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Effect of N addition on root exudation and associated microbial N transformation under Sibiraea angustata in an alpine shrubland

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Abstract

Background and aim

Root exudates are generally known to play an important role in ecosystem carbon (C) and nitrogen (N) cycling. We aimed to quantify the responses of root exudates to increased N availability in an alpine shrub-dominated ecosystem, and unravel the associated ecological consequences to N cycling.

Methods

After three consecutive years of N addition at three rates (N0, control; N5, 5 g N m−2 year−1; N10, 10 g N m−2 year−1), we measured in situ rate of root exudation for mature Sibiraea angustata shrubs, as well as soil microbial biomass, the activities of three extracellular enzymes, and net N mineralization rates (Nmin) in both rhizosphere and bulk soil.

Results

Exudation rates were 13% and 45% lower in the N5 and N10 plots compared to the control plots over the primary growing season. This, together with decreasing fine root biomass and length, lead to an annual decline of 44% and 66% in root exudate C inputs to soil, respectively. These decreased exudation rates were both directly and indirectly, through its effect on the rhizosphere effect (RE) on polyphenol oxidase activity, linked to decreased the RE on Nmin. As a result of N-induced decreases in both the RE on Nmin and rhizosphere volume, we estimated that the ecosystem-level rhizosphere effect for Nmin from 13% in the control plots to 8% in the N5 plots, and to 2% in the N10 plots.

Conclusions

Overall, our results demonstrate that N addition may decelerate the C efflux from root exudates, resulting in a slower decomposition of soil organic matter and also gradually decelerating soil N cycling in alpine shrub ecosystems.

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References

  • Aitkenhead-peterson JA, Kalbitz K (2005) Short-term response on the quantity and quality ofrhizo-deposited carbon from Norway spruce exposed to low and high N inputs. J Plant Nutr Soil Sci 168(5):687–693

    Article  CAS  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681

    Article  CAS  PubMed  Google Scholar 

  • Belnap J, Hawkes CV, Firestone MK (2003) Boundaries in miniature: Two examples from soil. BioScience 53:739–749

    Article  Google Scholar 

  • Brookes P, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17(6):837–842

    Article  CAS  Google Scholar 

  • Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD 422 (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201(1):31–44.

  • Darwent MJ, Paterson E, McDonald AJS, Tomos AD (2003) Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration. J Exp Bot 54(381):325–334

    Article  CAS  PubMed  Google Scholar 

  • DeAngelis KM, Lindow SE, Firestone MK (2008) Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microbio Ecol 66(2):197–207

  • Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJ (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14(4):349–357

    Article  PubMed  Google Scholar 

  • Ekblad A, Nordgren A (2002) Is growth of soil microorganisms in boreal forests limited by carbon or nitrogen availability? Plant Soil 242(1):115–122

    Article  CAS  Google Scholar 

  • Falchini L, Naumova N, Kuikman PJ, Bloem J, Nannipieri P (2003) CO2 evolution and denaturing gradient gel electrophoresis profiles of bacterial communities in soil following addition of low molecular weight substrates to simulate root exudation. Soil Bio Biochem 35(6):775–782

    Article  CAS  Google Scholar 

  • Gao Q, Yang X, Yin C, Liu Q (2014) Estimation of biomass allocation and carbon density in alpine dwarf shrubs in Garzê Zangzu Autonomous Prefecture of Sichuan Province, China. Chin J Plant Ecol 38(4):355–365

    Article  Google Scholar 

  • Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS (2004) Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139:545–550

    Article  PubMed  Google Scholar 

  • Haichar FEZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80

  • He HL, Yang XC, Wang D, Sun YY, Yin CY, Li T, Li YX, Zhou GY, Zhang L, Liu Q (2015) Ecological stoichiometric characteristics of soil carbon, nitrogen and phosphorus of Sibiraea angustata shrub in eastern Qinghai-Tibetan Plateau. Chin J Appl Environ Biol 21(6):1128–1135

    CAS  Google Scholar 

  • Heath J, Ayres E, Possell M, Bardgett RD, Black HI, Grant H, Ineson P, Kerstiens G (2005) Rising atmospheric CO2 reduces sequestration of root-derived soil carbon. Science 309(5741):1711–1713

    Article  CAS  PubMed  Google Scholar 

  • Jin M, Li Y, Wang S, Zhang X, Lei L (2012) Alpine shrubs biomass and its distribution characteristics in Qilian Mountains. Arid Land Geography 35(6):952–959

    Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163(3):459–480

    Article  CAS  Google Scholar 

  • Kirkby CA, Richardson AE, Wade LJ, Passioura JB, Batten GD, Blanchard C, Kirkegaard JA (2014) Nutrient availability limits carbon sequestration in arable soils. Soil Biol Biochem 68:402–409

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165:382–396

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42(9):1363–1371

    Article  CAS  Google Scholar 

  • Landi L, Valori F, Ascher J, Renella G, Falchini L, Nannipieri P (2006) Root exudate effects on the bacterial communities, CO2 evolution, nitrogen transformations and ATP content of rhizosphere and bulk soils. Soil Bio Biochem 38(3):509–516

    Article  CAS  Google Scholar 

  • Lei L, Liu X, Wang S, Li Y, Zhang X (2011) Assignment rule of alpine shrubs biomass and its relationships to environmental factors in Qilian Mountains. Ecol Environ Sci 20(11):1602–1607

    Google Scholar 

  • Li J, Yin C, Zhou X, Wei Y, Gao Q, Liu Q (2014) Effects of nitrogen addition on soil respiration of Sibiraea angustata shrub in the eastern margin of Qinghai-Tibetan Plateau. Act Ecol Sin 34(19):5558–5569

    Google Scholar 

  • Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828

    Article  PubMed  Google Scholar 

  • Lü C, Tian H (2007) Spatial and temporal patterns of nitrogen deposition in China: synthesis of observational data. Atmospheres 112(D22)

  • Maier A, Riedlinger J, Fiedler HP, Hampp R (2004) Actinomycetales bacteria from a spruce stand: characterization and effects on growth of root symbiotic and plant parasitic soil fungi in dual culture. Mycol Prog 3(2):129–136

    Article  Google Scholar 

  • Meier IC, Avis AG, Phillips RP (2012) Fungal communities influence root exudation rates in pine seedlings. FEMS microbiology ecology 83(3):585–595

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Mikan CJ, Zak DR, Kubiske ME, Pregitzer KS (2000) Combined effects of atmospheric CO 2 and N availability on the belowground carbon and nitrogen dynamics of aspen mesocosms. Oecologia 124(3):432–445

    Article  CAS  PubMed  Google Scholar 

  • Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147(1):131–139

    Article  CAS  Google Scholar 

  • Neumann G, Romheld V (2000) The release of root exudates as affected by the plant’s physiological status. The rhizosphere: CRC press. pp. 57–110.

  • Paterson E, Sim A (2000) Effect of nitrogen supply and defoliation on loss of organic compounds from roots of Festuca rubra. J Exp Bot 51(349):1449–1457

    Article  CAS  PubMed  Google Scholar 

  • Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Soil Biol Biochem 24(1):1–2

    Google Scholar 

  • Persson T, Rudebeck A, Jussy JH, Colin-Belgrand M, Priemé A, Dambrine E, Karlsson PS, Sjöberg RM (2000) Soil nitrogen turnover—mineralisation, nitrification and denitrification in European forest soils. Carbon and nitrogen cycling in European forest ecosystems: Springer. pp.:297–311

  • Perveen N, Barot S, Alvarez G, Klumapp K, Martin R, Rapaport A, Herfurth D, Louault F, Fontaine S (2014) Priming effect and microbial diversity in ecosystem functioning and response to global change: a modeling approach using the SYMPHONY model. Glob Change Biol 20:1174–1190

    Article  Google Scholar 

  • Phillips RP, Fahey TJ (2006) Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Ecology 87(5):1302–1313

    Article  PubMed  Google Scholar 

  • Phillips RP, Fahey TJ (2008) The influence of soil fertility on rhizosphere effects in northern hardwood forest soils. Soil Sci Soc Am J 72(2):453–461

    Article  CAS  Google Scholar 

  • Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22(6):990–999

    Article  Google Scholar 

  • Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol 29(12):1513–1523

    Article  CAS  PubMed  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (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

    Article  PubMed  Google Scholar 

  • Phillips RP, Meier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC (2012) Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol Lett 15(9):1042–1049

    Article  PubMed  Google Scholar 

  • Reich PB, Hungate BA, Luo Y (2006) Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu Rev. Ecol Evol Syst 37:611–636

    Article  Google Scholar 

  • Saiya-Cork K, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34(9):1309–1315

    Article  CAS  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85(3):591–602

    Article  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35(4):549–563

    Article  CAS  Google Scholar 

  • Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) (2014) IPCC, 2013: climate change 2013: the physical science basis: contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

  • Sturm M, Racine C, Tape K (2001) Increasing shrub abundance in the Arctic. Nature 411(31):546–547

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Xu X, Kuzyakov Y (2014) Mechanisms of rhizosphere priming effects and their ecological significance. Chinese Journal of Plant Ecology 38(1):62–75

    Article  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

    Article  CAS  Google Scholar 

  • Wang D, He H, Gao Q, He W, Zhao C, Yin H, Liu Q (2017) Effects of short-term N addition on soil C fluxes in alpine Sibiraea angustata scrub on the eastern margin of the Qinghai-Tibetan Plateau. Agricultural forest meteorology 247:151–158

    Article  Google Scholar 

  • Wang Q, Xiao J, Ding J, Zou T, Zhang Z, Liu Q, Yin H (2019) Differences in root exudate inputs and rhizosphere effects on soil N transformation between deciduous and evergreen trees. Plant Soil 29:1–3

    CAS  Google Scholar 

  • Warembourg F, Estelrich H (2001) Plant phenology and soil fertility effects on below-ground carbon allocation for an annual (Bromus madritensis) and a perennial (Bromus erectus) grass species. Soil Biol Biochem 33(10):1291–1303

    Article  CAS  Google Scholar 

  • Werth M, Kuzyakov Y (2006) Assimilate partitioning affects 13C fractionation of recently assimilated carbon in maize. Plant Soil 284(1-2):319–333

  • Wu N (1998) The community types and biomass of Sibiraea angustata scrub and their relationship with environmental factors in northwestern Sichuan. Act Bot Sin 40:860–870

    Google Scholar 

  • Wu J, Joergensen R, Pommerening B, Chaussod R, Brookes P (1990) Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biol Biochem 22(8):1167–1169

    Article  CAS  Google Scholar 

  • Yang Y, Wu Q, Yang W, Wu F, Zhang L, Xu Z, Yang L, Tan B, Han L, Zhou W (2020) Temperature and soil nutrients drive the spatial distributions of soil macroinvertebrates on the eastern Tibetan Plateau. Ecosphere 11(3):e03075

    Article  Google Scholar 

  • Yin H, Li Y, Xiao J, Xu Z, Cheng X, Liu Q (2013) Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Glob Change Biol 19(7):2158–2167

    Article  Google Scholar 

  • Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221

    Article  CAS  Google Scholar 

  • Yin H, Phillips RP, Liang R, Xu Z, Liu Q (2016) Resource stoichiometry mediates soil C loss and nutrient transformations in forest soils. Appl Soil Ecol 108:248–257

    Article  Google Scholar 

  • Zhao L, Li Y, Xu S, Zhou H, Gu S, Yu G, Zhao X (2006) Diurnal, seasonal and annual variation in net ecosystem CO2 exchange of an alpine shrubland on Qinghai-Tibetan plateau. Glob Change Biol 12(10):1940–1953

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported jointly by the Science and Technology Basic Work of Science and Technology (2015FY110300), Frontier Science Key Research Programs of CAS (QYZDB-SSW-SMC023), and the National Natural Science Foundation of China (No. 31872700, 31670449, 31270552 and 31960271). RL was supported by the Academy of Finland grant 289116.

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He, W., Yuan, Y., Zhang, Z. et al. Effect of N addition on root exudation and associated microbial N transformation under Sibiraea angustata in an alpine shrubland. Plant Soil 460, 469–481 (2021). https://doi.org/10.1007/s11104-020-04753-4

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