Plant and Soil

, Volume 409, Issue 1–2, pp 87–97 | Cite as

Maize rhizosphere priming: field estimates using 13C natural abundance

  • Amit KumarEmail author
  • Yakov Kuzyakov
  • Johanna Pausch
Regular Article



Root-mediated changes in soil organic matter (SOM) decomposition, termed rhizosphere priming effects (RPE), play crucial roles in the global carbon (C) cycle, but their mechanisms and field relevance remain ambiguous. We hypothesize that nitrogen (N) shortages may intensify SOM decomposition in the rhizosphere because of increase of fine roots and rhizodeposition.


RPE and their dependence on N-fertilization were studied using a C3-to-C4 vegetation change. N-fertilized and unfertilized soil cores, with and without maize, were incubated in the field for 50 days. Soil CO2 efflux was measured, partitioned for SOM- and root-derived CO2, and RPE was calculated. Plant biomass, microbial biomass C (MBC) and N (MBN), and enzyme activities (β-1,4-glucosidase; N-acetylglucosaminidase; L-leucine aminopeptidase) were analyzed.


Roots enhanced SOM mineralization by 35 % and 126 % with and without N, respectively. This was accompanied by higher specific root-derived CO2 in unfertilized soils. MBC, MBN and enzyme activities increased in planted soils, indicating microbial activation, causing positive RPE. N-fertilization had minor effects on MBC and MBN, but it reduced β-1,4-glucosidase and L-leucine aminopeptidase activities under maize through lower root-exudation. In contrast, N-acetylglucosaminidase activity increased with N-fertilization in planted and unplanted soils.


This study showed the field relevance of RPE and confirmed that, despite higher root biomass, N availability reduces RPE by lowering root and microbial activity.


C3/C4 vegetation change Soil CO2 SOM decomposition Enzyme activities Microbial biomass N-fertilization 



The authors thank Thomas Splettstößer and Yue Sun for field assistance and Dirk Böttger for his help in constructing the closed-circulation system. We also would like to thank Karin Schmidt and Anita Kriegel for laboratory assistance and Reinhard Langel at the Center for Stable Isotope Research Analysis (KOSI) at the University of Göttingen for isotopic analyses. We gratefully acknowledge the German Academic Exchange Service (DAAD) for a scholarship award to Amit Kumar. This study was supported by the German Research Foundation (DFG) within project PA 2377/1-1.


  1. Ai C, Liang G, Sun J, Wang X, Zhou W (2012) Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma 173-174:330–338. doi: 10.1016/j.geoderma.2011.07.020 CrossRefGoogle Scholar
  2. Balesdent J, Mariotti A (1996) Measurement of soil organic matter turnover using 13C natural abundace. In: Boutton TW, Yamasaki S (eds) Mass Spectrometery of soils. Marcel Dekker, New York, pp. 83–111Google Scholar
  3. Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660. doi: 10.1046/j.1365-2435.1999.00362.x CrossRefGoogle Scholar
  4. Chen R, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Lin X, 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. doi: 10.1111/gcb.12475 CrossRefPubMedGoogle Scholar
  5. Cheng W, Kuzyakov Y (2005) Root effects on soil organic matter decomposition. Agronomy:119–144. doi: 10.2134/agronmonogr48.c7
  6. 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. doi: 10.1111/nph.12440 CrossRefPubMedGoogle Scholar
  7. Coleman DC, Odum EP, Crossley DAJ (1992) Soil biology, soil ecology, and global change. Biol Fertil Soils 14:104–111CrossRefGoogle Scholar
  8. Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113. doi: 10.1890/06-1847.1 CrossRefPubMedGoogle Scholar
  9. De Nobili M, Contin M, Mondini C, Brookes P (2001) Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol Biochem 33:1163–1170. doi: 10.1016/S0038-0717(01)00020-7 CrossRefGoogle Scholar
  10. Dijkstra FA, Cheng W, Johnson DW (2006) Plant biomass influences rhizosphere priming effects on soil organic matter decomposition in two differently managed soils. Soil Biol Biochem 38:2519–2526. doi: 10.1016/j.soilbio.2006.02.020 CrossRefGoogle Scholar
  11. Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:1–8. doi: 10.3389/fmicb.2013.00216 CrossRefGoogle Scholar
  12. Dormaar JF (1990) Effect of active roots on the decomposition of soil organic materials. Biol Fertil Soils 10:121–126. doi: 10.1007/bf00336247 Google Scholar
  13. Drake JE, Darby BA, Giasson M-A, 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. doi: 10.5194/bg-10-821-2013 CrossRefGoogle Scholar
  14. 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. doi: 10.1111/gcb.12816 CrossRefPubMedGoogle Scholar
  15. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843. doi: 10.1016/S0038-0717(03)00123-8 CrossRefGoogle Scholar
  16. Fontaine S, Barot S, Barré P, et al. (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280. doi: 10.1038/nature06275 CrossRefPubMedGoogle Scholar
  17. Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revallot 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. doi: 10.1016/j.soilbio.2010.09.017 CrossRefGoogle Scholar
  18. Fu SL, Cheng WX, Susfalk R (2002) Rhizosphere respiration varies with plant species and phenology: a greenhouse pot experiment. Plant Soil 239:133–140. doi: 10.1023/a:1014959701396 CrossRefGoogle Scholar
  19. Hodge A, Grayston SJ, Ord BG (1996) A novel method for characterisation and quantification of plant root exudates. Plant Soil 184:97–104. doi: 10.1007/BF00029278 CrossRefGoogle Scholar
  20. Joergensen RG, Mueller T (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEN value. Soil Biol Biochem 28:33–37. doi: 10.1016/0038-0717(95)00101-8 CrossRefGoogle Scholar
  21. Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12:1–15. doi: 10.1007/s10021-008-9199-z CrossRefGoogle Scholar
  22. Koch O, Tscherko D, Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Glob Biogeochem Cycles 21:1–11. doi: 10.1029/2007GB002983 CrossRefGoogle Scholar
  23. Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322. doi: 10.1016/0038-0717(84)90025-7 CrossRefGoogle Scholar
  24. Kuikman PJ, Jansen AG, Van Veen JA, Zehnder AJB (1990) Protozoan predation and the turnover of soil organic carbon and nitrogen in the presence of plants. Biol Fertil Soils 10:22–28CrossRefGoogle Scholar
  25. Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci Fur Pflanzenernahrung Und Bodenkd 165:382–396. doi: 10.1002/1522-2624(200208)165:4<382::AID-JPLN382>3.0.CO;2-# CrossRefGoogle Scholar
  26. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371. doi: 10.1016/j.soilbio.2010.04.003 CrossRefGoogle Scholar
  27. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199. doi: 10.1016/j.soilbio.2015.01.025 CrossRefGoogle Scholar
  28. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review Zeitschrift für Pflanzenernährung und Bodenkd 163:421–431. doi: 10.1002/1522-2624(200008)163:4<421::aid-jpln421>;2-r CrossRefGoogle Scholar
  29. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669. doi: 10.1111/nph.12235 CrossRefPubMedGoogle Scholar
  30. Kuzyakov Y, Hill PW, Jones DL (2007) Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant Soil 290:293–305. doi: 10.1007/s11104-006-9162-8 CrossRefGoogle Scholar
  31. Lal R (2011) Sequestering carbon in soils of agro-ecosystems. Food Policy 36:S33–S39. doi: 10.1016/j.foodpol.2010.12.001 CrossRefGoogle Scholar
  32. Liljeroth E, Van Veen JA, Miller HJ (1990) Assimilate translocation to the rhizosphere of two wheat lines and subsequent utilization by rhizosphere microorganisms at two soil nitrogen concentrations. Soil Biol Biochem 22:1015–1022CrossRefGoogle Scholar
  33. Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016) Substrate quality affects kinetics and catalytic efficiency of exo-enzymes in rhizosphere and detritusphere. Soil Biol Biochem 92:111–118. doi: 10.1016/j.soilbio.2015.09.020 CrossRefGoogle Scholar
  34. Marx MC, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640. doi: 10.1016/S0038-0717(01)00079-7 CrossRefGoogle Scholar
  35. Marx MC, Kandeler E, Wood M, et al. (2005) Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particle-size fractions. Soil Biol Biochem 37:35–48. doi: 10.1016/j.soilbio.2004.05.024 CrossRefGoogle Scholar
  36. Meier IC, Pritchard SG, Brzostek ER, McCormack ML, Phillips RP (2015) The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. New Phytol 2:1164–1174. doi: 10.1111/nph.13122 CrossRefGoogle Scholar
  37. Merckx R, Dijkstra A, den Hartog A, Van Veen JA (1987) Production of root-derived material and associated microbial growth in soil at different nutrient levels. Biol Fertil Soils 5:126–132. doi: 10.1007/BF00257647 CrossRefGoogle Scholar
  38. Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141. doi: 10.1016/j.soilbio.2012.05.011 CrossRefGoogle Scholar
  39. Mwafulirwa L, Baggs EM, Russell J, George T, Morley N, Sim A, Canto CF, Paterson E (2016) Barley genotype influences stabilization of rhizodeposition-derived C and soil organic matter mineralization. Soil Biol Biochem 95:60–69. doi: 10.1016/j.soilbio.2015.12.011 CrossRefGoogle Scholar
  40. Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In Pinton R (ed) The Rhizosphere: biochemistry and organic substances at the soil- plant interface, 2nd edn. CRC Press, Boca Raton, Fla, pp 23–72Google Scholar
  41. Paterson E, Sim A (1999) Rhizodeposition and C-partitioning of Lolium perenne in axenic culture affected by nitrogen supply and defoliation. Plant Soil 216:155–164. doi: 10.1023/a:1004789407065 CrossRefGoogle Scholar
  42. Paterson E, Sim A (2013) Soil-specific response functions of organic matter mineralization to the availability of labile carbon. Glob Chang Biol 19:1562–1571. doi: 10.1111/gcb.12140 CrossRefPubMedGoogle Scholar
  43. Paul EA, Clark FE (1996) Soil microbiology and biochemistry, 2nd edn. Academic Press, San Diego, CA, p 340Google Scholar
  44. Pausch J, Tian J, Riederer M, Kuzyakov Y (2013a) Estimation of rhizodeposition at field scale: upscaling of a 14C labeling study. Plant Soil 364:273–285. doi: 10.1007/s11104-012-1363-8 CrossRefGoogle Scholar
  45. Pausch J, Zhu B, Kuzyakov Y, Cheng W (2013b) Plant inter-species effects on rhizosphere priming of soil organic matter decomposition. Soil Biol Biochem 57:91–99. doi: 10.1016/j.soilbio.2012.08.029 CrossRefGoogle Scholar
  46. 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 14:187–194. doi: 10.1111/j.1461-0248.2010.01570.x CrossRefPubMedGoogle Scholar
  47. Ratnayake M, Leonard R, Menge J (1978) Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal formation. New Phytol 81:543–552. doi: 10.1111/j.1469-8137.1978.tb01627.x CrossRefGoogle Scholar
  48. Razavi BS, Blagodatskaya E, Kuzyakov Y (2015) Nonlinear temperature sensitivity of enzyme kinetics explains canceling effect—a case study on loamy haplic Luvisol. Front Microbiol. doi: 10.3389/fmicb.2015.01126 PubMedPubMedCentralGoogle Scholar
  49. Reid JB, Goss MJ (1982) Suppression of decomposition of 14C-labelled plant roots in the presence of living roots of maize and perennial ryegrass. J Soil Sci 33:387–395. doi: 10.1111/j.1365-2389.1982.tb01775.x CrossRefGoogle Scholar
  50. Sinsabaugh RL (1994) Enzymic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74. doi: 10.1007/BF00418675 CrossRefGoogle Scholar
  51. Sinsabaugh RL, Shah JJF (2012) Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 102:31–43. doi: 10.1007/s10533-010-9482-x CrossRefGoogle Scholar
  52. Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331. doi: 10.2307/1934820 CrossRefGoogle Scholar
  53. Smith P (2012) Agricultural greenhouse gas mitigation potential globally, in Europe and in the UK: what have we learnt in the last 20 years? Glob Chang Biol 18:35–43. doi: 10.1111/j.1365-2486.2011.02517.x CrossRefGoogle Scholar
  54. Smith P, Haberl H, Popp A, Erb KH, Lauk C, Harper R, Tubiello FN, Pinto ADS, Jafari M, Sohi S, Masera M, Böttcher H, Berndes G, Bustamante M, Ahammad H, Clark H, Dong H, Elsiddig EA, Mbow C, Ravindranath NH, Rice CW, Adab CR, Romanovskaya A, Sperling F, Herrero M, House JI, Rose S (2013) How much land-based greenhouse gas mitigation can be achieved without compromising food security and environmental goals? Glob Chang Biol 19:2285–2302. doi: 10.1111/gcb.12160 CrossRefPubMedGoogle Scholar
  55. Sparling GP, Cheshire MV, Mundie CM (1982) Effect of barley plants on the decomposition of 14C-labelled soil organic matter. J Soil Sci 33:89–100. doi: 10.1111/j.1365-2389.1982.tb01750.x CrossRefGoogle Scholar
  56. Stemmer M, Gerzabek MH, Kandeler E (1998) Invertase and xylanase activity of bulk soil and particle-size fractions during maize straw decomposition. Soil Biol Biochem 31:9–18. doi: 10.1016/S0038-0717(98)00083-2 CrossRefGoogle Scholar
  57. Stewart BJ, Leatherwood JM (1976) Derepressed synthesis of cellulase by Cellulomonas. J Bacteriol 128:609–615PubMedPubMedCentralGoogle Scholar
  58. Turner BL, Hopkins DW, Haygarth PM, Ostle N (2002) Glucosidase activity in pasture soils. Appl Soil Ecol 20:157–162. doi: 10.1016/S0929-1393(02)00020-3 CrossRefGoogle Scholar
  59. Van Veen JA, Merckx R, Van De Geijn SC (1989) Plant and soil related controls of the flow of carbon from roots through the soil microbial biomass. Plant Soil 115:179–188. doi: 10.1007/BF02202586 CrossRefGoogle Scholar
  60. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. doi: 10.1016/0038-0717(87)90052-6 CrossRefGoogle Scholar
  61. 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 33:1291–1303. doi: 10.1016/S0038-0717(01)00033-5 CrossRefGoogle Scholar
  62. Weand MP, Arthur MA, Lovett GM, McCulley RL, Weathers KC (2010) Effects of tree species and N additions on forest floor microbial communities and extracellular enzyme activities. Soil Biol Biochem 42:2161–2173. doi: 10.1016/j.soilbio.2010.08.012 CrossRefGoogle Scholar
  63. Werth M, Kuzyakov Y (2010) 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partioning studies. Soil Biol Biochem 42:1372–1384. doi: 10.1016/j.soilbio.2010.04.009 CrossRefGoogle Scholar
  64. Wutzler T, Reichstein M (2013) Priming and substrate quality interactions in soil organic matter models. Biogeosciences 10:2089–2103. doi: 10.5194/bg-10-2089-2013 CrossRefGoogle Scholar
  65. 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 Chang Biol 19:2158–2167. doi: 10.1111/gcb.12161 CrossRefPubMedGoogle Scholar
  66. Zhu B, Cheng W (2012) Nodulated soybean enhances rhizosphere priming effects on soil organic matter decomposition more than non-nodulated soybean. Soil Biol Biochem 51:56–65. doi: 10.1016/j.soilbio.2012.04.016 CrossRefGoogle Scholar
  67. Zhu B, Gutknecht JLM, Herman DJ, Keck DC, Firestone MK, Cheng W (2014) Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol Biochem 76:183–192. doi: 10.1016/j.soilbio.2014.04.033 CrossRefGoogle Scholar
  68. Zhu B, Panke-Buisse K, Kao-Kniffin J (2015) Nitrogen fertilization has minimal influence on rhizosphere effects of smooth crabgrass (Digitaria ischaemum) and bermudagrass (Cynodon dactylon). J Plant Ecol 8:390–400. doi: 10.1093/jpe/rtu034 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Agricultural Soil ScienceGeorg-August University of GöttingenGöttingenGermany
  2. 2.Department of Soil Science of Temperate EcosystemsGeorg-August University of GöttingenGöttingenGermany

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