Skip to main content
SpringerLink
Log in

Priming effect of litter mineralization: the role of root exudate depends on its interactions with litter quality and soil condition

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Root exudation can prime microbial synthesis of additional exoenzymes and consequently accelerate organic carbon (C) and nitrogen (N) mineralization. Such exudate induced priming effect (EPE) has been hypothesized to depend on exudate rate and stoichiometry. Little is known about how EPE would affect litter decomposition. We employed a microcosm experiment to evaluate the influence of root exudate on litter nutrient release and microbial enzyme functions.

Methods

Leaf litters of Pinus massoniana, Quercus variabilis and Robinia pseudoacacia were incubated under two soil conditions (fertile versus barren). Solutions of chemicals often found in root exudates with contrasting C:N ratios were inoculated frequently into the microcosms to simulate exudation. By comparing with a water control, exudate effect was determined.

Results

In barren soils, exudates with C:N ratio of 10 significantly decelerated C loss of R. pseudoacacia, all N-containing exudates significantly enhanced the N-cycling related enzymes in decomposing Q. variabilis, while C-only exudate accelerated N loss of P. massoniana. In fertile soils, C-only exudate promoted the N-cycling related enzymes in decomposing R. pseudoacacia.

Conclusions

A stoichiometric C:N constraint on microbial utilization of exudates arose in decomposing recalcitrant litters in barren soil. EPE and its stoichiometric constraint depend on interactions with litter quality and soil condition. The findings arouse the consequences of exudate rate and stoichiometry changes in determining soil nutrient balance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, Heidelberg, pp 229–243

    Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98

    Article  CAS  PubMed  Google Scholar 

  • Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD (2014) Rhizosphere stoichiometry: are C : N : P ratios of plants, soils, and enzymes conserved at the plant species-level. New Phytol 201:505–517

    Article  CAS  PubMed  Google Scholar 

  • Bengtson P, Barker J, Grayston SJ (2012) Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects. Ecol Evol 2:1843–1852

    Article  PubMed  PubMed Central  Google Scholar 

  • Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131

    Article  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211

    Article  CAS  Google Scholar 

  • Bonanomi G, Cesarano G, Gaglione SA, Ippolito F, Sarker T, Rao MA (2017) Soil fertility promotes decomposition rate of nutrient poor, but not nutrient rich litter through nitrogen transfer. Plant Soil 412:397–411

    Article  CAS  Google Scholar 

  • Bowen GD (1969) Nutrient status effects on loss of amides and amino acids from pine roots. Plant Soil 30:139–142

    Article  CAS  Google Scholar 

  • Bradford MA, Fierer N, Reynolds JF (2008) Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–974

    Article  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  CAS  Google Scholar 

  • Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644

    Article  CAS  Google Scholar 

  • Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157

    Article  PubMed  PubMed Central  Google Scholar 

  • Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365

    Article  Google Scholar 

  • Chen RR, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Lin XG, Blagodatskaya E, Kuzyakov Y (2014) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Chang Biol 20:2356–2367

    Article  PubMed  Google Scholar 

  • Cheng W (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801

    Article  CAS  Google Scholar 

  • Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071

    Article  PubMed  Google Scholar 

  • Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113

    Article  PubMed  Google Scholar 

  • De Nobili M, Contin M, Mondini C, Brookes PC (2001) Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol Biochem 33:1163–1170

    Article  Google Scholar 

  • 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 

  • Dorodnikov M, Blagodatskaya E, Blagodatsky S, Marhan S, Fangmeier A, Kuzyakov Y (2009) Stimulation of microbial extracellular enzyme activities by elevated CO2 depends on soil aggregate size. Glob Chang Biol 15:1603–1614

    Article  Google Scholar 

  • Drake JE, Darby BA, Giasson MA, Kramer MA, Phillips RP, Finzi AC (2013) Stoichiometry constrains microbial response to root exudation-insights from a model and a field experiment in a temperate forest. Biogeosciences 10:821–838

    Article  CAS  Google Scholar 

  • Fanin N, Fromin N, Buatois B, Hättenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecol Lett 16:764–772

    Article  PubMed  Google Scholar 

  • Fanin N, Fromin N, Bertrand I (2016) Functional breadth and home-field advantage generate functional differences among soil microbial decomposers. Ecology 97:1023–1037

    PubMed  Google Scholar 

  • Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094

    Article  PubMed  Google Scholar 

  • Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  CAS  Google Scholar 

  • Freschet GT, Aerts R, Cornelissen JHC (2012) A plant economics spectrum of litter decomposability. Funct Ecol 26:56–65

    Article  Google Scholar 

  • Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171

    Article  Google Scholar 

  • Frost PC, Benstead JP, Cross WF, Hillebrand H, Larson JH, Xenopoulos MA, Yoshida T (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779

    Article  PubMed  Google Scholar 

  • Gholz HL, Wedin DA, Smitherman SM, Harmon ME, Parton WJ (2000) Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Glob Chang Biol 6:751–765

    Article  Google Scholar 

  • Guyonnet JP, Vautrin F, Meiffren G, Labois C, Cantarel AAM, Michalet S, Comte G, Haichar FZ (2017) The effects of plant nutritional strategy on soil microbial denitrification activity through rhizosphere primary metabolites. FEMS Microbiol Ecol 93:fix022

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hall EK, Maixner F, Franklin O, Daims H, Richter A, Battin T (2011) Linking microbial and ecosystem ecology using ecological stoichiometry: a synthesis of conceptual and empirical approaches. Ecosystems 14:261–273

    Article  Google Scholar 

  • Hamer U, Marschner B (2005) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol Biochem 37:445–454

    Article  CAS  Google Scholar 

  • He ZL, Xiong JB, Kent AD, Deng Y, Xue K, Wang GJ, Wu LY, Van Nostrand JD, Zhou JZ (2014) Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem. ISME J 8:714–726

    Article  CAS  PubMed  Google Scholar 

  • Hessen DO, Agren GI, Anderson TR, Elser JJ, De Ruiter PC (2004) Carbon, sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192

    Article  Google Scholar 

  • Hobbie SE, Reich PB, Oleksyn J, Ogdahl M, Zytkowiak R, Hale C, Karolewski P (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297

    Article  PubMed  Google Scholar 

  • Hopkins F, Gonzalez-Meler MA, Flower CE, Lynch DJ, Czimczik C, Tang JW, Subke JA (2013) Ecosystem-level controls on root-rhizosphere respiration. New Phytol 199:339–351

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, van der Heijden MGA, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33

    Article  CAS  Google Scholar 

  • Keiser AD, Keiser DA, Strickland MS, Bradford MA (2014) Disentangling the mechanisms underlying functional differences among decomposer communities. J Ecol 102:603–609

    Article  Google Scholar 

  • Koenker R (2012) quantreg: Quantile regression in R. R package version 5.5. https://CRAN.R-project.org/package=quantreg. Accessed 7 Jan 2016

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

    Article  CAS  Google Scholar 

  • Langley JA, McKinley DC, Wolf AA, Hungate BA, Drake BG, Megonigal JP (2009) Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem exposed to elevated CO2. Soil Biol Biochem 41:54–60

    Article  CAS  Google Scholar 

  • Manzoni S, Porporato A (2009) Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biol Biochem 41:1355–1379

    Article  CAS  Google Scholar 

  • Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91

    Article  CAS  PubMed  Google Scholar 

  • Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  PubMed  Google Scholar 

  • Nottingham AT, Turner BL, Winter K, Chamberlain PM, Stott A, Tanner EVJ (2013) Root and arbuscular mycorrhizal mycelial interactions with soil microorganisms in lowland tropical forest. FEMS Microbiol Ecol 85:37–50

    Article  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: Community ecology package. R package version 20.10. http://CRAN.R-project.org/package=vegan. Accessed 7 Jan 2016

  • Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331

    Article  Google Scholar 

  • Osono T, Takeda H (2002) Comparison of litter decomposing ability among diverse fungi in a cool temperate deciduous forest in Japan. Mycologia 94:421–427

    Article  CAS  PubMed  Google Scholar 

  • Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC, Fasth B (2007) Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315:361–364

    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 umigation. Ecol Lett 14:187–194

    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 15:1042–1049

    Article  PubMed  Google Scholar 

  • Purahong W, Schloter M, Pecyna MJ, Kapturska D, Daumlich V, Mital S, Buscot F, Hofrichter M, Gutknecht JLM, Kruger D (2014) Uncoupling of microbial community structure and function in decomposing litter across beech forest ecosystems in Central Europe. Sci Rep 4:7014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R version 3.2.3. R Foundation for Statistical Computing, Vienna. http://CRAN.R-project.org/. Accessed 7 Jan 2016

  • Ross DJ, Grayston SJ, Whitehead D (2006) Changes in soil carbon and nitrogen properties and microbial communities in relation to growth of Pinus radiata and Nothofagus fusca trees after 6 years at ambient and elevated atmospheric CO2. Glob Chang Biol 12:1690–1706

    Article  Google Scholar 

  • Rousk K, Michelsen A, Rousk J (2016) Microbial control of soil organic matter mineralization responses to labile carbon in subarctic climate change treatments. Glob Chang Biol 22:4150–4161

    Article  PubMed  Google Scholar 

  • Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57

    Article  CAS  Google Scholar 

  • Sanchez-Carrillo S, Alvarez-Cobelas M, Angeler DG, Serrno-Grijalva L, Sanchez- Andres R, Cirujano S, Schmid T (2018) Elevated atmospheric CO2 increases root exudation of carbon in wetlands: results from the first free-air CO2 enrichment facility (FACE) in a marshland. Ecosystems 21:852–867

    Article  CAS  Google Scholar 

  • Sayer EJ, Tanner EVJ, Cheesman AW (2006) Increased litterfall changes fine root distribution in a moist tropical forest. Plant Soil 281:5–13

    Article  CAS  Google Scholar 

  • Schimel DS (1995) Terrestrial ecosystems and the carbon-cycle. Glob Chang Biol 1:77–91

    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 35:549–563

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Moorhead DL (1994) Resource-allocation to extracellular enzyme-production - a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311

    Article  Google Scholar 

  • Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331

    Article  CAS  Google Scholar 

  • Staddon PL, Reinsch S, Olsson PA, Ambus P, Luscher A, Jakobsen I (2014) A decade of free-air CO2 enrichment increased the carbon throughput in a grass-clover ecosystem but did not drastically change carbon allocation patterns. Funct Ecol 28:538–545

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press

  • Subke JA, Hahn V, Battipaglia G, Linder S, Buchmann N, Cotrufo MF (2004) Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139:551–559

    Article  PubMed  Google Scholar 

  • Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Univ of California Press

  • van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev 37:477–494

    Article  CAS  PubMed  Google Scholar 

  • von Stockar U, Maskow T, Liu JS, Marison IW, Patino R (2006) Thermodynamics of microbial growth and metabolism: an analysis of the current situation. J Biotechnol 121:517–533

    Article  CAS  Google Scholar 

  • Wang FC, Fang XM, Ding ZQ, Wan SZ, Chen FS (2016) Effects of understory plant root growth into the litter layer on the leaf litter decomposition of two woody species in a subtropical forest. For Ecol Manag 364:39–45

    Article  Google Scholar 

  • Wickings K, Grandy AS, Reed SC, Cleveland CC (2012) The origin of litter chemical complexity during decomposition. Ecol Lett 15:1180–1188

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Elizabeth Tokarz at the Yale University for her assistance with English language and grammatical editing of this manuscript. This work was supported by the National Key Research and Development Program of the Ministry of Science and Technology of China (No. 2016YFD0600204); the State Key Program of National Natural Science Foundation of China (No. 31530007); the Sanxin Forestry Project in Jiangsu Province (No. LYSX[2016]46); the specimen platform of China and the teaching specimens sub-platform (2005DKA21403-JK); the specimen platform of China, and the teaching specimens sub-platform (2005DKA21400); the Water Conservancy Science and Technology Project of Jiangsu Province (2018063); and the National Natural Science Foundation of China (31870598).

Author information

Authors and Affiliations

  1. School of Life Sciences, Nanjing University, Nanjing, 210023, People’s Republic of China

    Kai Tian, Xiangshi Kong, Liuhuan Yuan, Hong Lin, Zaihua He, Bei Yao, Yanli Ji, Junbo Yang, Shucun Sun & Xingjun Tian

  2. Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, 210037, People’s Republic of China

    Xingjun Tian

Authors
  1. Kai Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiangshi Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liuhuan Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zaihua He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bei Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanli Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junbo Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shucun Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xingjun Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xingjun Tian.

Additional information

Responsible Editor: Zucong Cai.

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 562 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tian, K., Kong, X., Yuan, L. et al. Priming effect of litter mineralization: the role of root exudate depends on its interactions with litter quality and soil condition. Plant Soil 440, 457–471 (2019). https://doi.org/10.1007/s11104-019-04070-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04070-5

Keywords

Search

Navigation