Skip to main content
SpringerLink
Log in

Subsoil biogeochemical properties induce shifts in carbon allocation pattern and soil C dynamics in wheat

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

Abstract

Aims

Microbial turnover processes are typically restricted by low substrate availability in the subsoil. We hypothesized that SOM decomposition increases with plant density and decreases with N fertilization: We expected a greater rate of C allocation to the rhizosphere in the topsoil than in the subsoil treatments.

Methods

In order to simulate different degrees of rhizodeposition, wheat was planted in pots at four different densities. The plants were continuously labeled with 13C-depleted CO2. Soil CO2 efflux was partitioned for root- and SOM-derived CO2. Moreover, we determined the enzyme kinetics by measuring catalytic efficiency and enzyme stoichiometry in both topsoil and subsoil.

Results

Shoot biomass and the shoot to root ratio were significantly higher for plants grown in the topsoil compared with the subsoil, which demonstrated higher relative C allocation to root biomass in the subsoil treatment. Despite the similar size of the rhizosphere, root-derived CO2 was always higher in the topsoil compared with the subsoil treatment, indicating enhanced root exudation. Effect sizes of all enzyme activities showed stronger magnitudes for the subsoil treatments. This was in line with a two-times increase of the effect size of SOM decomposition in the subsoil relative to topsoil.

Conclusions

Overall, the plants in the subsoil treatments allocated more C to root biomass, less C to shoot biomass, and substantially less C to root exudates. However, the effect sizes of both SOM decomposition and enzyme activities were higher in the subsoil than in the topsoil, reflecting a stronger sensitivity to C inputs.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allison, S. D., Weintraub, M. N., Gartner, T. B., & Waldrop, M. P. (2010). Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In Soil enzymology (pp. 229-243). Springer, Berlin, Heidelberg.

  • Bahn M, Lattanzi FA, Hasibeder R, Wild B, Koranda M, Danese V, Brüggemann N, Schmitt M, Siegwolf R, Richter A (2013) Responses of belowground carbon allocation dynamics to extended shading in mountain grassland. New Phytol 198(1):116–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banfield CC, Dippold MA, Pausch J, Hoang DT, Kuzyakov Y (2017) Biopore history determines the microbial community composition in subsoil hotspots. Biol Fertil Soils 53(5):573–588

    Article  CAS  Google Scholar 

  • Barraclough PB (1984) The growth and activity of winter wheat roots in the field: root growth of high-yielding crops in relation to shoot growth. J Agric Sci 103(2):439–442

    Article  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 

  • Bending GD, Turner MK, Rayns F, Marx MC, Wood M (2004) Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biol Biochem 36(11):1785–1792

    Article  CAS  Google Scholar 

  • Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2009) Contrasting effects of glucose, living roots and maize straw on microbial growth kinetics and substrate availability in soil. Eur J Soil Sci 60(2):186–197

    Article  CAS  Google Scholar 

  • Brouwer R (1983) Functional equilibrium: sense or nonsense? Neitherlands J Agric Sci 31:335–348

    Google Scholar 

  • Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14(5):423–427

    Article  CAS  Google Scholar 

  • Cheng W, Dijkstra FA (2007) Theoretical proof and empirical confirmation of a continuous labeling method using naturally 13C-depleted carbon dioxide. J Integr Plant Biol 49(3):401–407

    Article  CAS  Google Scholar 

  • Cheng W, Gershenson A (2007) Carbon fluxes in the rhizosphere. Rhizosphere:31–56

  • Cheng W, Johnson DW, Fu S (2003) Rhizosphere effects on decomposition. Soil Sci Soc Am J 67(5):1418–1427

    Article  CAS  Google Scholar 

  • Cornish-Bowden A (1995) Introduction to the enzyme kinetics. In: Fundamentals of enzyme kinetics. Portland Press Limited, Portland, pp 243–252

    Google Scholar 

  • De Cesare, F., Garzillo, A. M. V., Buonocore, V., & Badalucco, L. (2000). Use of sonication for measuring acid phosphatase activity in soil. Soil Biology and Biochemistry, 32(6), 825-832.

  • Eilers KG, Debenport S, Anderson S, Fierer N (2012) Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem 50:58–65

    Article  CAS  Google Scholar 

  • El-Sharkawy MA, Cock JH, Lynam JK, del Pilar Hernàndez A, Cadavid LFZ (1990) Relationships between biomass, root-yield and single-leaf photosynthesis in field-grown cassava. Field Crop Res 25(3–4):183–201

    Article  Google Scholar 

  • Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450(7167):277–280

    Article  CAS  PubMed  Google Scholar 

  • Farrar, J. F., & Jones, D. L. (2000). The control of carbon acquisition by roots. The New Phytologist, 147(1), 43-53.

  • Gavrichkova O, Kuzyakov Y (2017) The above-belowground coupling of the C cycle: fast and slow mechanisms of C transfer for root and rhizomicrobial respiration. Plant Soil 410(1–2):73–85

    Article  CAS  Google Scholar 

  • Gavrichkova O, Moscatelli MC, Kuzyakov Y, Grego S, Valentini R (2010) Influence of defoliation on CO2 efflux from soil and microbial activity in a Mediterranean grassland. Agric Ecosyst Environ 136(1–2):87–96

    Article  CAS  Google Scholar 

  • Gianfreda LA, De Cristofaro A, Rao MA, Violante A (1995) Kinetic behavior of synthetic organo- and organo-mineral-urease complexes. J Soil Sci Soc Am 59:811–815

    Article  CAS  Google Scholar 

  • Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science? Eur J Soil Sci 57(1):2–12

    Article  Google Scholar 

  • Guenet B, Juarez S, Bardoux G, Abbadie L, Chenu C (2012) Evidence that stable C is as vulnerable to priming effect as is more labile C in soil. Soil Biol Biochem 52:43–48

    Article  CAS  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST-palaeontological statistics, ver. 1.89. Palaeontol Electron 4(1):1–9

    Google Scholar 

  • Harris D, Porter LK, Paul EA (1997) Continuous flow isotope ratio mass spectrometry of carbon dioxide trapped as strontium carbonate. Commun Soil Sci Plant Anal 28(9–10):747–757

    Article  CAS  Google Scholar 

  • Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129

    Article  CAS  Google Scholar 

  • Hill BH, Elonen CM, Jica TM, Kolka RK, Lehto LLP, Sebestyen SD, Siefert-Monson LR (2014) Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120:203e224

    Article  CAS  Google Scholar 

  • Hirte J, Leifeld J, Abiven S, Oberholzer HR, Mayer J (2018) Below ground carbon inputs to soil via root biomass and rhizodeposition of field-grown maize and wheat at harvest are independent of net primary productivity. Agric Ecosyst Environ 265:556–566

    Article  Google Scholar 

  • Hoberg E, Marschner P, Lieberei R (2001) Pflanze-Bakterien-Interaktionen bei Phosphatmangel in Sterilkultur. In: Physiologie und Funktion von Pflanzenwurzeln. Vieweg+ Teubner Verlag, pp 64–69

  • Huo C, Luo Y, Cheng W (2017) Rhizosphere priming effect: a meta-analysis. Soil Biol Biochem 111:78–84

    Article  CAS  Google Scholar 

  • Jones DL, Magthab EA, Gleeson DB, Hill PW, Sánchez-Rodríguez AR, Roberts P, Ge T, Murphy DV (2018) Microbial competition for nitrogen and carbon is as intense in the subsoil as in the topsoil. Soil Biol Biochem 117:72–82

    Article  CAS  Google Scholar 

  • Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165(4):277–304

    Article  CAS  Google Scholar 

  • Kautz T, Amelung W, Ewert F, Gaiser T, Horn R, Jahn R et al (2013) Nutrient acquisition from arable subsoils in temperate climates: a review. Soil Biol Biochem 57:1003–1022

    Article  CAS  Google Scholar 

  • Keith H, Oades JM, Martin JK (1986) Input of carbon to soil from wheat plants. Soil Biol Biochem 18(4):445–449

    Article  CAS  Google Scholar 

  • Koshland DE (2002) The application and usefulness of the ratio kcat/Km. Bioorg Chem 30:211–213

    Article  CAS  PubMed  Google Scholar 

  • Kuzyakov Y, Cheng W (2001) Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biol Biochem 33(14):1915–1925

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Gavrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Chang Biol 16(12):3386–3406

    Article  Google Scholar 

  • Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198(3):656–669

    Article  CAS  PubMed  Google Scholar 

  • Larcher W (2003) Physiological plant ecology, 4th edn. Springer, Berlin

    Book  Google Scholar 

  • Liang Z, Olesen JE, Jensen JL, Elsgaard L (2019) Nutrient availability affects carbon turnover and microbial physiology differently in topsoil and subsoil under a temperate grassland. Geoderma 336:22–30

    Article  CAS  Google Scholar 

  • Loeppmann S, Semenov M, Blagodatskaya E, Kuzyakov Y (2016a) Substrate quality affects microbial-and enzyme activities in rooted soil. J Plant Nutr Soil Sci 179(1):39–47

    Article  CAS  Google Scholar 

  • Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016b) Enzyme properties down the soil profile-a matter of substrate quality in rhizosphere and detritusphere. Soil Biol Biochem 103:274–283

    Article  CAS  Google Scholar 

  • Loeppmann S, Semenov M, Kuzyakov Y, Blagodatskaya E (2018) Shift from dormancy to microbial growth revealed by RNA:DNA ratio. Ecol Indic 85:603–612

    Article  CAS  Google Scholar 

  • Lorenz K, Lal R (2005) The depth distribution of soil organic carbon in relation to land use and management and the potential of carbon sequestration in subsoil horizons. Adv Agron 88:35–66

    Article  CAS  Google Scholar 

  • Lützow MV, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions–a review. Eur J Soil Sci 57(4):426–445

    Article  CAS  Google Scholar 

  • Lynch JP (2007) Rhizoeconomics: the roots of shoot growth limitations. HortScience 42(5):1107–1109

    Article  Google Scholar 

  • Lynch JP, Wojciechowski T (2015) Opportunities and challenges in the subsoil: pathways to deeper rooted crops. J Exp Bot 66(8):2199–2210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marx MC, Kandeler E, Wood M, Wermbter N, Jarvis SC (2005) Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particle-size fractions. Soil Biol Biochem 37(1):35–48

    Article  CAS  Google Scholar 

  • Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme based decomposition models. Front Terrestrial Microbiol 4(223):1–12

    Google Scholar 

  • Moscatelli MC, Lagomarsino A, Garzillo AMV, Pignataro A, Grego S (2012) b-Glucosidase kinetic parameters as indicators of soil quality under conventional and organic cropping systems applying two analytical approaches. Ecol Indic 13(1):322–327

    Article  CAS  Google Scholar 

  • Motulsky HM, Brown RE (2006) Detecting outliers when fitting data with nonlinear regression e a new method based on robust nonlinear regression and the false discovery rate. BMC Bioinformatics 7:123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48(7):743–762

    Article  Google Scholar 

  • Ostle N, Ineson P, Benham D, Sleep D (2000) Carbon assimilation and turnover in grassland vegetation using an in situ 13CO2 pulse labelling system. Rapid Commun Mass Spectrom 14(15):1345–1350

    Article  CAS  PubMed  Google Scholar 

  • Panikov NS (1995) Microbial growth kinetics. Springer Science & Business Media

  • Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Eur J Soil Sci 54:741–750

    Article  Google Scholar 

  • Paudel BR, Udawatta RP, Anderson SH (2011) Agroforestry and grass buffer effects on soil quality parameters for grazed pasture and row-crop systems. Appl Soil Ecol 48(2):125–132

    Article  Google Scholar 

  • Pausch J, Kuzyakov Y (2012) Soil organic carbon decomposition from recently added and older sources estimated by δ13C values of CO2 and organic matter. Soil Biol Biochem 55:40–47

    Article  CAS  Google Scholar 

  • Pausch, J., Kuzyakov, Y., 2017. Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Global change biology

    Google Scholar 

  • Pausch J, Tian J, Riederer M, Kuzyakov Y (2013) Estimation of rhizodeposition at field scale: upscaling of a 14 C labeling study. Plant Soil 364(1–2):273–285

    Article  CAS  Google Scholar 

  • Pausch J, Loeppmann S, Kühnel A, Forbush K, Kuzyakov Y, Cheng W (2016) Rhizosphere priming of barley with and without root hairs. Soil Biol Biochem 100:74–82

    Article  CAS  Google Scholar 

  • Pinton R, Varanini Z, Nannipieri P (2007) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC press

  • Poeplau C, Kätterer T, Leblans NI, Sigurdsson BD (2017) Sensitivity of soil carbon fractions and their specific stabilization mechanisms to extreme soil warming in a subarctic grassland. Glob Chang Biol 23(3):1316–1327

    Article  PubMed  Google Scholar 

  • Prikryl Z, Vancura V (1980) Root exudates of plants VI. Wheat root exudation as dependant on growth, concentration gradient of exudates and the presence of bacteria. Plant Soil:57–69

  • Ramirez KS, Craine JM, Fierer N (2010) Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied. Soil Biol Biochem 42(12):2336–2338

    Article  CAS  Google Scholar 

  • Remus R, Augustin J (2016) Dynamic linking of 14C partitioning with shoot growth allows a precise determination of plant-derived C input to soil. Plant Soil 408(1–2):493–513

    Article  CAS  Google Scholar 

  • Rumpel C, Kögel-Knabner I (2011) Deep soil organic matter—a key but poorly understood component of terrestrial C cycle. Plant Soil 338(1–2):143–158

    Article  CAS  Google Scholar 

  • Rumpel C, Eusterhues K, Kögel-Knabner I (2004) Location and chemical composition of stabilized organic carbon in topsoil and subsoil horizons of two acid forest soils. Soil Biol Biochem 36(1):177–190

    Article  CAS  Google Scholar 

  • Schenk HJ, Jackson RB (2002) Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90(3):480–494

    Article  Google Scholar 

  • Salomé, C., Nunan, N., Pouteau, V., Lerch, T. Z., & Chenu, C. (2010). Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Global Change Biology, 16(1), 416-426.

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

    Article  Google Scholar 

  • Shahbaz M, Kumar A, Kuzyakov Y, Börjesson G, Blagodatskaya E (2018) Priming effects induced by glucose and decaying plant residues on SOM decomposition: a three-source 13 C/14 C partitioning study. Soil Biol Biochem 121:138–146

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462(7274):795–798

    Article  CAS  PubMed  Google Scholar 

  • Smith NG, Dukes JS (2013) Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2. Glob Chang Biol 19(1):45–63

    Article  PubMed  Google Scholar 

  • Tarkalson DD, Jolley VD, Robbins CW, Terry RE (1998) Mycorrhizal colonization and nutrition of wheat and sweet corn grown in manure-treated and untreated topsoil and subsoil. J Plant Nutr 21(9):1985–1999

    Article  CAS  Google Scholar 

  • Thornley JHM (1977) Growth, maintenance and respiration: a re-interpretation. Ann Bot 41(6):1191–1203

    Article  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418(6898):671–677

    Article  CAS  PubMed  Google Scholar 

  • Tückmantel T, Leuschner C, Preusser S, Kandeler E, Angst G, Mueller CW, Meier IC (2017) Root exudation patterns in a beech forest: dependence on soil depth, root morphology, and environment. Soil Biol Biochem 107:188–197

    Article  CAS  Google Scholar 

  • Van Dyk J, Pletschke B (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes—factors affecting enzymes, conversion and synergy. Biotechnol Adv 30(6):1458–1480

    Article  PubMed  CAS  Google Scholar 

  • Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass C. Soil biology and Biochemistry, 19(6), 703-707.

  • Wordell-Dietrich P, Don A, Helfrich M (2017) Controlling factors for the stability of subsoil carbon in a Dystric Cambisol. Geoderma 304:40–48

    Article  CAS  Google Scholar 

  • Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass-C by fumigation-extraction-an automated procedure. Soil Biol Biochem 22:167–169

    Article  Google Scholar 

  • Zang H, Blagodatskaya E, Wang J, Xu X, Kuzyakov Y (2017) Nitrogen fertilization increases rhizodeposits incorporation into microbial biomass and reduces soil organic matter losses. Biol Fertil Soils 53:419–429

    Article  CAS  Google Scholar 

  • Zhang X, Han X, Yu W, Wang P, Cheng W (2017) Priming effects on labile and stable soil organic carbon decomposition: pulse dynamics over two years. PLoS One 12(9):e0184978

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu B, Cheng W (2011) 13 C isotope fractionation during rhizosphere respiration of C 3 and C 4 plants. Plant Soil 342(1–2):277–287

    Article  CAS  Google Scholar 

  • Zhu, B., & Cheng, W. (2012). Nodulated soybean enhances rhizosphere priming effects on soil organic matter decomposition more than non-nodulated soybean. Soil Biology and Biochemistry, 51, 56-65.

Download references

Acknowledgments

We thank Susann Enzmann for the helping hand in the lab.

Funding

This study received funding from the Deutscher Akademischer Austauschdienst (DAAD) 57051794. Furthermore, this study also received funding from the H.W. Schaumann Stiftung.

Author information

Authors and Affiliations

  1. Biogeochemistry of Agroecosystems, Georg-August University, Goettingen, Germany

    Sebastian Loeppmann

  2. Institute of Plant Nutrition and Soil Science, Christian-Albrechts University, Rodewald Str. 4, 24118, Kiel, Germany

    Sebastian Loeppmann

  3. Department of Environmental Studies, University of California, Santa Cruz, Santa Cruz, CA, USA

    Kelsey Forbush & Weixin Cheng

  4. Agroecology, University of Bayreuth, Bayreuth, Germany

    Johanna Pausch

Authors
  1. Sebastian Loeppmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kelsey Forbush
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weixin Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Johanna Pausch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sebastian Loeppmann.

Additional information

Responsible Editor: Simon Jeffery.

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 1142 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Loeppmann, S., Forbush, K., Cheng, W. et al. Subsoil biogeochemical properties induce shifts in carbon allocation pattern and soil C dynamics in wheat. Plant Soil 442, 369–383 (2019). https://doi.org/10.1007/s11104-019-04204-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04204-9

Keywords

Search

Navigation