:10.1016/j.soilbio.2021.108516.
  • Hickman JE, Ashton IW, Howe KM, Lerdau MT. 2013. The native–invasive balance: implications for nutrient cycling in ecosystems. Oecologia. 173:319–328. doi:10.1007/s00442-013-2607-x.
  • Hobbie EA, Högberg P. 2012. Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol. 196(2):367–382. doi:10.1111/j.1469-8137.2012.04300.x.
  • 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. doi:10.1007/s11104-017-3434-3.
  • Hong J, Ma X, Zhang X, Wang X. 2017. Nitrogen uptake pattern of herbaceous plants: coping strategies in altered neighbor species. Biol Fertil Soils. 53:729–735. doi:10.1007/s00374-017-1230-0.
  • Houle D, Moore JD, Ouimet R, Marty C. 2014. Tree species partition N uptake by soil depth in boreal forests. Ecology. 95(5):1127–1133. doi:10.1890/14-0191.1.
  • Inselsbacher E, Näsholm T. 2012. The below-ground perspective of forest plants: soil provides mainly organic nitrogen for plants and mycorrhizal fungi. New Phytol. 195(2):329–334. doi:10.1111/j.1469-8137.2012.04169.x.
  • Jach-Smith LC, Jackson RD. 2018. N addition undermines N supplied by arbuscular mycorrhizal fungi to native perennial grasses. Soil Biol Biochem. 116:148–157. doi:10.1016/j.soilbio.2017.10.009.
  • Jiang Q, Lin C, Guo R, Xiong D, Yao X, Wang X, Chen T, Jia L, Wu D, Fan A, et al. 2023. Root nitrogen uptake capacity of Chinese fir enhanced by warming and nitrogen addition. Tree Physiol. 43(1):31–46. doi:10.1093/treephys/tpac103.
  • Kamminga-Van Wijk C, Prins HB. 1993. The kinetics of NH4+ and NO3− uptake by Douglas fir from single N-solutions and from solutions containing both NH4+ and NO3−. Plant Soil. 151:91–96. doi:10.1007/BF00010789.
  • Kamminga-van Wijk J. 1991. Mycorrhizal and nonmycorrhizal Douglas fir grown in hydroculture [Ph.D. thesis]. State Univ. Groningen. 133 p.
  • Kou L, Guo D, Yang H, Gao W, Li S. 2015. Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtropical China. Plant Soil. 391:207–218. doi:10.1007/s11104-015-2420-x.
  • Kronzucker HJ, Siddiqi MY, Glass AD. 1996. Kinetics of NH4+ influx in spruce. Plant Physiol. 110(3):773–779. doi:10.1104/pp.110.3.773.
  • 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. doi:10.1111/nph.12235.
  • Li C, Li Q, Qiao N, Xu X, Li Q, Wang H. 2016. Inorganic and organic nitrogen uptake by nine dominant subtropical tree species. iFor Biogeosci For. 9(2):253. doi:10.3832/ifor1502-008.
  • Li W, Wang W, Sun R, Li M, Liu H, Shi Y, Zhu D, Li J, Ma L, Fu S. 2023. Influence of nitrogen addition on the functional diversity and biomass of fine roots in warm-temperate and subtropical forests. For Ecol Manag. 545:121309. doi:10.1016/j.foreco.2023.121309.
  • Lipson D, Näsholm T. 2001. The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia. 128:305–316. doi:10.1007/s004420100693.
  • Liu M, Li C, Xu X, Wanek W, Jiang N, Wang H, Yang X. 2017a. Organic and inorganic nitrogen uptake by 21 dominant tree species in temperate and tropical forests. Tree Physiol. 37(11):1515–1526. doi:10.1093/treephys/tpx046.
  • Liu X, Duan L, Mo J, Du E, Shen J, Lu X, Zhang Y, Zhou X, He C, Zhang F. 2011. Nitrogen deposition and its ecological impact in China: an overview. Environ Pollut. 159(10):2251–2264. doi:10.1016/j.envpol.2010.08.002.
  • Liu XJA, van Groenigen KJ, Dijkstra P, Hungate BA. 2017b. Increased plant uptake of native soil nitrogen following fertilizer addition–not a priming effect? Appl Soil Ecol. 114:105–110. doi:10.1016/j.apsoil.2017.03.011.
  • Long Y, Kong D, Chen Z, Zeng H. 2013. Variation of the linkage of root function with root branch order. PLoS One. 8(2):e57153. doi:10.1371/journal.pone.0057153.
  • Lü C, Tian H. 2007. Spatial and temporal patterns of nitrogen deposition in China: synthesis of observational data. J Geophys Res Atmos. 112(D22). doi:10.1029/2006JD007990.
  • Ma X, Zhu B, Nie Y, Liu Y, Kuzyakov Y. 2021. Root and mycorrhizal strategies for nutrient acquisition in forests under nitrogen deposition: a meta-analysis. Soil Biol Biochem. 163:108418. doi:10.1016/j.soilbio.2021.108418.
  • Ma Z, Guo D, Xu X, Lu M, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO. 2019. Evolutionary history resolves global organization of root functional traits. Nature. 555(7694):94–97. doi:10.1038/nature25783.
  • Mao J, Mao Q, Gundersen P, Gurmesa GA, Zhang W, Huang J, Wang S, Li A, Wang Y, Guo Y, et al. 2022. Unexpected high retention of 15N-labeled nitrogen in a tropical legume forest under long-term nitrogen enrichment. Glb Chg Bio. 28(4):1529–1543. doi:10.1111/gcb.16005.
  • Metcalfe RJ, Nault J, Hawkins BJ. 2011. Adaptations to nitrogen form: comparing inorganic nitrogen and amino acid availability and uptake by four temperate forest plants. Can J For Res. 41(8):1626–1637. doi:10.1139/x11-090.
  • Näsholm T, Kielland K, Ganeteg U. 2009. Uptake of organic nitrogen by plants. New Phytol. 182(1):31–48. doi:10.1111/j.1469-8137.2008.02751.x.
  • Nordin A, Högberg P, Näsholm T. 2001. Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia. 129:125–132. doi:10.1007/s004420100698.
  • Owen AG, Jones DL. 2001. Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem. 33(4-5):651–657. doi:10.1016/S0038-0717(00)00209-1.
  • Persson J, Högberg P, Ekblad A, Högberg MN, Nordgren A, Näsholm T. 2003. Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia. 137:252–257. doi:10.1007/s00442-003-1334-0.
  • Purugganan MD, Fuller DQ. 2009. The nature of selection during plant domestication. Nature. 457(7231):843–848. doi:10.1038/nature07895.
  • Rennenberg H, Dannenmann M, Gessler A, Kreuzwieser J, Simon J, Papen H. 2009. Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biol. 11:4–23. doi:10.1111/j.1438-8677.2009.00241.x.
  • Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology. 85(3):591–602. doi:10.1890/03-8002.
  • Song L, Li Z, Niu S. 2021. Global soil gross nitrogen transformation under increasing nitrogen deposition. Global Biogeochem Cycles. 35(1):e2020GB006711. doi:10.1029/2020GB006711.
  • 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. 394:215–224. doi:10.1007/s11104-015-2532-3.
  • Stevens CJ. 2019. Nitrogen in the environment. Science. 363(6427):578–580. doi:10.1126/science.aav8215.
  • Tahovska K, Choma M, Kaštovská E, Oulehle F, Bárta J, Šantrůčková H, Moldan F. 2020. Positive response of soil microbes to long-term nitrogen input in spruce forest: results from Gårdsjön whole-catchment N-addition experiment. Soil Biol Biochem. 143:107732. doi:10.1016/j.soilbio.2020.107732.
  • Teglia A, Di Baccio D, Matteucci G, Scartazza A, De Cinti B, Mazzenga F, Ravaioli D, Muzzi E, Marcolini G, Magnani F. 2022. Effects of simulated nitrogen deposition on the nutritional and physiological status of beech forests at two climatic contrasting sites in Italy. Sci Total Environ. 834:155362. doi:10.1016/j.scitotenv.2022.155362.
  • 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. doi:10.1023/B:PLSO.0000037047.16616.98.
  • Tian D, Du E, Jiang L, Ma S, Zeng W, Zou A, Feng C, Xu L, Xing A, Wang W, et al. 2018. Responses of forest ecosystems to increasing N deposition in China: a critical review. Environ Pollut. 243:75–86. doi:10.1016/j.envpol.2018.08.010.
  • Uscola M, Villar-Salvador P, Oliet J, Warren CR. 2017. Root uptake of inorganic and organic N chemical forms in two coexisting Mediterranean forest trees. Plant Soil. 415:387–392. doi:10.1007/s11104-017-3172-6.
  • Wang L, Macko SA. 2011. Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell Environ. 34(3):525–534. doi:10.1111/j.1365-3040.2010.02260.x.
  • Wang X, Wang N, Xing Y, Ben El Caid M. 2018. Synergetic effects of plastic mulching and nitrogen application rates on grain yield, nitrogen uptake and translocation of maize planted in the Loess Plateau of China. Sci Rep. 8(1):14319. doi:10.1038/s41598-018-32749-9.
  • Warren CR. 2009. Does nitrogen concentration affect relative uptake rates of nitrate, ammonium, and glycine? J Plant Nutr Soil Sci. 172(2):224–229. doi:10.1002/jpln.200800251.
  • Yu G, Jia Y, He N, Zhu J, Chen Z, Wang Q, Piao S, Liu X, He H, Guo X, et al. 2019. Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat Geosci. 12(6):424–429. doi:10.1038/s41561-019-0352-4.
  • 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. doi:10.1016/j.soilbio.2018.01.002.
  • Zhao X, Tian Q, Huang L, Lin Q, Wu J, Liu F. 2022. Fine-root functional trait response to nitrogen deposition across forest ecosystems: a meta-analysis. Sci Total Environ. 844:157111. doi:10.1016/j.scitotenv.2022.157111.
  • Zhou M, Yan G, Xing Y, Chen F, Zhang X, Wang J, Zhang J, Dai G, Zheng X, Sun W, et al. 2019. Nitrogen deposition and decreased precipitation does not change total nitrogen uptake in a temperate forest. Sci Total Environ. 651:32–41. doi:10.1016/j.scitotenv.2018.09.166.
  • Zhou X, Wang A, Hobbie EA, Zhu F, Qu Y, Dai L, Li D, Liu X, Zhu W, Koba K, et al. 2021. Mature conifers assimilate nitrate as efficiently as ammonium from soils in four forest plantations. New Phytol. 229(6):3184–3194. doi:10.1111/nph.17110.

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