Skip to main content
SpringerLink
Log in

Determining the timepoint when 14C tracer accurately reflect photosynthate use in the plant-soil system

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

Abstract

Background and aims

Only the carbon (C) isotope pulse labeling approach can provide time-resolved data concerning the input and turnover of plant-derived C in the soil, which are urgently needed to improve the performance of terrestrial C cycle models. However, there is currently very limited information about the point in time after pulse labeling at which the distribution of tracer C accurately represents the usage of photosynthates in different components of the plant-soil system. This should be the case as soon as the tracer has disappeared from the mobile C pool due to respiration, incorporation into the structural C pool of shoot and root tissue and exudation into the soil (rhizodeposition).

Methods

Following \(^{14} {CO}_{2}\) pulse labeling in laboratory and outdoor experiments with spring rye, the 14C dilution rates of soluble fractions and different substances from the structural C pool of the shoot (molecular level), the release of labeled CO2 by belowground respiration (component level), and the 14C kinetics of shoot respiration and 14C remaining in the plant-soil-soil gas continuum (system level) were analyzed during different stages of plant development.

Results

At all three levels investigated, 14C kinetics indicated that the C tracer levels changed very little between 15 and 21 days after labeling. Results also showed increasing tracer depletion in the mobile C pool. Consequently, only 0.42 % and 0.06 % of all 14C was still available for shoot respiration 15 and 21 days after labeling, respectively.

Conclusions

The similarities between 14C tracer kinetics at the three investigated levels indicate that tracer disappearance from the mobile pool and distribution throughout the plant-soil system was nearly complete between 15 and 21 days after labeling. Therefore, this appears to be the point at which the pulse labeling approach provides sufficiently precise data concerning the use of C (assimilated during labeling) for root growth, rhizodeposition, root respiration and the microbial turnover of rhizodeposits.

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

Similar content being viewed by others

References

  • Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: A highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69. doi:10.1104/pp.110.167684

    Article  CAS  PubMed  Google Scholar 

  • Allen SE, Grimshaw HM, Parkinson JA, Quarmby C (1974) Chemical analysis of ecological materials. Black Well Scientific Publications, Oxford

    Google Scholar 

  • Bancal P, Triboi E (1993) Temperature effect on fructan oligomer contents and fructan-related enzyme-activities in stems of wheat (Triticum-aestivum L.) during grain filling. New Phytol 123:247–253

    Article  CAS  Google Scholar 

  • van Bel AJE, Hess PH (2008) Hexoses as phloem transport sugars: the end of a dogma? J Exp Bot 59:261–272

    Article  CAS  PubMed  Google Scholar 

  • Bihmidine S, Hunter CT, Johns CE, Koch KE, Braun DM (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front Plant Sci 4:177. doi:10.3389/fpls.2013.00177

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolinder M, Katterer T, Andren O, Parent L (2012) Estimating carbon inputs to soil in forage-based crop rotations and modeling the effects on soil carbon dynamics in a swedish long-term field experiment. Can J Soil Sci 92:821–833

    Article  Google Scholar 

  • Bolinder MA, Janzen HH, Gregorich EG, Angers DA, VandenBygaart AJ (2007) An approach for estimating net primary productivity and annual carbon inputs to soil for common agricultural crops in Canada. Agric Ecosyst Environ 118:29–42

    Article  Google Scholar 

  • Borrell AK, Incoll LD, Simpson RJ, Dalling MJ (1989) Partitioning of dry-matter and the deposition and use of stem reserves in a semi-dwarf wheat crop. Ann Bot 63:527–539

    Google Scholar 

  • Brüggemann N, Gessler A, Kayler Z, Keel S, Badeck F, Barthel M, Boeckx P, Buchmann N, Brugnoli E, Esperschütz J, Gavrichkova O, Ghashghaie J, Gomez-Casanovas N, Keitel C, Knohl A, Kuptz D, Palacio S, Salmon Y, Uchida Y, Bahn M (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences 8:3457–3489

    Article  Google Scholar 

  • Carbone MS, Trumbore SE (2007) Contribution of new photosynthetic assimilates to respiration by perennial grasses and shrubs: residence times and allocation patterns. New Phytol 176:124–135

    Article  CAS  PubMed  Google Scholar 

  • Carbone MS, Czimczik CI, McDuffee KE, Trumbore SE (2007) Allocation and residence time of photosynthetic products in a boreal forest using a low-level C-14 pulse-chase labeling technique. Glob Chang Biol 13:466–477. doi:10.1111/j.1365-2486.2006.01300.x

    Article  Google Scholar 

  • Dilkes NB, Jones DL, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiol 134:706–715

    Article  CAS  PubMed  PubMed Central  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. doi:10.1111/gcb.12816

    Article  PubMed  Google Scholar 

  • Gordon AJ, Ryle GJA, Powell CE, Mitchell D (1980) Export, mobilization, and respiration of assimilates in uniculm barley during light and darkness. J Exp Bot 31:461–473

    Article  Google Scholar 

  • Gregory PJ, Atwell BJ (1991) The fate of carbon in pulse-labeled crops of barley and wheat. Plant Soil 136:205–213

    Article  CAS  Google Scholar 

  • Heldt HW, Piechulla B (2008) Pflanzenbiochemie. Spectrum Akademischer Verlag, Heidelberg

  • Hoch G (2007) Cell wall hemicelluloses as mobile carbon stores in non-reproductive plant tissues. Funct Ecol 21:823–834

    Article  Google Scholar 

  • Kardol P, De Deyn GB, Laliberte E, Mariotte P, Hawkes CV (2013) Biotic plant-soil feedbacks across temporal scales. J Ecol 101:309–315. doi:10.1111/1365-2745.12046

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Rev J Plant Nutr Soil Sci 163:421–431

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Ehrensberger H, Stahr K (2001) Carbon partitioning and below-ground translocation by lolium perenne. Soil Biol Biochem 33:61–74

    Article  CAS  Google Scholar 

  • Kvålseth TO (1985) Cautionary note about R2. Am Stat 39:279–285

    Google Scholar 

  • Lambers H, Chapin III FS, Pons TL (2008) Plant Physiological Ecology, 2nd edn. Springer

  • Lattanzi FA, Schnyder H, Thornton B (2005) The sources of carbon and nitrogen supplying leaf growth: Assessment of the role of stores with compartmental models. Plant Physiol 137:383–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmeier CA, Lattanzi FA, Schaeufele R, Wild M, Schnyder H (2008) Root and shoot respiration of perennial ryegrass are supplied by the same substrate pools: Assessment by dynamic C-13 labeling and compartmental analysis of tracer kinetics. Plant Physiol 148:1148–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmeier CA, Lattanzi FA, Schaeufele R, Schnyder H (2010) Nitrogen deficiency increases the residence time of respiratory carbon in the respiratory substrate supply system of perennial ryegrass. Plant Cell Environ 33:76–87

    CAS  PubMed  Google Scholar 

  • Lemoine R, La Camera S, Atanassova R, Ddaldchamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thvenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272. doi:10.3389/fpls.2013.00272

    Article  PubMed  PubMed Central  Google Scholar 

  • MacRobbie E (1971) Phloem translocation - facts and mechanisms - comparative survey. Biol Rev Camb Philos Soc 46:429–481

    Article  Google Scholar 

  • Meharg AA (1994) A critical-review of labeling techniques used to quantify rhizosphere carbon-flow. Plant Soil 166:55–62

    Article  CAS  Google Scholar 

  • Meng F, Dungait JAJ, Zhang X, He M, Guo Y, Wu W (2013) Investigation of photosynthate-C allocation 27 days after 13C-pulse labeling of Zea mays L. at different growth stages. Plant Soil 373:755–764

    Article  CAS  Google Scholar 

  • Milchunas D (2009) Estimating root production: Comparison of 11 methods in shortgrass steppe and review of biases. Ecosystems 12:1381–1402

    Article  CAS  Google Scholar 

  • Millenaar FF, Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5:2–15

    Article  CAS  Google Scholar 

  • Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396

    Article  CAS  Google Scholar 

  • Nguyen C, Todorovic C, Robin C, Christophe A, Guckert A (1999) Continuous monitoring of rhizosphere respiration after labelling of plant shoots with (CO2)-C-14. Plant Soil 212:191–201

    Article  CAS  Google Scholar 

  • Oikawa PY, Grantz DA, Chatterjee A, Eberwein JE, Allsman LA, Jenerette GD (2014) Unifying soil respiration pulses, inhibition, and temperature hysteresis through dynamics of labile soil carbon and O2. J Geophys Res Biogeosci 119:521–536. doi:10.1002/2013JG002434

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Qureshi RM, Fritz P, Drimmie RJ (1985) The use of CO2 absorbers for the determination of specific 14C activities. Int J Appl Radiat Isot 36:165–170

  • 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. doi:10.1007/s11104-016-3006-y

  • Richardson AD, Carbone MS, Huggett BA, Furze ME, Czimczik CI, Walker JC, Xu X, Schaberg PG, Murakami P (2015) Distribution and mixing of old and new nonstructural carbon in two temperate trees. New Phytologist 206:590–597. doi:10.1111/nph.13273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauerbeck D, Johnen B, Six R (1976) Respiration, decomposition and excretion of wheat roots during their development. Landwirtschaftliche Forschung Sonderheft 32:49–58

    CAS  Google Scholar 

  • Schnyder H, Gillenberg C, Hinz J (1993) Fructan contents and dry-matter deposition in different tissues of the wheat-grain during development. Plant Cell Environ 16:179–187

    Article  CAS  Google Scholar 

  • Schopfer P, Brennecke A (2006) Pflanzenphysiologie elsevier. Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Sey BK, Manceur AM, Whalen JK, Gregorich EG, Rochette P (2010) Root-derived respiration and nitrous oxide production as affected by crop phenology and nitrogen fertilization. Plant Soil 326:369–379

    Article  CAS  Google Scholar 

  • Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149

    Article  CAS  PubMed  Google Scholar 

  • Stewart DPC, Metherell AK (1999) Carbon C-13 uptake and allocation in pasture plants following field pulse-labelling. Plant Soil 210:61–73

    Article  CAS  Google Scholar 

  • Swinnen J, Van Veen JA, Merckx R (1994a) C-14 pulse-labeling of field-grown spring wheat - an evaluation of its use in rhizosphere carbon budget estimations. Soil Biol Biochem 26:161–170

    Article  Google Scholar 

  • Swinnen J, Van Veen JA, Merckx R (1994b) Rhizosphere carbon fluxes in field-grown spring wheat - model calculation based on C-14 partitioning after pulse-labeling. Soil Biol Biochem 26:171–182

    Article  Google Scholar 

  • Thome U, Kuhbauch W (1985) Change in the carbohydrate pattern in the cell content of wheat stems during grain-filling. J Agron Crop Sci 155:253–260

    CAS  Google Scholar 

  • Trumbore S (2000) Age of soil organic matter and soil respiration: Radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411. doi:10.2307/2641102

    Article  Google Scholar 

  • Turnbull MH, Whitehead D, Tissue DT, Schuster WSF, Brown KJ, Grifin KL (2001) Responses of leaf respiration to temperature and leaf characteristics in three deciduous tree species vary with site water availability. Tree Physiol 21:571–578

    Article  CAS  PubMed  Google Scholar 

  • Wardlaw IF, Willenbrink J (2000) Mobilization of fructan reserves and changes in enzyme activities in wheat stems correlate with water stress during kernel filling. New Phytol 148:413–422

    Article  CAS  Google Scholar 

  • Warembourg FR, Estelrich HD (2000) Towards a better understanding of carbon flow in the rhizosphere: a time-dependent approach using carbon-14. Biol Fert Soils 30:528–534

    Article  CAS  Google Scholar 

  • Warembourg FR, Estelrich HD (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

    Article  CAS  Google Scholar 

  • Werth M, Kuzyakov Y (2008) Root-derived carbon in soil respiration and microbial biomass determined by C-14 and C-13. Soil Biol Biochem 40:625–637

    Article  CAS  Google Scholar 

  • Xu JG, Juma NG (1993) Aboveground and belowground transformation of photosynthetically fixed carbon by 2 barley (Hordeum vulgare L.) cultivars in a typic cryoboroll. Soil Biol Biochem 25:1263–1272

    Article  Google Scholar 

  • Yasumura Y (2009) The effect of altered sink-source relations on photosynthetic traits and matter transport during the phase of reproductive growth in the annual herb chenopodium album. Photosynthetica 47:263–270

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Evelyn Becker from the Helmholtz Centre for Environmental Research (UFZ) in Leipzig, Germany, for chemical fractionation of the plant material and Christine Ewald, Krystyna Herrendorf, and Susanne Remus from the Leibniz Center for Agricultural Landscape Research (ZALF) in Müncheberg, Germany, for preparing the soil, root and shoot samples. In addition, we thank the DFG for providing financial support.

Author information

Authors and Affiliations

  1. Institute for Landscape Biogeochemistry, Leibniz Center for Agricultural Landscape Research (ZALF), Müncheberg, Germany

    Rainer Remus & Jürgen Augustin

  2. Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia

    Katja Hüve

  3. Helmholtz Centre for Environmental Research (UFZ), Leipzig, Germany

    Jürgen Pörschmann

Authors
  1. Rainer Remus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katja Hüve
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jürgen Pörschmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jürgen Augustin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rainer Remus.

Additional information

Responsible Editor: Johan Six.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Remus, R., Hüve, K., Pörschmann, J. et al. Determining the timepoint when 14C tracer accurately reflect photosynthate use in the plant-soil system. Plant Soil 408, 457–474 (2016). https://doi.org/10.1007/s11104-016-3002-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3002-2

Keywords

Search

Navigation